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Urbanization, industrialization, and intensification of agriculture have led to considerable heavy metal pollution across the globe, harming our ecosystems. Concentrations of arsenic (As), cadmium (Cd), copper (Cu), and lead (Pb) have been analysed in 249 eggshells collected between 2006 and 2021 from 83 female Common Cranes (Grus grus) nesting within north-eastern Germany. Information on the presence of trace elements in cranes from Europe and their potential adverse effects on the reproduction are largely missing. Only Cu and Pb were found to be present in eggshell samples. Levels of both metals did not exceed concentrations considered potentially toxic in birds and unhatched eggs did not contain higher metal concentrations compared to eggshell residues from hatched eggs. Statistical analysis revealed that trace element concentrations decreased significantly over the course of the study period. The ban of leaded gasoline in the early twenty-first century and strict limitations of heavy metal-based biocontrol products are likely responsible for this decrease over the years. However, as Cu levels gradually increase with increasing proportions of agricultural areas within the cranes’ home ranges, we suggest that considerable amounts of Cu originating from agricultural practises are still being released into the environment. We found no increase in metal concentrations in eggshells with increasing female age, suggesting that heavy metals do not accumulate in the circulatory systems of the adults over time. This study is the first to assess heavy metal contamination in Common Cranes and indicates the suitability of crane’s eggshells as bioindicator for monitoring environmental pollution.
Comparative neuroanatomy of the central nervous system in web-building and cursorial hunting spiders
(2023)
Spiders (Araneae) include cursorial species that stalk their prey and more stationary species that use webs for prey capture. While many cursorial hunting spiders rely on visual cues, web-building spiders use vibratory cues (mechanosensation) for prey capture. We predicted that the differences in primary sensory input between the species are mirrored by differences in the morphology/architecture of the central nervous system (CNS). Here, we investigated the CNS anatomy of four spider species, two cursorial hunters Pardosa amentata (Lycosidae) and Marpissa muscosa (Salticidae), and two web-building hunters Argiope bruennichi (Araneidae) and Parasteatoda tepidariorum (Theridiidae). Their CNS was analyzed using Bodian silver impregnations, immunohistochemistry, and microCT analysis. We found that there are major differences between species in the secondary eye pathway of the brain that pertain to first-order, second-order, and higher order brain centers (mushroom bodies [MB]). While P. amentata and M. muscosa have prominent visual neuropils and MB, these are much reduced in the two web-building species. Argiope bruennichi lacks second-order visual neuropils but has specialized photoreceptors that project into two distinct visual neuropils, and P. tepidariorum lacks MB, suggesting that motion vision might be absent in this species. Interestingly, the differences in the ventral nerve cord are much less pronounced, but the web-building spiders have proportionally larger leg neuropils than the cursorial spiders. Our findings suggest that the importance of visual information is much reduced in web-building spiders, compared to cursorial spiders, while processing of mechanosensory information requires the same major circuits in both web-building and cursorial hunting spiders.
Animals face strong environmental variability even on short time scales particularly in shallow coastal habitats, forcing them to permanently adjust their metabolism. Respiration rates of aquatic ectotherms are directly influenced by water temperature, whereas ingestion rates might additionally be influenced by behavior. We aim to understand how respiration and ingestion rates of an aquatic invertebrate respond to changing temperature during a diurnal thermal fluctuation cycle and how both processes are related. We studied the benthopelagic mysid Neomysis integer as an important food web component of coastal ecosystems. Mysids were collected at the southern Baltic Sea coast and exposed in the laboratory to either constant temperature of 15°C or daily temperature fluctuation of 15 ± 5°C. Short-term (1–2 h) respiration and ingestion rates were measured at four equidistant time points within 24 h and did not differ among time points at constant temperature, but differed among time points in the fluctuating treatment. Respiration was highest at the thermal maximum and lowest at the thermal minimum. Ingestion rates showed the opposite pattern under fluctuation, likely due to differences in underlying thermal performance curves. When temperature transited the average, the direction of temperature change influenced the animals' response in respiration and ingestion rates differently. Our results suggest that respiration is not only instantaneously affected by temperature, but also influenced by the previously experienced direction of thermal change. Our experiment, using an important non-model organism, delivered new insights on the relationship between the crucial organismal processes ingestion and respiration under thermal variability.
In mandibulate arthropods, the primary olfactory centers, termed olfactory lobes in crustaceans, are typically organized in distinct fields of dense synaptic neuropils called olfactory glomeruli. In addition to olfactory sensory neuron terminals and their postsynaptic efferents, the glomeruli are innervated by diverse neurochemically distinctive interneurons. The functional morphology of the olfactory glomeruli is understudied in crustaceans compared with insects and even less well understood and described in a particular crustacean subgroup, the Peracarida, which embrace, for example, Amphipoda and Isopoda. Using immunohistochemistry combined with confocal laser scanning microscopy, we analyzed the neurochemistry of the olfactory pathway in the amphipod Parhyale hawaiensis. We localized the biogenic amines serotonin and histamine as well as the neuropeptides RFamide, allatostatin, orcokinin, and SIFamide. As for other classical neurotransmitters, we stained for γ-aminobutyric acid and glutamate decarboxylase and used choline acetyltransferase as indicator for acetylcholine. Our study is another step in understanding principles of olfactory processing in crustaceans and can serve as a basis for understanding evolutionary transformations of crustacean olfactory systems.
Background
The ‘wallflower’ hypothesis proposes females mate indiscriminately to avoid reproductive delays. Post-copulatory mechanisms may then allow ‘trading up’, favouring paternity of future mates. We tested links between pre- and post-copulatory choice in Latrodectus geometricus female spiders paired sequentially with two males. These females copulate as adults or as subadults and store sperm in paired spermathecae. Choosy adults have a higher risk of delays to reproduction than subadults.
Results
We predicted low pre-copulatory, but high post-copulatory choice at first matings for adults and the opposite for subadults. At second matings, we expected all females would prefer males superior to their first. We found all females mated indiscriminately at their first pairing, but in contrast to subadults, adults usually allowed only a single insertion (leaving one of their paired spermatheca empty); a mechanism of post-copulatory choosiness. Adult-mated females were more likely to remate than subadult-mated females when they became adults, showing a preference for larger males, while subadult-mated females tended to prefer males of greater size-corrected mass.
Conclusions
Our results show that the ‘wallflower’ effect and ‘trading up’ tactics can be utilized at different life stages, allowing females to employ choice even if rejecting males is costly.
Animals often respond to climate change with changes in morphology, e.g., shrinking body size with increasing temperatures, as expected by Bergmann’s rule. Because small body size can have fitness costs for individuals, this trend could threaten populations. Recent studies, however, show that morphological responses to climate change and the resulting fitness consequences cannot be generalized even among related species. In this long-term study, we investigate the interaction between ambient temperature, body size and survival probability in a large number of individually marked wild adult female Natterer’s bats (Myotis nattereri). We compare populations from two geographical regions in Germany with a different climate. In a sliding window analysis, we found larger body sizes in adult females that were raised in warmer summers only in the northern population, but not in the southern population that experienced an overall warmer climate. With a capture-mark-recapture approach, we showed that larger individuals had higher survival rates, demonstrating that weather conditions in early life could have long-lasting fitness effects. The different responses in body size to warmer temperatures in the two regions highlight that fitness-relevant morphological responses to climate change have to be viewed on a regional scale and may affect local populations differently.
Flies form high-density associations with human settlements and groups of nonhuman primates and are implicated in transmitting pathogens. We investigate the movement of nonhuman primate-associated flies across landscapes surrounding Kibale National Park, Uganda, using a mark–recapture experiment. Flies were marked in nine nonhuman primate groups at the forest edge (x̄ = 929 flies per group), and we then attempted to recapture them in more anthropized areas (50 m, 200 m and 500 m from where marked; 2–21 days after marking). Flies marked in nonhuman primate groups were recaptured in human areas (19/28,615 recaptured). Metabarcoding of the flies in nonhuman primate groups revealed the DNA of multiple eukaryotic primate parasites. Taken together, these results demonstrate the potential of flies to serve as vectors between nonhuman primates, livestock and humans at this biodiverse interface.
How well populations can cope with global warming will often depend on the evolutionary potential and plasticity of their temperature-sensitive, fitness-relevant traits. In Bechstein's bats (Myotis bechsteinii), body size has increased over the last decades in response to warmer summers. If this trend continues it may threaten populations as larger females exhibit higher mortality. To assess the evolutionary potential of body size, we applied a Bayesian ‘animal model’ to estimate additive genetic variance, heritability and evolvability of body size, based on a 25-year pedigree of 332 wild females. Both heritability and additive genetic variance were reduced in hot summers compared to average and cold summers, while evolvability of body size was generally low. This suggests that the observed increase in body size was mostly driven by phenotypic plasticity. Thus, if warm summers continue to become more frequent, body size likely increases further and the resulting fitness loss could threaten populations.
Haematophagous leeches express a broad variety of secretory proteins in their salivary glands, among them are hirudins and hirudin-like factors. Here, we describe the identification, molecular and initial functional characterization of Tandem-Hirudin (TH), a novel salivary gland derived factor identified in the Asian medicinal leech, Hirudinaria manillensis. In contrast to the typical structure of hirudins, TH comprises two globular domains arranged in a tandem-like orientation and lacks the elongated C-terminal tail. Similar structures of thrombin inhibitors have so far been identified only in kissing bugs and ticks. Expression of TH was performed in both cell-based and cell-free bacterial systems. A subsequent functional characterization revealed no evidence for a thrombin-inhibitory potency of TH.
How organisms that are part of the same trophic network respond to environmental variability over small spatial scales has been studied in a multitude of systems. Prevailing theory suggests a large role for plasticity in key traits among interacting species that allows matching of life cycles or life‐history traits across environmental gradients, for instance insects tracking host‐plant phenology across variable environments (Posledovich et al. 2018). A key aspect that remains understudied is the extent of intrapopulation variability in plasticity and whether stressful conditions canalize plasticity to an optimal level, or alternatively if variation in plasticity indeed could increase fitness in itself via alternative strategies. In a From the Cover article in this issue of Molecular Ecology, Kahilainen et al. (2022) investigate this issue in a classical insect study system, the metapopulation of the Glanville fritillary butterfly (Melitea cinxia) in the Åland archipelago of Finland. The authors first establish how a key host plant responds to water limitation, then quantify among‐family variation in larval growth and development across control and water‐limited host plants. Finally, they use RNA sequencing to gain mechanistic insights into some of these among‐family differences in larval performance in response to host‐plant variation, finding results suggesting the existence of heritable, intrapopulation variability in ecologically relevant plasticity. This final step represents a critically important and often overlooked component of efforts to predict sensitivity of biological systems to changing environmental conditions, since it provides a key metric of adaptive resilience present in the system.
Flies are implicated in carrying and mechanically transmitting many primate pathogens. We investigated how fly associations vary across six monkey species (Cercopithecus ascanius, Cercopithecus mitis, Colobus guereza, Lophocebus albigena, Papio anubis, and Piliocolobus tephrosceles) and whether monkey group size impacts fly densities. Fly densities were generally higher inside groups than outside them, and considering data from these primate species together revealed that larger groups harbored more flies. Within species, this pattern was strongest for colobine monkeys, and we speculate this might be due to their smaller home ranges, suggesting that movement patterns may influence fly–primate associations. Fly associations increase with group sizes and may thus represent a cost to sociality.
