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Abstracts

Alan Le Moan
Anja Marie Westram
Anna Qvarnström
Aurélien De Jode
Ciaran Gilchrist
Colin Olito
Elina Immonen
Ellika Faust
Emma Berdan
Eva Koch
James Reeve
Jessica Abbott
Jörgen Ripa
Mads Fristrup Schou
Marlene Jahnke
Martin Lind
Mats Ittonen
Matthew Nielsen
Miguel Brun-Usan
Nathalie Feiner
Paula Vasconcelos
Raissa de Boer
Rebekah Oomen
Robin Pranter
Roger Butlin
Sissel Jentoft
Staffan Bensch
Stephen Palumbi
Sören Nylin
Victoria Sork


Beyond parallel evolution: the importance of population history and standing genetic variation in local adaptatio

Alan Le Moan, Dept Marine Sciences, University of Gothenburg

The predictability of genomic signatures associated with population divergence and speciation is a key research topic in evolutionary biology. Parallel evolution have offered opportunities to study the role of the environment by providing replicates of ecologically driven speciation. In this presentation, I will speak about my PhD results where I apply an extension of the parallel evolution framework to study replicates of speciation where multiple species went through a process of population divergence during the colonization of a common environmental gradient. I used the conditions offered by the North Sea - Baltic Sea environmental transition zone and found clear evidence of population structure linked to the Baltic Sea salinity gradient in four flatfish species. I found highly heterogeneous signatures of population divergence within and between species, and no evidence of parallel genomic architecture across species associated with the divergence. Analyses of demographic history suggest that Baltic Sea lineages are older than the age of the Baltic Sea itself, and the analyses revealed that genomic patterns of divergence were likely the result of a combination of effects from past isolation and subsequent adaptation to a new environment, involving selection on standing genetic variation. These results highlight the heterogeneous genomic effects associated with complex interplays of evolutionary forces, and stress the importance of genomic background for studies of parallel evolution.

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What can replicate hybrid zones in a marine snail tell us about adaptive divergence and speciation? 

Anja Marie Westram, IST Austria

Combining hybrid zone analysis with genomic data is a promising approach to understanding the genomic basis of adaptive divergence and speciation. It allows for the identification of genomic regions underlying reproductive barriers, but also provides insights into spatial patterns of allele frequency change that inform about the interplay between environmental factors, dispersal and selection. We have applied this approach to the marine snail Littorina saxatilis, which contains two distinct and partially isolated ecotypes, adapted to wave-exposed vs. high-predation habitats. The existence of numerous similar hybrid zones in L. saxatilis offers the opportunity to test for the repeatability of genomic architectures and spatial patterns of divergence. Here, we have studied seven Swedish hybrid zones. Most genomic regions showing steep clines and/or high differentiation are shared among hybrid zones, consistent with a common evolutionary history and extensive gene flow, and supporting the importance of these regions for divergence. In addition, we find evidence for consistent displacement of clines into the Wave habitat. We discuss potential causes for this result, including between-ecotype differences in population sizes and the extent of dispersal.

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Divergent mitochondrial and nuclear OXPHOS genes are candidates for genetic incompatibilities in Ficedula Flycatchers

Anna Qvarnström, Department of Ecology and Genetics, Animal Ecology, Uppsala University

Bateson-Dobzhansky-Muller incompatibilities are recognized as important for speciation by causing hybrid dysfunction. However, little empirical evidence exists for which genes are involved in such incompatibilities leaving the relative role of ecological divergence and other processes such as genomic conflict unknown. Genes involved in energy metabolism are potential candidates because energy metabolism depends on co-expression of mitochondrial DNA (mtDNA) and nuclear DNA (nDNA). When mitochondrial and nuclear genes lacking a co-evolutionary history appear together in hybrids, incompatibilities could arise. Ficedula flycatcher F1 hybrids have a higher resting metabolic rate (RMR) compared to the parental species, which could be a sign of genetic incompatibilities between energy metabolism genes that diverged in response to environmental differences while the species were geographically separated. Based on sequences of 15 mitochondrial genes of 265 individuals, we show that specific codon identified sites might be under positive selection in both mitochondrial and nuclear genes encoding OXPHOS proteins for complex I and III. We also find that mitochondrial and nuclear OXPHOS genes have higher levels of divergence between collared and pied flycatchers than the average gene in the genome. This divergence could provide at least some of the fuel for BDMIs between the species affecting hybrid performance.

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Ecological differentiation between cryptic engineering species of coralligenous habitats: the Lithophyllum stictiforme/cabiochiae species complex

Aurélien De Jode, Dept Marine Sciences, University of Gothenburg

Ecosystem engineering species alter the physical structure of their environment and can create or modify habitats, having a massive impact on local biodiversity. Coralligenous reefs are highly diverse habitats endemic to the Mediterranean Sea built by calcareous benthic organisms among which Crustose Coralline Algae are the main engineering species. We analyzed the diversity of Lithophyllum stictiforme or L. cabiochiae in coralligenous habitats combining a multiple barcode and a population genomics approach with seascape features. Population genomics allowed disentangling pure spatial effects from environmental effects. We found that these taxa form a complex of eight highly divergent cryptic species that are easily identifiable using classic barcode markers (psbA, LSU, COI). Three factors have a significant effect on the relative abundances of these cryptic species: the location along the French Mediterranean coast, depth and Photosynthetic Active Radiation (PAR). The analysis of around 5000 SNPs for the most abundant species revealed genetic differentiation among localities in the Bay of Marseille but no differentiation between depths within locality. Thus, the effect of depth and PAR on cryptic species communities is not a consequence of restricted connectivity but rather due to differential settlement or survival among cryptic species. This differential is more likely driven by irradiance levels rather than by pressure or temperature. Both the genetic and species diversity patterns are congruent with the main patterns of currents in the Bay. Ecological differentiation among these engineering cryptic species, sensitive to ocean warming and acidification, could have important consequences on the diversity and structure of the coralligenous communities.

