590 Tiere (Zoologie)
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- Biologie , Allgemeine Zoologie , Zoologie , Spinnen , Klimaänderung , Genomik , Mikrobiologie , Ökologie (1)
- Biology, Zoology, Spiders, Genomics, Microbiology, Ecology (1)
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Institute
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.
Bats are special: although they have a small body size, bats are extremely long-lived and have a low annual reproductive output, which puts them at the ‘slow’ end of the slow-fast continuum of mammalian life-histories. Species typically respond to climate change by genetic adaptation, range shifts or phenotypic plasticity. However, limited dispersal behavior in many bat species and long generation times make it very likely, that adaptive responses in bats are rather driven by phenotypic plasticity than by genetic adaptation or range shifts. Changing weather patterns, a higher frequency of extreme weather events and overall rising temperatures, caused by climate change, will impact phenology, energy supply and energy expenditure. In species where adult survival largely shapes population dynamics, it is thus of crucial importance to understand how climate change affects individual fitness and fitness relevant traits by altering behavior and development.
In my study, I investigated how weather impacts behavior, fitness and fitness relevant traits in free ranging Natterer’s bats from two geographical regions (south vs. north) in Germany. In the Nature Park Nossentiner/Schwinzer Heide (northern region, NSH), long-term data for investigations on population dynamics are partially collected by hibernation counts. Although counting hibernating bats is a regularly applied method, it is still unclear to which degree human visits in the hibernaculum trigger energy consuming arousals and thus increase energy expenditure. Thus, I first investigated if hibernation counts potentially threaten winter survival by assessing the number of energy consuming arousals of hibernating Natterer’s bats (Myotis nattereri) and two other bat species (Pipistrellus spp., Plecotus auritus) using thermal imaging. Additionally, I used light barriers in the hibernacula to investigate the relative impact of winter temperatures and human visits on flight activity of hibernating bats. Secondly, I investigated effects on survival and reproduction during summer by analyzing capture-mark-recapture data from summer roosts. Data from summer roosts have been collected since 2011 in Würzburg (WB, south) and 1990 in the Nature Park (NSH, north). Based on these data, I analyzed the effect of intrinsic (e.g. age) and extrinsic(e.g. different weather parameters) factors on individual survival probability and reproductive success. I further focused on the question if individual body size is a fitness relevant trait in Natterer’s bats and how body size of young bats is affected by summer temperatures.
During hibernation, ambient temperatures were the most important driver for bat activity and were positively correlated with the number of flight passes in the light barrier, suggesting that bats can exploit foraging opportunities more frequently during warm weather bouts. Monitoring caused only a small number of arousals and only a slight increase in activity, which was less severe on warmer days, when activity was generally higher. Thus, I propose that benefits of hibernation counts outweigh the costs of human presence in the hibernaculum and unlikely threaten winter survival in hibernating bats.
In spring, increased precipitation during a short time window strongly reduced the probability of successful reproduction in first-year females (females that returned from first hibernation, FY). In terms of timing, this sensitive period comprises the implantation or early pregnancy, a time before substantial investment into embryo development. Moreover, I identified a positive correlation between a large body size and reproductive success in FY females. Given the evidence that suitable weather conditions during early life support juvenile growth and thus a large body size, my findings suggest that reproduction may be condition dependent in young females. Reproductive success of older females was not affected by either weather or individual parameters. This suggests that older and experienced females can better deal with adverse conditions.
To examine if beneficial weather conditions are linked to a large body size, I investigated the effect of ambient temperatures during the growing season on body size. I found that higher ambient temperatures during summer led to larger individuals, however, only in the northern population. In the on average colder North, warmer summers may benefit juvenile growth by reducing thermoregulatory costs and increasing prey abundance, whereas in the general warmer South, this effect might not be visible or relevant. When I analyzed the link between body size and survival, I revealed that larger adult females have higher survival rates. Given the fact, that a large body size is a response to beneficial early life conditions, this demonstrates the impact of early life conditions on long lasting fitness effects.
The results of my research lead to the assumption that warmer ambient temperatures have positive effects on Natterer’s bats, both during winter and summer. However, increased activity in response to rising winter temperatures, as expected under climate change scenarios, could be a serious thread for hibernating bats, if food availability does not increase in the same amount as bat activity. During summer, warmer temperatures may have positive effects on juvenile development in northern regions, but this effect could be negative in more southern regions by exceeding heat tolerance and resulting in water stress. This research highlights, that investigating periods of weather sensitivity on a finer time scale and also in a spatial context is of crucial importance to gain a better understanding for mechanisms leading to the impacts of weather on fitness.
As the effects of anthropogenic climate change become more pronounced, it is critical to understand if and how species can persist in novel environments. Range-expanding species provide a natural experiment to study this topic: by studying the factors contributing to successful colonization of new habitats, we can gain insight into what influences organisms’ adaptive potential. The wasp spider, Argiope bruennichi, has expanded its range from warm, oceanic and Mediterranean climate zones (populations in this region are referred to as “ancestral” or “core”) into a new thermal niche, the continental climate of the Baltic States and Scandinavia (referred to as “expanding” or “edge”) within the last century. Past work demonstrated that the expanding populations are European in origin, but are more diverse than the ancestral populations, due to genetic admixture. This discovery led to the following questions, which are investigated in this dissertation: (i) Was the successful colonization of colder, more continental northern climates due to phenotypic plasticity or genetic adaptation? (ii) If A. bruennichi’s establishment of northern latitudes can be attributed to genetic adaptation, did selection act on standing genetic variation, on genetic variation introduced via admixture/introgression, on specific genomic regions, or on novel mutations? (iii) Is there a role of the microbiome in the A. bruennichi range expansion?