Animal species differ considerably in longevity. Among mammals, short-lived species such as shrews have a maximum lifespan of about a year, whereas long-lived species such as whales can live for more than two centuries. Because of their slow pace of life, long-lived species are typically of high conservation concern and of special scientific interest. This applies not only to large mammals such as whales, but also to small-sized bats and mole-rats. To understand the typically complex social behavior of long-lived mammals and protect their threatened populations, field studies that cover substantial parts of a species’ maximum lifespan are required. However, long-term field studies on mammals are an exception because the collection of individualized data requires considerable resources over long time periods in species where individuals can live for decades. Field studies that span decades do not fit well in the current career and funding regime in science. This is unfortunate, as the existing long-term studies on mammals yielded exciting insights into animal behavior and contributed data important for protecting their populations. Here, I present results of long-term field studies on the behavior, demography, and life history of bats, with a particular focus on my long-term studies on wild Bechstein’s bats. I show that long-term studies on individually marked populations are invaluable to understand the social system of bats, investigate the causes and consequences of their extraordinary longevity, and assess their responses to changing environments with the aim to efficiently protect these unique mammals in the face of anthropogenic global change.
The Common Tern (Sterna hirundo) is one of Germany’s farthest migrating bird species. Ringing studies have shown the use of the East Atlantic flyway, and according to their main wintering areas at the western and southern African coasts, German and European Common Tern populations have been divided into two allohiemic groups. However, first ring recoveries of German Common Terns in Israel indicated that some of the birds breeding in eastern Germany cross central Europe and migrate along the eastern African coast. To investigate the migratory behavior of Common Terns from East Germany, we fitted 40 Common Terns breeding in a colony at the German Baltic coast with light-level geolocators. Twenty-four loggers with analyzable datasets could be retrieved, revealing two different migratory strategies within one population. Seventeen individuals (70.83%) used the eastern Atlantic flyway and spent the winter at the western African coast, the Gulf of Guinea and the southern African coast, while the other individuals (n = 7; 29.17%) crossed central Europe, migrated along the eastern African coast and overwintered in the Mozambique Channel and South African coast. We, therefore, suggest to add a third allohiemic group to complement the picture of European Common Tern migration. Moreover, our results provide new knowledge and open new questions, which can be used for future studies regarding the evolution of different migratory strategies and its consequences in relation to climate change.
Primary producer communities are often growth-limited by essential nutrients such as nitrogen (N) and phosphorus (P). The magnitude of limitation and whether N, P or both elements are limiting autotroph growth depends on the supply and ratios of these essential nutrients. Previous studies identified single, serial or co-limitation as predominant limitation outcomes in autotroph communities by factorial nutrient additions. Little is known about potential consequences of such scenarios for herbivores and whether their growth is primarily affected by changes in autotroph quantity or nutritional quality. We grew a community of phytoplankton species differing in various food quality aspects in experimental microcosms at varying N and P concentrations resulting in three different N:P ratios. At carrying capacity, N, P, both nutrients or none were added to reveal which nutrients were limiting. The nutrient-supplied communities were fed to the generalist herbivorous rotifer Brachionus calyciflorus to investigate how changing phytoplankton biomass and community composition affect herbivore abundance. We found phytoplankton being growth-limited either by N alone (single limitation) or serially, i.e. primarily by N and secondarily by P, altering available food quantity for rotifers. Rotifer growth showed a different response pattern compared to phytoplankton, suggesting that apart from food quantity food quality aspects played a substantial role in the transfer from primary to secondary production. The combined addition of N and P to phytoplankton had generally a positive effect on herbivore growth, whereas adding non-limiting nutrients had a rather detrimental effect probably due to stoichiometrically imbalanced food in terms of nutrient excess. Our experiment shows that adding various nutrients to primary producer communities will not always lead to increased autotroph and herbivore growth, and that differences between autotroph and herbivore responses under co-limiting conditions can be partly well explained by concepts of ecological stoichiometry theory.
Urbanization is a major contributor to the loss of biodiversity. Its rapid progress is mostly at the expense of natural ecosystems and the species inhabiting them. While some species can adjust quickly and thrive in cities, many others cannot. To support biodiversity conservation and guide management decisions in urban areas, it is important to find robust methods to estimate the urban affinity of species (i.e. their tendency to live in urban areas) and understand how it is associated with their traits. Since previous studies mainly relied on discrete classifications of species' urban affinity, often involving inconsistent assessments or variable parameters, their results were difficult to compare. To address this issue, we developed and evaluated a set of continuous indices that quantify species' urban affinity based on publicly available occurrence data. We investigated the extent to which a species' position along the urban affinity gradient depends on the chosen index and how this choice affects inferences about the relationship between urban affinity and a set of morphological, sensory and functional traits. While these indices are applicable to a wide range of taxonomic groups, we examined their performance using a global set of 356 bat species. As bats vary in sensitivity to anthropogenic disturbances, they provide an interesting case study. We found that different types of indices resulted in different rankings of species on the urban affinity spectrum, but this had little effect on the association of traits with urban affinity. Our results suggest that bat species predisposed to urban life are characterized by low echolocation call frequencies, relatively long call durations, small body size and flexibility in the selection of the roost type. We conclude that simple indices are appropriate and practical, and propose to apply them to more taxa to improve our understanding of how urbanization favours or filters species with particular traits.
Metabarcoding of invertebrate-derived DNA (iDNA) is increasingly used to describe vertebrate diversity in terrestrial ecosystems. Fly iDNA has also shown potential as a tool for detecting pathogens. Combining these approaches makes fly iDNA a promising tool for understanding the ecology and distribution of novel pathogens or emerging infectious diseases. Here, we use fly iDNA to explore the geographic distribution of Bacillus cereus biovar anthracis (Bcbva) along a gradient from the forest within Taï National Park, Côte d'Ivoire, out to surrounding villages. We tested fly pools (N = 100 pools of 5 flies) collected in the forest (N = 25 pools), along the forest edge (N = 50 pools), and near surrounding villages (N = 25 pools) for Bcbva. Using the same iDNA, we sought to reconstruct fly and mammal communities with metabarcoding, with the aim of investigating potential links with Bcbva detection. We detected Bcbva in 5/100 fly pools and positivity varied significantly across the habitat types (forest = 4/25, edge = 1/50, village = 0/25). It was possible to culture Bcbva from all positive fly pools, confirming their positivity, while sequencing of their whole genomes revealed a considerable portion of known genomic diversity for this pathogen. iDNA generated data about the mammal and fly communities in these habitats, revealing the highest mammal diversity in the forest and considerable changes in fly community composition along the gradient. Bcbva host range estimates from fly iDNA were largely identical to the results of long-term carcass monitoring efforts in the region. We show that fly iDNA can generate data on the geographic distribution and host range of a pathogen at kilometer scales, as well as reveal the pathogen's phylogenetic diversity. Our results highlight the power of fly iDNA for mammal biomonitoring and pathogen surveillance.
Extra-organismal DNA (eoDNA) from material left behind by organisms (noninvasive DNA, e.g., feces, hair) or from environmental samples (eDNA, e.g., water, soil) is a valuable source of genetic information. However, the relatively low quality and quantity of eoDNA, which can be further degraded by environmental factors, results in reduced amplification and sequencing success. This is often compensated for through cost- and time-intensive replications of genotyping/sequencing procedures. Therefore, system- and site-specific quantifications of environmental degradation are needed to maximize sampling efficiency (e.g., fewer replicates, shorter sampling durations), and to improve species detection and abundance estimates. Using 10 environmentally diverse bat roosts as a case study, we developed a robust modeling pipeline to quantify the environmental factors degrading eoDNA, predict eoDNA quality, and estimate sampling-site-specific ideal exposure duration. Maximum humidity was the strongest eoDNA-degrading factor, followed by exposure duration and then maximum temperature. We also found a positive effect when hottest days occurred later. The strength of this effect fell between the strength of the effects of exposure duration and maximum temperature. With those predictors and information on sampling period (before or after offspring were born), we reliably predicted mean eoDNA quality per sampling visit at new sites with a mean squared error of 0.0349. Site-specific simulations revealed that reducing exposure duration to 2–8 days could substantially improve eoDNA quality for future sampling. Our pipeline identified high humidity and temperature as strong drivers of eoDNA degradation even in the absence of rain and direct sunlight. Furthermore, we outline the pipeline's utility for other systems and study goals, such as estimating sample age, improving eDNA-based species detection, and increasing the accuracy of abundance estimates.
BatNet: a deep learning-based tool for automated bat species identification from camera trap images
(2023)
Automated monitoring technologies can increase the efficiency of ecological data collection and support data-driven conservation. Camera traps coupled with infrared light barriers can be used to monitor temperate-zone bat assemblages at underground hibernacula, where thousands of individuals of multiple species can aggregate in winter. However, the broad-scale adoption of such photo-monitoring techniques is limited by the time-consuming bottleneck of manual image processing. Here, we present BatNet, an open-source, deep learning-based tool for automated identification of 13 European bat species from camera trap images. BatNet includes a user-friendly graphical interface, where it can be retrained to identify new bat species or to create site-specific models to improve detection accuracy at new sites. Model accuracy was evaluated on images from both trained and untrained sites, and in an ecological context, where community- and species-level metrics (species diversity, relative abundance, and species-level activity patterns) were compared between human experts and BatNet. At trained sites, model performance was high across all species (F1-score: 0.98–1). At untrained sites, overall classification accuracy remained high (96.7–98.2%), when camera placement was comparable to the training images (<3 m from the entrance; <45° angle relative to the opening). For atypical camera placements (>3 m or >45° angle), retraining the detector model with 500 site-specific annotations achieved an accuracy of over 95% at all sites. In the ecological case study, all investigated metrics were nearly identical between human experts and BatNet. Finally, we exemplify the ability to retrain BatNet to identify a new bat species, achieving an F1-score of 0.99 while maintaining high classification accuracy for all original species. BatNet can be implemented directly to scale up the deployment of camera traps in Europe and enhance bat population monitoring. Moreover, the pretrained model can serve as a baseline for transfer learning to automatize the image-based identification of bat species worldwide.
Introduction: At the cellular level, acute temperature changes alter ionic conductances, ion channel kinetics, and the activity of entire neuronal circuits. This can result in severe consequences for neural function, animal behavior and survival. In poikilothermic animals, and particularly in aquatic species whose core temperature equals the surrounding water temperature, neurons experience rather rapid and wide-ranging temperature fluctuations. Recent work on pattern generating neural circuits in the crustacean stomatogastric nervous system have demonstrated that neuronal circuits can exhibit an intrinsic robustness to temperature fluctuations. However, considering the increased warming of the oceans and recurring heatwaves due to climate change, the question arises whether this intrinsic robustness can acclimate to changing environmental conditions, and whether it differs between species and ocean habitats.
Methods: We address these questions using the pyloric pattern generating circuits in the stomatogastric nervous system of two crab species, Hemigrapsus sanguineus and Carcinus maenas that have seen a worldwide expansion in recent decades.
Results and discussion: Consistent with their history as invasive species, we find that pyloric activity showed a broad temperature robustness (>30°C). Moreover, the temperature-robust range was dependent on habitat temperature in both species. Warm-acclimating animals shifted the critical temperature at which circuit activity breaks down to higher temperatures. This came at the cost of robustness against cold stimuli in H. sanguineus, but not in C. maenas. Comparing the temperature responses of C. maenas from a cold latitude (the North Sea) to those from a warm latitude (Spain) demonstrated that similar shifts in robustness occurred in natural environments. Our results thus demonstrate that neuronal temperature robustness correlates with, and responds to, environmental temperature conditions, potentially preparing animals for changing ecological conditions and shifting habitats.
Background
Haemosporidian parasites of the genus Polychromophilus infect bats worldwide. They are vectored by obligate ectoparasitic bat flies of the family Nycteribiidae. Despite their global distribution, only five Polychromophilus morphospecies have been described to date. The two predominant species, Polychromophilus melanipherus and Polychromophilus murinus, are broadly distributed and mainly infect miniopterid and vespertilionid bats, respectively. In areas where species from different bat families aggregate together, the infection dynamics and ability of either Polychromophilus species to infect other host families is poorly characterized.
Methods
We collected 215 bat flies from two bat species, Miniopterus schreibersii and Rhinolophus ferrumequinum, which sometimes form mixed clusters in Serbia. Miniopterus schreibersii is known to be frequently infected with P. melanipherus, whereas R. ferrumequinum has been observed to be incidentally infected with both Polychromophilus species. All flies were screened for Polychromophilus infections using a PCR targeting the haemosporidian cytb gene. Positive samples were subsequently sequenced for 579 bp of cytochrome b (cytb) and 945 bp of cytochrome oxidase subunit 1 (cox1).
Results
Polychromophilus melanipherus DNA was detected at six out of nine sampling locations and in all three examined bat fly species collected from M. schreibersii (Nycteribia schmidlii, n = 21; Penicillidia conspicua, n = 8; Penicillidia dufourii, n = 3). Four and five haplotypes were found for cytb and cox1, respectively. Evidence for multiple Polychromophilus haplotypes was found in 15 individual flies. These results point to a high diversity of P. melanipherus parasites in Miniopterus hosts and efficient transmission throughout the study area. A single Phthiridium biarticulatum bat fly collected from R. ferrumequinum screened positive for P. melanipherus, but only yielded a partial cox1 sequence fragment. Nevertheless, this result suggests that secondary hosts (both bat and fly species) are regularly confronted with this parasite.
Conclusions
The results of this study provide new insights into the prevalence and distribution of Polychromophilus parasites in European bats and their nycteribiid vectors. The use of bat flies for the non-invasive investigation of Polychromophilus infections in bat populations has proven to be efficient and thus represents an alternative for large-scale studies of infections in bat populations without the need to invasively collect blood from bats.
Lacewings (Neuroptera) have predatory larvae with highly specialised mouthparts. Larvae of many groups within Neuroptera are well represented as fossils preserved in ambers; however, larvae of some groups are less often reported in the literature. Here we report such a rare case, a larva of the group Hemerobiidae, an aphidlion, preserved in a piece of Eocene Baltic amber (about 40 million years old). It is preserved together with three possible prey items, wingless aphids, most likely representatives of Germaraphis (or at least closely related to this group). The aphidlion can be identified based on the morphology of the antennae, simple curved and toothless stylets, well developed labial palps, and the absence of other mouth-part structures such as a protruding labrum or maxillary palps. A long, club-shaped distal element of the labial palps identifies the specimen as a larva of Hemerobiidae. The aphids can be identified based on their very long, beak-like mouth parts. This find is, to our knowledge, the first example of a lacewing larva preserved together with its potential prey. We briefly discuss other cases in which fossils preserved in amber allow us to reconstruct aspects of behaviour and interactions of fossil lacewing larvae.
Copulatory mechanics of ghost spiders reveals a new self-bracing mechanism in entelegyne spiders
(2023)
Spiders evolved a distinctive sperm transfer system, with the male copulatory organs located on the tarsus of the pedipalps. In entelegyne spiders, these organs are usually very complex and consist of various sclerites that not only allow the transfer of the sperm themselves but also provide a mechanical interlock between the male and female genitalia. This interlocking can also involve elements that are not part of the copulatory organ such as the retrolateral tibial apophysis (RTA)—a characteristic of the most diverse group of spiders (RTA clade). The RTA is frequently used for primary locking i.e., the first mechanical engagement between male and female genitalia. Despite its functional importance, some diverse spider lineages have lost the RTA, but evolved an apophysis on the femur instead. It can be hypothesized that this femoral apophysis is a functional surrogate of the RTA during primary locking or possibly serves another function, such as self-bracing, which involves mechanical interaction between male genital structures themselves to stabilize the inserted pedipalp. We tested these hypotheses using ghost spiders of the genus Josa (Anyphaenidae). Our micro-computed tomography data of cryofixed mating pairs show that the primary locking occurs through elements of the copulatory organ itself and that the femoral apophysis does not contact the female genitalia, but hooks to a projection of the copulatory bulb, representing a newly documented self-bracing mechanism for entelegyne spiders. Additionally, we show that the femoral self-bracing apophysis is rather uniform within the genus Josa. This is in contrast to the male genital structures that interact with the female, indicating that the male genital structures of Josa are subject to different selective regimes.
Geometric regularity of spider webs has been intensively studied in orb‐weaving spiders, although it is not exclusive of orb weavers. Here, we document the geometrically regular, repetitive elements in the webs of the non‐orb‐weaving groups Leptonetidae and Telemidae for the first time. Similar to orb weavers, we found areas with regularly spaced parallel lines in the webs of Calileptoneta helferi, Sulcia sp., and cf. Pinelema sp. Furthermore, we provide a detailed account of the regular webs of Ochyrocera (Ochyroceratidae). The sections of the web with regularly disposed parallel lines are built as U‐shaped modules reminiscent of orb webs. It has been suggested that the regularly spaced parallel lines in the webs of Ochyroceratidae and Psilodercidae may be produced in a single sweep of their posterior lateral spinnerets, which have regularly spaced aciniform gland spigots, perhaps involving expansion of the spinnerets. To test this hypothesis, we compared the spacing between parallel lines with the spacing between spigots, searched for expansible membranes in the spinnerets, and examined the junctions of regularly spaced lines. The distance between parallel lines was 10–20 times the distance between spigots, and we found no expansible membranes, and the intersection of parallel lines are cemented, which opposes the single sweep hypothesis. Furthermore, we found cues of viscid silk in the parallel lines of the psilodercid Althepus and broadened piriform gland spigots that may be responsible of its production. Finally, we evaluated the presence or absence of geometrically regular web elements across the spider tree of life. We found reports of regular webs in 31 spider families, including 20 families that are not orb weavers and hypothesize that the two basic aspects of regularity (parallel lines spaced at regular intervals, and radial lines spaced at regular angles) probably appeared many times in the evolution of spiders.
Background
Hibernation allows species to conserve energy and thereby bridge unfavorable environmental conditions. At the same time, hibernation imposes substantial ecological and physiological costs. Understanding how hibernation timing differs within and between species can provide insights into the underlying drivers of this trade-off. However, this requires individualized long-term data that are often unavailable. Here, we used automatic monitoring techniques and a reproducible analysis pipeline to assess the individualized hibernation phenology of two sympatric bat species. Our study is based on data of more than 1100 RFID-tagged Daubenton’s bats (Myotis daubentonii) and Natterer’s bats (Myotis nattereri) collected over seven years at a hibernaculum in Germany. We used linear mixed models to analyze species-, sex- and age-specific differences in entrance, emergence and duration of the longest continuous period spent in the hibernaculum.
Results
Overall, Daubenton’s bats entered the hibernaculum earlier and emerged later than Natterer’s bats, resulting in a nearly twice as long hibernation duration. In both species, adult females entered earlier and emerged from hibernation later than adult males. Hibernation duration was shorter for juveniles than adults with the exception of adult male Natterer’s bats whose hibernation duration was shortest of all classes. Finally, hibernation timing differed among years, but yearly variations in entrance and emergence timing were not equally shifted in both species.
Conclusions
Our results suggest that even in sympatric species, and across sex and age classes, hibernation timing may be differentially affected by environmental conditions. This highlights the necessity of using individualized information when studying the impact of changing environments on hibernation phenology.
Background
Pycnogonida (sea spiders) is the sister group of all other extant chelicerates (spiders, scorpions and relatives) and thus represents an important taxon to inform early chelicerate evolution. Notably, phylogenetic analyses have challenged traditional hypotheses on the relationships of the major pycnogonid lineages (families), indicating external morphological traits previously used to deduce inter-familial affinities to be highly homoplastic. This erodes some of the support for phylogenetic information content in external morphology and calls for the study of additional data classes to test and underpin in-group relationships advocated in molecular analyses. In this regard, pycnogonid internal anatomy remains largely unexplored and taxon coverage in the studies available is limited.
Results
Based on micro-computed X-ray tomography and 3D reconstruction, we created a comprehensive atlas of in-situ representations of the central nervous system and midgut layout in all pycnogonid families. Beyond that, immunolabeling for tubulin and synapsin was used to reveal selected details of ganglionic architecture. The ventral nerve cord consistently features an array of separate ganglia, but some lineages exhibit extended composite ganglia, due to neuromere fusion. Further, inter-ganglionic distances and ganglion positions relative to segment borders vary, with an anterior shift in several families. Intersegmental nerves target longitudinal muscles and are lacking if the latter are reduced. Across families, the midgut displays linear leg diverticula. In Pycnogonidae, however, complex multi-branching diverticula occur, which may be evolutionarily correlated with a reduction of the heart.
Conclusions
Several gross neuroanatomical features are linked to external morphology, including intersegmental nerve reduction in concert with trunk segment fusion, or antero-posterior ganglion shifts in partial correlation to trunk elongation/compaction. Mapping on a recent phylogenomic phylogeny shows disjunct distributions of these traits. Other characters show no such dependency and help to underpin closer affinities in sub-branches of the pycnogonid tree, as exemplified by the tripartite subesophageal ganglion of Pycnogonidae and Rhynchothoracidae. Building on this gross anatomical atlas, future studies should now aim to leverage the full potential of neuroanatomy for phylogenetic interrogation by deciphering pycnogonid nervous system architecture in more detail, given that pioneering work on neuron subsets revealed complex character sets with unequivocal homologies across some families.
Whether species can cope with environmental change depends considerably on their life history. Bats have long lifespans and low reproductive rates which make them vulnerable to environmental changes. Global warming causes Bechstein’s bats (Myotis bechsteinii) to produce larger females that face a higher mortality risk. Here, we test whether these larger females are able to offset their elevated mortality risk by adopting a faster life history. We analysed an individual-based 25-year dataset from 331 RFID-tagged wild bats and combine genetic pedigrees with data on survival, reproduction and body size. We find that size-dependent fecundity and age at first reproduction drive the observed increase in mortality. Because larger females have an earlier onset of reproduction and shorter generation times, lifetime reproductive success remains remarkably stable across individuals with different body sizes. Our study demonstrates a rapid shift to a faster pace of life in a mammal with a slow life history.