In Chapter 1, we assembled a chromosome-level genome for the species: the first such high-quality genome for a spider, which we made use of as a resource to provide the genomic context of single nucleotide polymorphisms in our primary study on genetic adaptation and phenotypic plasticity (Chapter 3). The genome assembly also opened the door to many new projects, such as the study presented in Chapter 2. In Chapter 2, the chromosome-level resolution of our assembly allowed us to identify the sex chromosomes in A. bruennichi. Due to the X1X20 sex chromosome system, where males have one copy of two X chromosomes, and females have two copies, the X chromosomes have a lower effective population size, and lower recombination rate, than autosomes. These characteristics give rise to the theoretical prediction of increased evolutionary rates in sex chromosomes. Knowing the identity of the sex chromosomes in our A. bruennichi genome assembly will allow us to test if there is stronger differentiation between populations on the X chromosomes.
Chapter 3 represents the central study of this dissertation. We performed a reciprocal transplant common garden experiment to assess plasticity and adaptation in cold tolerance traits, using spiderlings from the core of the range in France, and the edge of the range in Estonia. We combined this with data on clinal variation in adult phenotypes (body size, pigmentation, and fecundity) and genotypes in a transect across the European range. This study revealed a strong signature of genetic adaptation for increased cold tolerance in edge populations, and clear genetic differentiation of ancestral and expanding populations over a very short geographic distance, despite gene flow. We provide genome-wide evidence for adaptive introgression, and conclude that the A. bruennichi range
expansion was enabled by adaptive introgression, but has reached a poleward range limit.
Interactions with microbes shape all aspects of eukaryotic life. Endosymbiotic bacteria have been shown to alter the thermal tolerance of arthropod hosts, and influence dispersal behavior in spiders. With this background, in Chapter 4, we asked whether the microbiome might play a role in the rapid range expansion of A. bruennichi. We characterized the microbiome in various dissected tissues of spiders from two populations. Although we found no obvious differences between populations or tissues, this study yielded the discovery of a novel, dominant, vertically transmitted symbiont with astoundingly low similarity to all other sequenced bacteria. Since that discovery, we have found evidence of the unknown symbiont in A. bruennichi populations across the Palearctic (unpublished data), making it relatively unlikely to play a role in the range expansion.
By studying the establishment and subsequent differentiation of core versus edge populations of A. bruennichi following range expansion, we were able to gain insight into the evolutionary and ecological processes that allowed this species to successfully cope with novel environments. The rapidity with which local adaptation arose in A. bruennichi suggests that evolutionary adaptation to novel environments is possible over short time periods. However, this may only be possible in species with sufficient standing genetic variation, or with genetic variation introduced via admixture, as in A. bruennichi, which has important implications for our understanding of species responses in the face of ongoing global climate change.
Under the influence of human activities, increased climate variability induces changes in
multiple marine environments. Especially vulnerable are the coastal ecosystems where organisms
must cope with constant extreme changes of environmental drivers, such as temperature, salinity, pH,
and oxygen content. In coastal areas, brachyuran crabs are important animals that have a high impact
on ecosystem functioning and serve as a link in food webs and pelagic-benthic coupling. Larval stages
of crabs are crucial for population persistence and dispersal. They are generally more vulnerable to
changes of environmental drivers and failure to adapt to new conditions may result in population
collapse. To analyse the effects of multiple environmental drivers on larval performance and to
elucidate interspecific and intraspecific difference, this project examined larval performance in the
European shore crab Carcinus maenas. In this study, larvae of C. maenas from three native
populations (Cádiz: Cádiz Bay, Helgoland: North Sea, Kerteminde: Baltic Sea) were reared in a
factorial design consisting of different temperature (15-24 °C) and salinity treatments (20, 25, 32.5
PSU). Results demonstrated how descriptors of larval performance (growth, physiological, and
developmental rates, and survival) were affected by combined environmental drivers. Larval
responses to temperature and salinity showed contrasting patterns and differed among native
populations originating from distant or contrasting habitats, as well as within the populations. The
highest overall performance was recorded in the Cádiz population, while the Kerteminde population
had the lowest performance in most of tested traits. The interactive effects of multiple drivers differed
among the populations. In the Cádiz and Helgoland populations, higher temperatures mitigated the
effect of lower salinity while the Kerteminde population showed a maladaptive response when
exposed to lower salinity. Differences in performance showed better locally adapted populations (e.g.
Cádiz) that could acclimate faster, have better adaptive mechanisms or stronger dispersive abilities.
Because of their wider tolerance to increased temperature and decreased salinity, interactive effects
in particular populations may favour some populations in a changing climate, especially in coastal
habitats. Variation in larval performance showed complex interactions in larval performance and
highlighted the necessity to quantify inter-population responses to climate-driven environmental
change where responses of species should not be generalised. This study emphasizes the need for
inclusion of multiple traits, drivers, and populations in experimental studies to properly characterize
performance of marine coastal animals.