Background
Pholcidae represent one of the largest and most diverse spider families and have been subject to various studies regarding behavior and reproductive biology. In contrast to the solid knowledge on phylogeny and general reproductive morphology, the primary male reproductive system is strongly understudied, as it has been addressed only for few species. Those studies however suggested a high diversity of sperm and seminal secretions across the family. To address this disparity and reconstruct the evolution of sperm traits, we investigate the primary male reproductive system of pholcid spiders by means of light, X-ray, and transmission electron microscopy using a comprehensive taxon sampling with 46 species from 33 genera, representing all five subfamilies.
Results
Our data show a high disparity of sperm morphology and seminal secretions within pholcids. We document several sperm characters that are unique for pholcids, such as a helical band (Pholcinae) or a lamellate posterior centriolar adjunct material (Modisiminae). Character mapping revealed several putative synapomorphies for individual taxa. With regard to sperm transfer forms, we found that synspermia occur only in the subfamily Ninetinae, whereas the other subfamilies have cleistospermia. In several species with cleistospermia, we demonstrate that spermatids remain fused until late stages of spermiogenesis before ultimately separating shortly before the coiling process. Additionally, we explored the previously hypothesized correlation between sperm size and minimum diameter of the spermophor in the male palpal organ. We show that synspermia differ strongly in size whereas cleistospermia are rather uniform, but neither transfer form is positively correlated with the diameter of the spermophor.
Conclusions
Our data revealed a dynamic evolution of sperm characters, with convergences across all subfamilies and a high level of homoplasy. The present diversity can be related to subfamily level and allows for assignments of specific subtypes of spermatozoa. Our observations support the idea that Ninetinae are an ancestral clade within Pholcidae that have retained synspermia and that synspermia represent the ancestral sperm transfer form of Pholcidae.
Background
Phylogenomic studies over the past two decades have consolidated the major branches of the arthropod tree of life. However, especially within the Chelicerata (spiders, scorpions, and kin), interrelationships of the constituent taxa remain controversial. While sea spiders (Pycnogonida) are firmly established as sister group of all other extant representatives (Euchelicerata), euchelicerate phylogeny itself is still contested. One key issue concerns the marine horseshoe crabs (Xiphosura), which recent studies recover either as sister group of terrestrial Arachnida or nested within the latter, with significant impact on postulated terrestrialization scenarios and long-standing paradigms of ancestral chelicerate traits. In potential support of a nested placement, previous neuroanatomical studies highlighted similarities in the visual pathway of xiphosurans and some arachnopulmonates (scorpions, whip scorpions, whip spiders). However, contradictory descriptions of the pycnogonid visual system hamper outgroup comparison and thus character polarization.
Results
To advance the understanding of the pycnogonid brain and its sense organs with the aim of elucidating chelicerate visual system evolution, a wide range of families were studied using a combination of micro-computed X-ray tomography, histology, dye tracing, and immunolabeling of tubulin, the neuropil marker synapsin, and several neuroactive substances (including histamine, serotonin, tyrosine hydroxylase, and orcokinin). Contrary to previous descriptions, the visual system displays a serial layout with only one first-order visual neuropil connected to a bilayered arcuate body by catecholaminergic interneurons. Fluorescent dye tracing reveals a previously reported second visual neuropil as the target of axons from the lateral sense organ instead of the eyes.
Conclusions
Ground pattern reconstruction reveals remarkable neuroanatomical stasis in the pycnogonid visual system since the Ordovician or even earlier. Its conserved layout exhibits similarities to the median eye pathway in euchelicerates, especially in xiphosurans, with which pycnogonids share two median eye pairs that differentiate consecutively during development and target one visual neuropil upstream of the arcuate body. Given multiple losses of median and/or lateral eyes in chelicerates, and the tightly linked reduction of visual processing centers, interconnections between median and lateral visual neuropils in xiphosurans and arachnopulmonates are critically discussed, representing a plausible ancestral condition of taxa that have retained both eye types.
Background
Asymmetries are a widespread phenomenon in otherwise bilaterally symmetric organisms, and investigation of asymmetric structures can help us gather insights into fundamental evolutionary processes such as the selection for morphological novelties caused by behavioural changes. In insects, asymmetric genitalia have evolved in almost every order, and usually it’s the sclerotized parts and most conspicuous male phallic organs that are known to exhibit asymmetries. While external copulatory organs in insects have often been subject to investigations concerning asymmetries and the evolution thereof, internal reproductive structures have received far less attention. Here we describe the internal and external male genitalia in three species of Austrophasmatidae, Mantophasmatodea, using μ-CT imaging and light microscopy. Mantophasmatodea is the most recently discovered insect order, and with 21 species described to date, it is among the smallest insect orders currently known.
Results
We confirm that male heelwalkers exhibit asymmetries in the external genitalia and associated structures, represented by asymmetric phallic lobes and cerci. Moreover, we found an extreme asymmetry within the internal male genitalia: in all adult males investigated (N = 5), the seminal vesicle, a dilatation of the vas deferens, was only developed on the right side of the male while missing on the left side.
Conclusion
The false-male-above mating position exhibited by Mantophasmatodea and especially the long copulation duration of ca. 3 days might select for this unusual absence asymmetry of the left seminal vesicle. If this holds true for all heelwalker species, this absence asymmetry constitutes another autapomorphy for Austrophasmatidae or even the insect order Mantophasmatodea.
The aquatic gastropod Theodoxus fluviatilis occurs in Europe and adjacent areas of Asia. The snail species has formed two genetically closely related subgroups, the freshwater ecotype (FW) and the brackish water ecotype (BW). Other than individuals of the FW ecotype, those of the BW ecotype survive in salinities of up to 28‰. Coastal aquatic ecosystems may be affected by climate change due to salinization. Thus, we investigated how the two Theodoxus ecotypes adjust to changes in environmental salinity, focusing on the question whether Na+/K+-ATPase or V-ATPase are regulated on the transcriptional, the translational or at the activity level under changing external salinities. Animals were gradually adjusted to extreme salinities in containers under long-day conditions and constant temperature. Whole body RNA- or protein extracts were prepared. Semi-quantitative PCR- and western blot-analyses did not reveal major changes in transcript or protein abundances for the two transporters under low or high salinity conditions. No significant changes in ATPase activities in whole body extracts of animals adjusted to high or low salinity conditions were detected. We conclude that constitutive expression of ATPases is sufficient to support osmotic and ion regulation in this species under changing salinities given the high level of tolerance with respect to changes in body fluid volume.
Shallow aquatic environments are characterized by strong environmental variability. For ectotherms, temperature is the main driver of metabolic activity, thus also shaping performance. Ingestion rates in mysids are fast responses, influenced by metabolic and behavioral activity. We examined ingestion rates of the mysid Neomysis integer, collected in the Baltic Sea, after one-week exposure to different constant and fluctuating temperature regimes (5, 10, 15, 20°C and 9 ± 5, 14 ± 5°C, respectively). To investigate possible differences between sexes, thermal performance curves (TPCs) were established for female and male mysids based on ingestion rates measured at constant temperatures. TPCs of ingestion rates at constant temperatures differed between sexes, with female mysids showing a higher total ingestion rate as well as a higher thermal optimum compared to male mysids. Females showed reduced ingestion rates when exposed to fluctuating temperatures around their thermal optimum, whereas ingestion of male mysids was not reduced when exposed to fluctuating temperatures. The observed sex-specific differences might be related to potentially higher lipid and energy demands of the females. We suggest future studies should investigate males and females to improve our understanding about impacts of environmental variability on natural populations.
Foraging behavior, neuroanatomy and neuroplasticity in cursorial and stationary hunting spiders
(2023)
The central nervous system (CNS) is the integration center for the coordination and regulation of
all body activities of animals and the source of behavioral patterns, behavioral plasticity and
personality. Understanding the anatomy and the potential for plastic changes of the CNS not only
widens the knowledge on the biology of the respective species, but also enables a more
fundamental understanding of behavioral and ecological patterns. The CNS of species with
different sensory ecologies for example, will show specific differences in the wiring of their CNS,
related to their lifestyle. Spiders are a group of mesopredators that include stationary hunting
species that build webs for prey capture, and cursorial hunting species that do not build capture
webs. These distinct lifestyles are associated with major differences in their sensory equipment,
such as size of the different eyes.
In this thesis, I aimed to answer if a cursorial mesopredator would change its behavior due to
different levels of perceived predation risk, and if this behavior would be influenced by individual
differences (chapter 1); how the visual pathways in the brain of the cursorial hunting jumping
spider Marpissa muscosa differs from that of the nocturnal cursorial hunting wandering spider
Cupiennius salei (chapter 2); to what degree the visual systems of stationary and cursorial hunting
spiders differ and whether CNS areas that process vibratory information show similar differences
(chapter 3); and finally if the CNS in stationary and cursorial hunting spiders shows different
patterns of neuroplasticity in response to sensory input and deprivation during development
(chapter 4).
In chapter 1, I found that jumping spiders adjust their foraging behavior to the perceived level of
risk. By favoring a dark over a light substrate, they displayed a background-matching strategy.
Short pulses of acute risk, produced by simulated bird overflights, had only small effects on the
behavior. Instead, a large degree of variation in behavior was due to among-individual differences
in foraging intensity. These covaried with consistent among-individual differences in activity,
forming a behavioral syndrome. Our findings highlight the importance of consistent amongindividual
differences in the behavior of animals that forage under risk. Future studies should
address the mechanisms underlying these stable differences, as well as potential fitness
consequences that may influence food-web dynamics.
In chapter 2, I found that the visual pathways in the brain of the jumping spider M. muscosa differ
from that in the wandering spider C. salei. While the pathway of the principal eyes, which are
responsible for object discrimination, is the same in both species, considerable differences occur
in the pathway of the secondary eyes, which detect movement. Notably, M. muscosa possesses
an additional second-order visual neuropil, which is integrating information from two different
secondary eyes, and may enable faster movement decisions. I also showed that the tiny posterior
median eye is connected to a first-order visual neuropil which in turn connects to the arcuate body
(a higher-order neuropil), and is thus not vestigial as suggested before. Subsequent studies should
focus on exploring the function of the posterior median eyes in different jumping spider species,
Foraging behavior, neuroanatomy, and neuroplasticity in cursorial and stationary hunting spiders
as they show considerable inter-specific size differences that may be correlated with a differing
connectivity in the brain.
In chapter 3, I described all neuropils and major tracts in the CNS of two stationary (Argiope
bruennichi and Parasteatoda tepidariorum) and two cursorial hunting spiders (Pardosa amentata
and M. muscosa). I found major differences in the visual systems of the secondary eyes between
cursorial and stationary hunting spiders, but also within the groups. A. bruennichi has specialized
retinula cells in two of the secondary eyes, which connect to different higher-order neuropils. P.
tepidariorum has only a single visual neuropil connected to all secondary eyes, and lacks
recognizable mushroom bodies. The neuroanatomy of CNS areas that process mechanosensory
information on the other hand, is remarkably similar between cursorial and stationary hunting
species. This suggests that the same major circuits are used for the processing of mechanosensory
information in both cursorial and stationary hunting spiders. Future studies on functional aspects
of sensory processing in spiders can build on the findings of our study.
In chapter 4, I found that developmental neuroplasticity in response to sensory input differs
between a cursorial (M. muscosa) and a stationary hunting spider (P. tepidariorum). While
deprivation of sensory input leads to a volume increase in several visual and mechanosensory
neuropils M. muscosa, neither sensory deprivation nor sensory enrichment had an effect on the
volume of neuropils in P. tepidariorum. However, exposure to mechanical cues during
development had an effect on the allometric scaling slope of the leg neuropils in both M. muscosa
and P. tepidariorum. Future studies should focus on the genetic and cellular basis of
developmental neuroplasticity in response to sensory input in order to explain the observed
patterns.
Increasing environmental changes primarily due to anthropogenic impacts, are affecting organisms all over the planet. In general, scientists distinguish between three different ways in which organisms can respond to environmental changes in their habitat: extinction, dispersal and adaptation. An example of organisms which are highly adaptable and can easily cope with new and changing environments are invasive species which are able to colonize new habitats with only few individuals. To successfully survive in their new environment, invasive species adapt fast to novel abiotic and biotic parameters, such as different temperature regimes. Phenotypic plasticity which enables organisms to quickly modify their phenotype to new environmental conditions, explains the success in adaptation of invasive species.
While underlying mechanisms of phenotypic plasticity are not fully understood, one possible “motor” of phenotypic plasticity is epigenetics. Especially DNA methylation could explain the fast changes of the organism’s phenotype due to plasticity when experiencing changing environments, as invasive species do. DNA methylation could even contribute to the adaptation of invasive species via phenotypic plasticity, especially with clonally reproducing species. Methods such as common garden experiments with clonally reproducing species are a useful tool to differentiate between phenotypic plasticity and genetic adaptation because the confusing effects of genetic variation are lowered in clonally reproducing species.
Our overall goal was to evaluate the genetic adaptive potential of New Zealand mud snail (Potamopyrgus antipodarum) populations from Europe since they went through an extreme bottleneck after colonizing Europe only 180-360 generations ago. Seemingly, two different clonal lineages colonized Europe because two 16 s rRNA and cytochrome b haplotypes were found across different European countries, haplotypes t and z. The NZMS is a highly successful invasive species that is nowadays nearly globally distributed. The shells of the NZMS show a habitat-dependent high variability and are a fitness-relevant trait. The high variability in shell morphology is due to both genetic variation and phenotypic plasticity. To disentangle genetic from environmental effects on the shell morphology NZMS, we conducted a common garden experiment. We kept asexually reproducing females from eleven European populations in climate cabinets with three different temperatures to produce offspring. We compared shell size and shape across three generations using the geometric morphometrics approach. Furthermore, we estimated reaction norms, maternal effects, broad-sense heritability, the coefficient of genetic variation (CVA) and evolvability (IA) in shell size and shape across different temperature conditions. Additionally, we investigated the reproductive rate of the parental generation.
Results showed that the shell morphology of the parental generation differed across populations. In contrast, the shell morphology of offspring generations became more similar. The reaction norms of the F1 generation were rather variable across the three temperatures. However, we were able to observe a haplotype-dependent pattern across the reaction norms suggesting a restricted genetic differentiation among NZMS in Europe. We detected high heritability values in size indicating a high genetic influence. Heritability values for shape were lower than in size. Generally, heritability varied slightly depending on temperature. Size seemed to have a higher evolvability than shape. However, the values of all our calculations were very low which indicates that the European NZMS populations are genetically diminished. The reproductive rate of the parental generation was rather haplotype than temperature dependent. In summary, we were able to display that the NZMS is capable to plastically adapt its shell morphology to different temperatures showing significant differences between the two haplotypes. Nevertheless, the low evolvability values indicate that little genetic variation has formed since the arrival of the NZMS in Europe and therefore, European NZMS seem to have a reduced ability to react to selection.
These results implied that phenotypic plasticity is important for the adaptation to different environmental conditions in the NZMS and maybe other molluscan species. Since classical experimental approaches can only describe the resulting phenotypes, we also intended to shed more light on the mechanistic side of environmentally induced phenotypic modifications using DNA methylation analysis. Although molluscs represent one of the most diverse taxa within the metazoan and are found in many different habitats, our knowledge of the DNA methylation in molluscs is scarce. Therefore, we aimed at deepening and summarizing our understanding about DNA methylation in molluscs. Publicly available molluscan genomic and transcriptomic data of all eight mollusc classes was downloaded to search for DNA methyltransferases (DNMTs 1-3) responsible for DNA methylation. Additionally, we estimated the normalized CpG dinucleotide content (CpG o/e) indicating the presence/absence and the frequency of DNA methylation in the genome. The CpG o/e ratio refers to the level of DNA methylation in the genome. Based on the sensitivity of methylated cytosines to mutate into thymine residues, species having a high germline methylation in genomic regions over evolutionary time, also have a lower CpG content, which is called CpG depletion. In contrary, species with a limited germline methylation in genomic regions over evolutionary time, show a higher CpG content and lack CpG depletion. The presence or absence of CpG depletion can be calculated with the CpG o/e ratio. Ultimately, the goal of our analyses was to gain insight into the evolution of methylation in molluscs.
We detected DNMTs in all eight mollusc classes and in most of the species. It is therefore plausible that the last common ancestor of molluscs has already had the enzymatic machinery which is needed for DNA methylation. However, various species did not possess the complete DNMT toolkit indicating evolutionary modification in DNA methylation. In general, we found a wide distribution of the bimodal CpG o/e pattern in six mollusc classes, resulting from CpG depletion. The genes in these groups seem to be divided into genes with a high degree of methylation and genes with a lower degree of methylation. This implies that DNA methylation seems to be rather common in molluscs. Species of Solenogastres and Monoplacophora were not or only sparsely methylated. It seems that those mollusc groups have undergone a reduction in DNA methylation. We hope that our investigations will demonstrate the lacking knowledge in epigenetics of molluscs and encourage scientist to execute and continue genetic studies on molluscs.
Emerging infectious diseases are among the greatest threats to human, animal and plant health as well as to global biodiversity. They often arise following the human-mediated transport of a pathogen beyond its natural geographic range, where host species are typically not well adapted due to a lack of co-evolutionary host-pathogen dynamics. One such pathogen is the fungus Pseudogymnoascus destructans (Pd), which causes White-Nose disease in hibernating bats. While Pd was first observed in North America where it has led to mass-mortalities in some bat species, the pathogen originates from Eurasia where infection is not associated with mortality. Most of the Pd research has focused on the invasive North American range, which likely underestimated the genetic structure of the pathogen and the role it might play in the disease dynamics.
In my work, I therefore evaluated the genetic structure of Pd in its native range with the aim of uncovering cryptic diversity and further use population genetic data to address some key ecological aspects of the disease dynamics. With an extensive reference collection of more than 5,000 isolates from 27 countries I first demonstrated strong differentiation between two monophyletic clades across several genetic measures (multi-locus genotypes, full genome long-read sequencing and Illumina NovaSeq on isolate pools). These findings are consistent with the presence of two cryptic species which are both causative agents of bat White-Nose disease (‘Pd-1’, which corresponds to P. destructans sensu stricto, and ‘Pd-2’). Both species exist in the same geographic range and co-occur in the same hibernacula (i.e., in sympatry), though with specialised host preferences. I further described the fine-scale population structure in Eurasia which revealed that most genotypes are unique to single hibernacula (more than 95% of genotypes). The associated differences in microsatellite allele frequencies among hibernacula allowed the use of assignment methods to assign the North American isolates (exclusively Pd-1) to regions in Eurasia. Hence, a region in Ukraine (Podilia) is the most likely origin of the North American introduction.
To gain further insights into the spatial and temporal dynamics of White-Nose disease on a localised scale, several hibernacula were sampled with high intensity (artificial hibernaculum in Germany and natural karst caves in Bulgaria). Low rates of Pd gene flow were observed even among closely situated hibernacula. This indicates that Pd does not remain viable on bats over summer or it would be frequently exchanged among bats (and hence hibernacula) resulting in a homogenous distribution of genotypes. Instead, bats need to become re-infected each hibernation season to explain the yearly re-occurrence of White-Nose disease. Given the distribution and richness of Pd genotypes on hibrnacula walls and infected bats of the same hibernacula, bats become infected from the hibernacula walls when they return after summer. This means that environmental reservoirs exist within hibernacula (i.e., the walls) on which Pd spores persist during bat absence and which drive the yearly re-occurrence of White-Nose disease. In an experimental setup, I confirmed the long-term viability of Pd spores on abiotic substrate for at least two years and furthermore discovered temporal variations in Pd spores’ ability to germinate. In fact, these variations followed a seasonal pattern consistent with the timing of bats absence (reduced germination) and presence (increased germination) and could indicate adaptations of Pd to the bats’ life-cycle. The infection of bats from environmental reservoirs hence seems to be a central aspect of White-Nose disease dynamics and Pd biology.
Pds ability to remain viable for extended periods outside the host increases its risk of being anthropogenically transported and might have played a role in the emergence of White-Nose disease in North America. The existence of a second species (Pd-2) poses a great additional danger to North American bats considering that its introduction there could lead to deaths and associated population declines in so-far unaffected species given what is known about differing host species preferences in Eurasian bats. Even within the native range of Pd, the movement of Pd between differentiated fungal populations could facilitate genetic exchanges (e.g., through sexual reproduction) between genetically distant genotypes. Such genetic exchanges could lead to phenotypic jumps in pathogenicity or host-species preferences and should hence be prevented.
The native range of a pathogen holds great potential to better understand the genetic and ecological basis of a (wildlife) disease. My work informs about the dangers associated with the accidental transport of Pd (and other pathogens) and highlights the need for ‘prezootic’ biosecurity-oriented strategies to prevent disease outbreaks globally. Once a pathogen has arrived in a new geographic range, and particularly if it has environmentally durable spores (as demonstrated for Pd), it will be difficult/impossible to eradicate. Furthermore, a pathogen’s ability to remain viable outside the host and infect them from environmental reservoirs has been associated with an increased risk of species extinctions and needs to be considered when designing management strategies to mitigate disease impact.
Amid the current global biodiversity crisis, being able to accurately monitor the changing state of biodiversity is essential for successful conservation actions and policy. Despite the pressing need for reliable and cost-effective monitoring methods, collecting such data remains extremely difficult for elusive species, such as temperate zone bats. Although bats are important indicators of environmental changes, monitoring bat populations is challenging because they are nocturnal, volant, small, and highly sensitive to human activities and disturbance. Thus far, population trends of temperate zone bats have been mainly based on visual surveys, including winter hibernation counts at underground sites. However, as bats may not always be roosting in visible locations within the hibernacula, it is currently unknown how these estimates relate to actual population sizes.
Infrared light barriers combined with camera traps are a novel method to monitor bats at underground sites. When installed at the entrance of hibernacula, infrared light barriers have the potential to estimate site-level population sizes more accurately than visual surveys, by counting all bats flying in and out of the site. Moreover, camera traps, consisting of a digital camera and white flash, can be used for species-level identification. However, for this new method to be applicable as a large-scale bat monitoring technique, it is important to characterize it with regard to three main criteria: is the method minimally invasive, is it accurate, and is it scalable in terms of spatial and temporal resolution? Therefore, the purpose of this thesis was to investigate the invasiveness and accuracy of this novel bat monitoring method, and to develop standardized and automated data analysis pipelines, both for the light barrier and camera trap data, to support the deployment of this method at scale.
In Publication I, we used light barrier data, infrared video recordings and acoustic data from an experimental field study to investigate whether the white flash of the camera trap has any measurable short- or long-term effect on bat activity and behavior. The flash of the camera trap was turned on and off every week at each site, which allowed us to compare the activity and behavior of bats between flash-on and flash-off nights. We found that despite the high sensitivity of bats to disturbance, they did not change their nightly activity patterns, flight direction, echolocation behavior, or long-term site use in response to the white flash of the camera trap. Based on these results, we concluded that camera traps using a white flash are a minimally invasive method for monitoring bat populations at hibernacula, providing high quality images that allows species-level identification.
In Publication II, we used infrared video surveillance to quantify the accuracy of infrared light barriers, and we described a standardized methodology to estimate population sizes and trends of hibernating bat assemblages using light barrier data. We showed that light barrier accuracy varies based on the model and location of the installation relative to the entrance, with the best combination achieving nearly perfect accuracy over the spring emergence phase. When compared to light barrier-based estimates, we found that visual counts markedly underestimated population sizes, recovering less than 10% of the bats at the most complex hibernacula. Moreover, light barrier-based population trends showed regional patterns of growth and decline that were not detectable using the visual count data. Overall, we established that the light barrier data can be used to estimate the population size and trends of hibernating bat assemblages with unprecedented accuracy and in a standardized way.
In Publication III, we described a deep learning-based tool, BatNet, that can accurately and efficiently identify bat species from camera trap images. The baseline model was trained to identify 13 European bat species or species complexes using camera trap images collected at 32 hibernation sites (i.e., trained sites). We showed that the baseline model performance was very high across all 13 bat species on trained sites, as well as on untrained sites when the camera angle and distance from the entrance were comparable to the training images. At untrained sites with more atypical camera placements, we demonstrated the ability to retrain the baseline model and achieve an accuracy comparable to the trained sites. Additionally, we showed that the model can learn to identify a new species, while maintaining high classification accuracy for all original species. Finally, we established that BatNet can be used to accurately describe ecological metrics from camera trap images (i.e., species diversity, relative abundance, and species-specific phenology) that are relevant for bat conservation.
We conclude that infrared light barriers and camera traps offer a minimally invasive and accurate method to monitor site-level bat population trends and species-specific phenological estimates at underground sites. Such remote data collection approaches are particularly relevant for monitoring large, complex hibernation sites, where traditional visual surveys are not feasible or account only for a small fraction of the actual population. Combining this automated monitoring method with a deep learning-based species identification tool, BatNet, allows us quickly and accurately analyze millions of camera trap images resulting from large-scale, long-term camera trap studies. As a result, we can gain unprecedented insights into the behavior and population dynamics of these enigmatic species, drastically improving our ability to support data-driven bat conservation.
The need for the diversification of utilised species has emerged in the present aquaculture
production environment. Shifts in consumer interest, climate change-induced temperature
increases, and major fish disease outbreaks have put a strain on this industry. In this context,
the pikeperch (Sander lucioperca) has become a new target species for aquaculture in Central
Europe. This new aquaculture focus species exhibits high numbers of offspring, fast growth,
and high consumer acceptance. It can also effectively deal with higher temperatures and turbid
water. However, the rate of successful rearing is still low, as various developmental
transformations and environmental effects commonly lead to high mortality rates during the
early ontogenetic stages. The aim of this doctoral project was thus to obtain insight into
embryonic to larval developmental changes during pikeperch ontogeny. Specifically, the times
of change that influence survival were of focus. Based on the available literature, particular
attention was paid to general growth patterns and the connected developmental changes, the
determination of myogenesis gene marker expression changes, and the support of animal
welfare efforts for pikeperch rearing procedures. To achieve the aims of the study, a methodical
setup consisting of morphometric and developmental observations was combined with
transcriptome gene marker analysis for the different ontogenetic stages.
Three developmental phases were differentiated during the embryo-larval transition. Each of
these possessed distinct growth patterns with different growth rates. The intermediate
threshold phase showed internal organ development that focused on digestive, neuronal, and
heart tissues. Three activity phases of myogenesis were determined: during early embryonic
development, before hatching, and after hatching during the larval stages. Therefore, muscle
development seemed to be regulated to balance energy expenditures. Additionally, two
coinciding skeletogenic phases were found. Furthermore, a cell line from whole embryos was
developed to support the replacement of animals in future experimental setups. A software
system for video analyses was developed to support rearing procedures in aquaculture
facilities. This prototype can be used to automate the counting of specimens and thus allows
for faster responses to increasing mortalities. Based on the results of this thesis project, further
insights into the early development of pikeperches were obtained. This will facilitate the design
and adaptation of raising and husbandry protocols, which can help to further establish
pikeperch as an aquaculture species and support its application in modern recirculatory
systems.
Relative importance of plastic and genetic responses to weather conditions in long-lived bats
(2022)
In the light of the accelerating pace of environmental change, it is imperative to understand how populations and species can adapt to altered environmental conditions. This is a crucial step in predicting current and future population persistence and limits thereof. Genetic adaption and phenotypic plasticity are two main mechanisms that can mediate the process of adaptation and are of particular importance for non-dispersing species. While phenotypic plasticity may enable individuals to cope with short term environmental changes, genetic adaptation will often be required for populations to survive in situ over longer time spans. However, a rapid genetic response is expected particularly in species with fast life histories or large population sizes, leaving species with slow life histories potentially at higher extinction risk. The Bechstein’s bat (Myotis bechsteinii) is a mammal of 10 g weight that - despite its small size - is characterized by a slow life history, with low reproductive output and long lifespan, and is already considered to be of high conservation concern. Past work demonstrated body size to be a highly fitness-relevant trait in Bechstein’s bats. Body size is further known to be a pivotal trait shaping the pace of life histories in numerous species. Simultaneously, many studies reported noteworthy changes in body size as a response to shifting environments across different taxa. This suggested a potential for high plasticity in this trait in Bechstein’s bats as well; however, changes in body size could have vital impacts on demographic rates.
Therefore, this dissertation investigated the following questions: firstly, what shapes the fundamental development of body size in M. bechsteinii, and, specifically, is there an impact of weather conditions on body size? If so, in what form and magnitude? Secondly, how does body size subsequently influence the pace of life in females? What is the cost of a faster or slower pace of life, and how does fitness compare across individuals with slow and fast life histories? And finally, to what extent can changes in body size be attributed to either phenotypic plasticity or genetic adaptation? What is the evolutionary potential of body size in the populations? And, consequently, what implications can we draw regarding population persistence of these colonies?
To answer these questions, we analyzed a long-term dataset of over two decades collected from four wild Bechstein’s bat colonies. We used individual-based data on survival, reproduction and body size, built multi-generational pedigrees, and combined everything with meteorological data. In Manuscript 1 we found that, in contrast to the declining body size observed in many species, body size in Bechstein’s bats increased significantly over the last decades. We demonstrated that ambient temperature was linked to the development of body size and identified a sensitive time period in the prenatal growth phase, in which body size was most susceptible to the impact of temperature. We established that warmer summers resulted in larger bats, but that these large bats had higher mortality risks throughout their lives. Manuscript 2 then revealed the influence of body size on the pace of life in Bechstein’s bats and demonstrated high plasticity in intraspecific life history strategies. Large females were characterized by a faster pace of life and shorter lifespans, but surprisingly, lifetime reproductive success remained remarkably stable across individuals with different body sizes. The acceleration of their pace of life means that larger females compensated for their reduced longevity by an earlier reproduction and higher fecundity to reach similar overall fitness. Ultimately, differences in body size resulted in changes in population growth rate via the impact of size on generation times. Results of Manuscript 3 were then able to clarify the extent to which changes in body size were founded on either phenotypic plasticity or genetic adaptation. We demonstrated a particularly low heritability in hot summers, indicating that variance in body size was mostly driven by phenotypic plasticity, with few genetic constraints. During cold summers, behavioural adaptations by reproducing bats seem to be able to mitigate negative effects of cold temperatures. These behaviours, such as social aggregation or preference for warm roosts, are, however, essentially irrelevant in hot environments. In addition, a low evolvability of forearm length points to a low capacity to respond to selection pressures associated with the trait.
We can conclude that body size in M. bechsteinii has increased over the last two decades as a response to global warming and is only slightly constrained by its genetic underpinnings. We can further demonstrate a direct link between body size and the pace of life histories in the Bechstein’s bat populations and how changes in body size impact demographic rates via this linkage. In the context of climate change and hotter summers, our findings consequently suggest that body size will likely increase further if warm summers continue to become more frequent. Whether this plastic response of body size proves to be adaptive in the long term, however, remains to be seen. While, up to this point, switching to a faster life history has been successful in compensating fitness losses, this strategy requires sufficient habitat quality and is likely risky in times when extreme weather events are becoming more frequent, as predicted by most climate change scenarios.
Podocytes are highly specialized kidney cells that are attached to the outer aspect of the glomerular capillaries and are damaged in more than 75% of patients with an impaired renal function. This specific cell type is characterized by a complex 3D morphology which is essential for proper filtration of the blood. Any changes of this unique morphology are directly associated with a deterioration of the size-selectivity of the filtration barrier. Since podocytes are postmitotic, there is no regenerative potential and the loss of these cells is permanent. Therefore, identification of small molecules that are able to protect podocytes is highly important. The aim of this work was to establish an in vivo high-content drug screening in zebrafish larvae. At first, we looked for a reliable podocyte injury model which is fast, reproducible and easy to induce. Since adriamycin is commonly used in rodents to damage podocytes, we administered it to the larvae and analyzed the phenotype by in vivo microscopy, (immuno-) histology and RT-(q)PCR. However, adriamycin did not result in a podocyte-specific injury in zebrafish larvae. Subsequently, we decided to use a genetic ablation model which specifically damages podocytes in zebrafish larvae. Treatment of transgenic zebrafish larvae with 80 µM metronidazole for 48 hours generated an injury resembling focal and segmental glomerulosclerosis which is characterized by podocyte foot process effacement, cell depletion and proteinuria. Following this, we established an in vivo high-content screening system by the use of a specific screening zebrafish strain. This screening strain expresses a circulating 78 kDa eGFP-labeled Vitamin D-binding fusion protein, which passes the filtration barrier only after glomerular injury. Therefore, we had an excellent readout to follow podocyte injury in vivo. We generated a custom image analysis software that measures the fluorescence intensity of podocytes and the vasculature automatically on a large scale. Furthermore, we screened a specific drug library consisting of 138 compounds for protective effects on larval podocytes using this in vivo high-content system. The analysis identified several initial hits and the subsequent validation experiments identified belinostat as a reliable and significant protective agent for podocytes. These results led to a patent request and belinostat is a promising candidate for a clinical use and will be tested in mammalian podocyte injury models.
Species are the basic units of evolution and biodiversity, and the process of speciation has been one of the most important questions in biology. The evolution of species with common descent is considered to be mainly driven by natural and sexual selection. The material basis and mechanical cause of organismic evolution were recognized during the formation of the modern synthesis of the evolutionary theory in the early 20th century, providing the framework for speciation studies. During this period, the biological species concept was developed in the frame of population genetics, putting emphasis on the reproductive isolation between populations. The phylogenetic species concept developed in the 1980s, on the other hand, does not make any particular assumption about evolutionary or speciation processes. It defines species via their unique combination of character states which are compatible with phylogenetic practices. However, the aforementioned two species concepts are difficult to apply in alpha-taxonomy, where newly discovered species are largely described by the morphological (typological) species concept for practical reasons. Nevertheless, the description of morphological species provides the basis for further assessments of species delimitation via other species concepts and approaches. One of the tools for assisting the identification and discovery of animal species is DNA barcoding, which uses a standard region of mitochondrial DNA sequence as a universal DNA barcode. However, its assumption of intraspecific genetic distances being smaller than interspecific genetic distances does not always hold. Species-level poly-/paraphyly is prevalent due to the discrepancy between the phylogenies of mitochondrial DNA and species. This suggests that the application of DNA barcodes must be combined with an integrative taxonomic approach. Beside the application as a tool for assisting species identification, the information from mitochondrial DNA sequences opens up a window for looking into the complex history of species.
Sexual selection is a potential mechanism driving the evolution of species. It favors traits that increase mating probability and mating success. It can result from intrasexual competition, female preference or sexual conflict. However, previous comparative studies using the degree of sexual dimorphism as a proxy for the strength of sexual selection have yielded inconsistent results as to the relationship between sexual selection and species richness. A possible cause of the inferred low association are factors other than sexual selection, which can also lead to the evolution of sexual dimorphism, such as selection for increased female fecundity. In order to assess the effect of sexual selection on speciation, the lability and evolvability of traits need to be studied that are clearly under sexual selection.
The aim of this thesis is to improve the knowledge about dwarf spider (Erigoninae, Linyphiidae) diversity and taxonomy, and to assess the evolutionary patterns of dimorphic traits that are under sexual selection. I focused on the abundant and diverse male prosomal modifications in dwarf spiders that are linked to the transfer of secretions from the male to the female during courtship and mating (gustatory courtship). This approach explores the process of speciation and the role of sexual selection on species diversification. I described new erigonine species and revised the classification of known species based on phylogenetic analyses. I also applied X-ray micro-computed tomography (micro-CT) to investigate the distribution and evolutionary pattern of the gustatory glands to tease apart the evolution of prosomal shape and glandular equipment.
This cumulative thesis consists of three publications:
Publication 1: This publication aimed at contributing to the knowledge of erigonine diversity. The genus Shaanxinus previously contained only two species from China. I collected dwarf spiders from multiple locations in Taiwan from above-ground vegetations with a seldom applied collecting method. Inspection of the collected material resulted in the discovery of 13 Shaanxinus species. An additional species from Vietnam was described from a museum collection. I provided a revision of the genus Shaanxinus. A phylogenetic analysis using morphological characters was conducted for determining the possible generic synamomorphies. I also reconstructed the glandular distribution associated with male prosomal modifications, as well as the detailed structure of a male secondary sexual organ (pedipalp) by micro-CT. Furthermore, I conducted phylogenetic analyses based on sequences from two mitochondrial and one nuclear loci, and assessed the efficacy of different criteria in species identification using DNA barcoding. Distinction of morphologically similar species have been assisted by molecular data. The species level poly-/paraphyly found in mitochondrial DNA sequences caused the low efficacy of many distance- and tree-based species identification methods, while the nearest neighbor method showed high identification success. The non-monophyly is likely caused by instances of interspecific hybridization and recent parapatric speciation. The genus Shaanxinus thus lend itself as an ideal group for congeneric phylogeographic studies addressing the interactions between closely related species. Published in: Lin, S.-W., Lopardo, L., Haase, M. & Uhl, G. 2019. Taxonomic revision of the dwarf spider genus Shaanxinus Tanasevitch, 2006 (Araneae, Linyphiidae, Erigoninae), with new species from Taiwan and Vietnam. Organism Diversity & Evolution, 19, 211-276.
Publication 2: Sexually dimorphic prosomal modifications that are related to gustatory courtship occur in many dwarf spider species. These features evolved in the context of sexual selection, which has a potential effect on species diversification. In contrast to many
erigonine genera which present little variability in male prosomal traits, the genus Oedothorax presents higher diversity in male prosomal structures among species not only in the position and shapes of the modifications, but also in the degree of modification, ranging from absent to highly elaborated. This genus thus lends itself as a suitable target group for studying the effect of gustatory-courtship-related traits on species diversification. I conducted a revision of the 82 species previously belonging to this genus. Based on the result of a phylogenetic analysis, this genus was re-delimited with 10 species as Oedothorax sensu stricto, while taxonomic decisions were made for other species including synonymization with species from other genera and transferring species to other existing and newly defined genera. 25 species were deemed as “Oedothorax” incertae sedis. The reconstruction of character state evolution suggested multiple origins of specific prosomal modification types. Convergent evolution of these traits among different lineages suggests that sexual selection has played an important role in the species diversification of dwarf spiders. Published in: Lin, S.-W., Lopardo, L. & Uhl, G. 2021. Evolution of nuptial-gift-related male prosomal structures: taxonomic revision and cladistic analysis of the genus Oedothorax (Araneae: Linyphiidae: Erigoninae). Zoological Journal of the Linnean Society, XX, 1-168.
Publication 3: Although sexually dimorphic traits have inspired the concept of sexual selection as the driving force of their evolution, they might also have evolved due to other ecological factors. These factors include the sexual signal adaptation to the environment as well as sexual differences in ecological relations and parental investment. In contrast, the gustatory courtship in dwarf spiders is associated with sexually dimorphic male prosomal modifications, which have clearly evolved in the context of sexual selection. Multiple origins of various external prosomal modifications have been shown in erigonine phylogeny, but the evolutionary pattern of the associated glands has not been investigated. Our phylogenetic analysis incorporated the characters related to the glandular distribution in the male prosoma as well as the external shapes yielded from X-ray micro-computed-tomography showed a single origin of gland among the investigated erigonine taxa. The internal anatomy revealed previously undetected trait lability in attachments of muscles to the cuticular structures, as well as the presence/absence and differences in glandular distribution even in species without external modification. Our finding further supports that erigonine male prosomal traits are under divergent selection, and corroborates the argument that erigonines are a suitable group for investigating the effect of sexual selection on speciation. Published in: Lin, S.-W., Lopardo, L. & Uhl, G. 2021. Diversification through gustatory courtship: an X‑ray micro‑computed tomography study on dwarf spiders. Frontiers in Zoology, 18: 51.
The results of this thesis corroborate the importance of applying phylogenetic methods and an integrative approach in the description of new species, as well as in revising taxa which might not be monophyletic. Overall, the studies contributed to a more comprehensive knowledge about erigonine species diversity, phylogeny and the possible diversifying effect of sexual selection on male traits associated with gustatory courtship.
Abstract
Social organisation in species with fluctuating population sizes can change with density. Therefore, information on (future) density obtained during early life stages may be associated with social behaviour. Olfactory cues may carry important social information. We investigated whether early life experience of different experimental densities was subsequently associated with differences in attraction to adult conspecific odours. We used common voles (Microtus arvalis), a rodent species undergoing extreme density fluctuations. We found that individuals originating from high experimental density populations kept in large outdoor enclosures invested more time in inspecting conspecific olfactory cues than individuals from low‐density populations. Generally, voles from both treatments spent more time with the olfactory cues than expected by chance and did not differ in their latency to approach the odour samples. Our findings indicate either that early experience affects odour sensitivity or that animals evaluate the social information contained in conspecific odours differently, depending on their early life experience of conspecific density.
Abstract
The two important mechanisms influencing the response of phytoplankton communities to alterations of abiotic factors in their environment are difficult to distinguish: species sorting resulting from a change in interspecific competitive pressure, and phenotypic plasticity (here explicitly physiological plasticity i.e. species‐specific physiological adjustment). A shift in species composition as well as physiological adjustments in species can lead to changes in fatty acid composition that determine the food quality for zooplankton consumers.
We used phytoplankton communities consisting of five species and exposed them to two different light intensities, two light conditions (constant and variable), and two levels of phosphorus supply. Changes in fatty acid and species composition were analyzed. We compared community pairs differing in one factor by calculating the Bray‐Curtis similarity index for the composition of both variables. Comparing the Bray‐Curtis similarity index of the species composition with the index of the fatty acid composition was used to estimate the effects of species sorting and physiological plasticity.
Changes in nutrient supply influenced fatty acid responses based on species sorting and physiological plasticity the most. On one hand, the relevance of physiological plasticity was highest at cultivation in different nutrient supplies but the same light environment. Conversely with low nutrients species sorting appeared to dominate the response to changes in light, while at high nutrients physiological plasticity appeared to influence the response. Overall, under low phosphorus supply the communities showed a lower total fatty acid content per carbon and had increased proportions of saturated and monounsaturated fatty acids. Instead, communities in low light produced more of eicosapentaenoic acid.
Our results suggest that the relevance of species sorting and physiological plasticity in shaping the community response highly depends on the environmental factors that influence the system. Nutrient supply had the largest effect, while light had more limited conditional effects. However, all of these factors are important in shaping the food quality of the phytoplankton community for higher trophic levels.
Abstract
Aim
Species ranges are highly dynamic, shifting in space and time as a result of complex ecological and evolutionary processes. Disentangling the relative contribution of both processes is challenging but of primary importance for forecasting species distributions under climate change. Here, we use the spectacular range expansion (ca. 1000 km poleward shift within 10 years) of the butterfly Pieris mannii to unravel the factors underlying range dynamics, specifically the role of (i) niche evolution (changes in host‐plant preference and acceptance) and (ii) ecological processes (climate change).
Location
Provence‐Alpes‐Côte d’Azur, France; North Rhine‐Westphalia, Rhineland‐Palatinate and Hesse, Germany.
Taxon
Insect and angiosperms.
Methods
We employed a combination of (i) common garden experiments, based on replicated populations from the species’ historical and newly established range and host‐plant species representative for each distribution range, co‐occurrence analyses and (ii) grid‐based correlative species distribution modelling (SDM) using Maxent.
Results
We observed changes in oviposition preference, with females from the newly established populations showing reduced host‐plant specialization and also an overall increased fecundity. These changes in behaviour and life history may have enabled using a broader range of habitats and thus facilitated the recent range expansion. In contrast, our results indicate that the range expansion is unlikely to be directly caused by anthropogenic climate change, as the range was not constrained by climate in the first place.
Main conclusions
We conclude that evolution of a broader dietary niche rather than climate change is associated with the rapid range expansion, and discuss potential indirect consequences of climate change as trigger for the genetic differences found. Our study thus illustrates the importance of species interactions in shaping species distributions and range shifts, and draws attention to indirect effects of climate change. Embracing this complexity is likely the key to a better understanding of range dynamics.
Abstract
Nervous system development has been intensely studied in insects (especially Drosophila melanogaster), providing detailed insights into the genetic regulatory network governing the formation and maintenance of the neural stem cells (neuroblasts) and the differentiation of their progeny. Despite notable advances over the last two decades, neurogenesis in other arthropod groups remains by comparison less well understood, hampering finer resolution of evolutionary cell type transformations and changes in the genetic regulatory network in some branches of the arthropod tree of life. Although the neurogenic cellular machinery in malacostracan crustaceans is well described morphologically, its genetic molecular characterization is pending. To address this, we established an in situ hybridization protocol for the crayfish Procambarus virginalis and studied embryonic expression patterns of a suite of key genes, encompassing three SoxB group transcription factors, two achaete–scute homologs, a Snail family member, the differentiation determinants Prospero and Brain tumor, and the neuron marker Elav. We document cell type expression patterns with notable similarities to insects and branchiopod crustaceans, lending further support to the homology of hexapod–crustacean neuroblasts and their cell lineages. Remarkably, in the crayfish head region, cell emigration from the neuroectoderm coupled with gene expression data points to a neuroblast‐independent initial phase of brain neurogenesis. Further, SoxB group expression patterns suggest an involvement of Dichaete in segmentation, in concordance with insects. Our target gene set is a promising starting point for further embryonic studies, as well as for the molecular genetic characterization of subregions and cell types in the neurogenic systems in the adult crayfish brain.
Abstract
The neritid snail Theodoxus fluviatilis has formed regional subgroups in northern Europe, where it appears in both freshwater (FW) and brackish water (BW) in coastal areas of the Baltic Sea. These ecotypes show clear differences in osmotolerance and in the modes of accumulating organic osmolytes under hyperosmotic stress. We reasoned that the expression patterns of soluble proteins in the two ecotypes may differ as well. BW snails have to deal with a higher salinity (up to 20‰) than FW snails (0.5‰) and also cope with frequent fluctuations in environmental salinity that occur after heavy rains or evaporation caused by extended periods of intense sunshine. Therefore, the protein expression patterns of specimens collected at five different FW and BW sites were analyzed using 2D SDS‐PAGE, mass spectrometry, and sequence comparisons based on a transcriptome database for Theodoxus fluviatilis. We identified 89 differentially expressed proteins. The differences in the expression between FW and BW snails may be due to phenotypic plasticity, but may also be determined by local genetic adaptations. Among the differentially expressed proteins, 19 proteins seem to be of special interest as they may be involved in mediating the higher tolerance of BW animals towards environmental change compared with FW animals.
Abstract
Climate change may force organisms to adapt genetically or plastically to new environmental conditions. Invasive species show remarkable potential for rapid adaptation. The ovoviviparous New Zealand mud snail (NZMS), Potamopyrgus antipodarum, has successfully established across Europe with two clonally reproducing mitochondrial lineages since its arrival in the first half of the 19th century. Its remarkable variation in shell morphology was shown to be fitness relevant. We investigated the effects of temperature on shell morphology across 11 populations from Germany and the Iberian Peninsula in a common garden across three temperatures. We analyzed size and shape using geometric morphometrics. For both, we compared reaction norms and estimated heritabilities. For size, the interaction of temperature and haplotype explained about 50% of the total variance. We also observed more genotype by environment interactions indicating a higher degree of population differentiation than in shape. Across the three temperatures, size followed the expectations of the temperature‐size rule, with individuals growing larger in cold environments. Changes in shape may have compensated for changes in size affecting space for brooding embryos. Heritability estimates were relatively high. As indicated by the very low coefficients of variation for clonal repeatability (CVA), they can probably not be compared in absolute terms. However, they showed some sensitivity to temperature, in haplotype t more so than in z, which was only found in Portugal. The low CVA values indicate that genetic variation among European populations is still restricted with a low potential to react to selection. A considerable fraction of the genetic variation was due to differences between the clonal lineages. The NZMS has apparently not been long enough in Europe to accumulate significant genetic variation relevant for morphological adaptation. As temperature is obviously not the sole factor influencing shell morphology, their interaction will probably not be a factor limiting population persistence under a warming climate in Europe.
Abstract
Human habitat disturbance affects both species diversity and intraspecific genetic diversity, leading to correlations between these two components of biodiversity (termed species–genetic diversity correlation, SGDC). However, whether SGDC predictions extend to host‐associated communities, such as the intestinal parasite and gut microbial diversity, remains largely unexplored. Additionally, the role of dominant generalist species is often neglected despite their importance in shaping the environment experienced by other members of the ecological community, and their role as source, reservoir and vector of zoonotic diseases. New analytical approaches (e.g. structural equation modelling, SEM) can be used to assess SGDC relationships and distinguish among direct and indirect effects of habitat characteristics and disturbance on the various components of biodiversity.
With six concrete and biologically sound models in mind, we collected habitat characteristics of 22 study sites from four distinct landscapes located in central Panama. Each landscape differed in the degree of human disturbance and fragmentation measured by several quantitative variables, such as canopy cover, canopy height and understorey density. In terms of biodiversity, we estimated on the one hand, (a) small mammal species diversity, and, on the other hand, (b) genome‐wide diversity, (c) intestinal parasite diversity and (d) gut microbial heterogeneity of the most dominant generalist species (Tome's spiny rat, Proechimys semispinosus). We used SEMs to assess the links between habitat characteristics and biological diversity measures.
The best supported SEM suggested that habitat characteristics directly and positively affect the richness of small mammals, the genetic diversity of P. semispinosus and its gut microbial heterogeneity. Habitat characteristics did not, however, directly impact intestinal parasite diversity. We also detected indirect, positive effects of habitat characteristics on both host‐associated assemblages via small mammal richness. For microbes, this is likely linked to cross species transmission, particularly in shared and/or anthropogenically altered habitats, whereas host diversity mitigates parasite infections. The SEM revealed an additional indirect but negative effect on intestinal parasite diversity via host genetic diversity.
Our study showcases that habitat alterations not only affect species diversity and host genetic diversity in parallel, but also species diversity of host‐associated assemblages. The impacts from human disturbance are therefore expected to ripple through entire ecosystems with far reaching effects felt even by generalist species.
Abstract
Background
Several leech species of the genera Hirudo, Hirudinaria, and Whitmania are widely used in traditional Chinese medicine (TCM) for the oral treatment of disorders associated with blood stasis. Among them, the non‐hematophagous leech Whitmania pigra expresses a variety of components that have the potential to act on the vertebrate blood coagulation system.
Objective
Whether the thrombin inhibitor hirudin, probably the most prominent leech‐derived anticoagulant, is actually present in Whitmania pigra, is still a matter of debate. To answer that open question was the aim of the study.
Methods
We identified several putative hirudin‐encoding sequences in transcriptome data of Whitmania pigra. Upon gene synthesis and molecular cloning the respective recombinant proteins were expressed in Escherichia coli, purified, processed, and eventually functionally characterized for thrombin‐inhibitory potencies in coagulation assays.
Results
We were successful in the identification and functional characterization of several putative hirudins in Whitmania pigra. Some, but not all, of these factors are indeed thrombin inhibitors. Whitmania pigra hence expresses both hirudins (factors that inhibit thrombin) and hirudin‐like factors (that do not or only very weakly inhibit thrombin). Furthermore, we revealed the exon/intron structures of the corresponding genes. Coding sequences of some putative hirudins of Whitmania pigra were present also in transcriptome datasets of Hirudo nipponia, a hematophagous leech that is likewise used in TCM.
Conclusions
Based on both structural and functional data we provide very strong evidence for the expression of hirudins in Whitmania pigra. This is the first description of hirudins in a non‐hematophagous leech.
Abstract
Surface waters are warming due to climate change, potentially pushing aquatic organisms closer to their thermal tolerance limits. However, cyanobacterial blooms are expected to occur more often with rising temperature, increasing the likelihood of poor‐quality food available for herbivorous zooplankton. Zooplankton can adapt locally by genetic differentiation or via adaptive phenotypic plasticity to increasing temperatures, but there is limited knowledge on how these processes may be affected by food quality limitation imposed by cyanobacteria.
To test the effects of cyanobacteria‐mediated food quality on local temperature adaptation, we measured juvenile somatic growth and reproduction of five Daphnia magna clones from different latitudinal origin grown on three food qualities at 20, 24, and 28°C. Additionally we estimated short‐term heat tolerance, measured as knockout time (time to immobility) at lethally high temperature, of two clones acclimated to the three temperatures and two food quality levels to test for the effects of food quality on adaptive plastic responses.
As expected, clones from lower latitudes showed on average better somatic growth and reproduction than clones from higher latitudes at higher temperatures. However, the difference in somatic growth diminished with increasing cyanobacteria abundance in the diet, suggesting constraints on local genetic adaptation under predicted decreases in food quality. As expected, short‐term heat tolerance of the clones generally increased with increasing acclimation temperature. However, heat tolerance of animals acclimated to the highest temperature was larger when grown at medium than at good food quality, whereas the opposite response was observed for animals acclimated to the lowest temperature. This suggests a better adaptive phenotypic response of animals to elevated temperatures under higher cyanobacteria abundance, and thus shows an opposite pattern to the results for somatic growth.
Overall, we demonstrate that food quality limitation can mediate responses of D. magna life history traits and heat tolerance to increasing temperatures, and that the effects differ depending on the time scale studied, that is, mid‐term (somatic growth) versus short‐term (tolerance to acute heat stress). These aspects will need further attention to accurately predict of how organisms will cope with future global warming by local adaptation and adaptive phenotypic plasticity.
Abstract
Pikeperch (Sander lucioperca) has become a species of interest in aquaculture. It is a popular and economically valuable food fish and can produce high numbers of offspring. However, during early development, there are transition phases when high mortality rates concur with growth changes, vital organ transformations and a limited energy budget. Up to now, no study focused on the developmental adaption of muscle tissue in pikeperch, regardless of muscle tissue influencing essential traits such as locomotion and thus the competence to hunt prey and avoid predators. In the present study, therefore, the developmental myogenesis of pikeperch was analysed using specimens from early embryonic to larval development. Myogenic and developmental genes were utilized to gain insights into transcriptomic regulation during these stages by applying a nanofluidic qPCR approach. Result, three phases of myogenic gene expression, during somitogenesis, during the late embryonic development and during the larval development were detected. Increased myostatin expression showed an interim arrest of muscle formation between embryonic and larval myogenesis. Expression patterns of satellite cell gene markers indicated an accumulation of stem cells before myogenesis interruption. The here gained data will help to broaden the knowledge on percid myogenesis and can support pikeperch rearing in aquaculture.
Abstract
Currently, poleward range expansions are observed in many taxa, often in response to anthropogenic climate change. At the expanding front, populations likely face cooler and more variable temperature conditions, imposing thermal selection. This may result in changes in trait means or plasticity, the relative contribution of which is not well understood. We, here, investigate evolutionary change in range‐expanding populations of the butterfly Pieris mannii, by comparing populations from the core and the newly established northern range under laboratory conditions. We observed both changes in trait means and in thermal reaction norms. Range‐expanding populations showed a more rapid development, potentially indicative of counter‐gradient variation and an increased cold tolerance compared with core populations. Genotype‐environment interactions prevailed in all associated traits, such that the above differences were restricted to cooler environmental conditions. In range‐expanding populations, plasticity was decreased in developmental traits enabling relatively rapid growth even under cooler conditions but increased in cold tolerance arguably promoting higher activity under thermally challenging conditions. Notably, these changes must have occurred within a time period of ca. 10 years only. Our results suggest, in line with contemporary theory, that the evolution of plasticity may play a hitherto underestimated role for adaptation to climatic variation. However, rather than generally increased or decreased levels of plasticity, our results indicate fine‐tuned, trait‐specific evolutionary responses to increase fitness in novel environments.