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1000 Generations of Adaptation to Stressful Environments - Experimental Evolution and Hybridisation with Baker’s Yeast

Ciaran Gilchrist, Department of Zoology, Stockholm University

With the advent of climate change, natural ecological mating barriers increasingly disappear and rates of hybridisation between genetically divergent populations and species increase. While hybrid offspring generally have poor average fitness, hybridisation can also be an important source of novel genetic variation. Exactly how detrimental or beneficial hybridisation is for fitness and adaptation depends on genetic and environmental factors. Here, we use the power of experimental evolution with the model system Saccharomyces cerevisiae to investigate whether genetic variation gained through hybridisation can assist populations with adaptation to stressful environments. We propagated replicate populations of S. cerevisiae in four stressful conditions for ~1000 generations using serial transfer. At regular intervals, we generated sexual crosses between populations from divergent environments (‘hybrids’). All evolved populations showed higher yield than the founders after 1000 generations, consistent with local adaptation. The fitness dynamics suggest that adaptation occurred initially from standing genetic variation and later from de novo mutations. Genetically admixed hybrid populations were often intermediate in fitness between the parents, but many populations exceeded or fell short of their parents’ fitness. Overall, our results suggest that whole genome admixture broadens the accessible phenotypic space and can give hybrids a selective advantage, even in parental habitats.

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The evolution of chromosomal inversions suppressing recombination between sex chromosomes

Colin Olito, Department of Biology, Lund University

The evolution of suppressed recombination is a characteristic feature of most sex chromosome systems. Now classic evolutionary theory proposes that sex-differences in selection, and especially sexual antagonism generates selection for this reduced recombination. Yet, empirical evidence for the sexually antagonistic selection hypothesis remains meagre, and several alternative hypotheses for the evolution of restricted recombination between sex chromosomes have received far less theoretical or empirical attention. Here, we present theoretical population genetic models to address the link between the size of chromosomal inversions suppressing recombination and their probability of fixation. Simply put, we ask whether the size of evolutionary strata caused by chromosomal inversions reflect the evolutionary processes driving their fixation? We show that neutral and unconditionally beneficial inversions should, on average, leave behind signatures of small evolutionary strata, while those capturing sexually antagonistic variation should involve intermediately sized strata. We also show that the sheltering mechanism often proposed by heterozygote advantage hypotheses are unlikely to contribute to suppressed recombination except under biologically implausible circumstances. We conclude by briefly discussing how our theoretical predictions can help distinguish between different processes potentially driving recombination suppression between sex chromosomes.

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Evolving sexual size differences in the seed beetle

Elina Immonen, Department of Ecology and Genetics, Uppsala University

Sex chromosomes have been theorized to play an important role in the evolution of phenotypic sex differences, because their asymmetric inheritance should allow a partial or complete resolution of sexual conflict for the alleles subject to sexually antagonistic selection. Molecular signatures of sexualization of sex chromosomes often align with theory, but demonstrations of their role in phenotypic dimorphisms are scarce. This is particularly so for the Y chromosome, which is subject to progressive degeneration as a result of halting recombination that limits segregating polymorphism. Here we utilize the seed beetle Callosobruchus maculatus to test how body size dimorphism can evolve. We first characterized the quantitative genetic architecture of size as well as size dimorphism, and then tested how replicated sex-limited and sexually antagonistic artificial selection affect body size in each sex. We find a high intersex genetic correlation but also a remarkably strong Y-linkage in males. In this talk I will show how this genetic architecture constrains or facilitates the evolution of size dimorphism in an experimental context depending on the nature of selection.

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Cleaner fish on the run: genetic implications of catching and transporting millions of wild fish for aquaculture

Ellika Faust, Department of Marine Sciences, University of Gothenburg

We provide the first quantitative estimate of corkwing wrasse escaping salmon farms and hybridizing with local populations. The use of wrasse as cleaner fish in salmon farms has increased exponentially over the last decade, where wild-caught fish are transported long distances to be used where local stocks do not exist or cannot meet the demand. Translocations and increased fishing pressure raises concerns of 1) potential overfishing and 2) human-mediated gene flow. We address these two major issues by investigating: 1) population structure for the identification of management units, and 2) the origin of wild corkwing wrasse amidst salmonid farms. Using genetic markers identified with 2bRAD sequencing, we find low diversity and weak population structure among source populations. However, we detect high divergence between source and local populations around farms. By using a panel of high divergent SNPs we quantify the level of gene flow to local populations, finding evidence of extensive hybridization between the divergent populations. Overall, these findings have implications for the increasing use of cleaner fish as parasite control in fish farms, which is both poorly documented and regulated.

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Dynamic variants: the evolution of chromosomal inversions

Emma Berdan, Department of Marine Sciences, University f Gothenburg

Chromosomal inversions contribute widely to adaptation and speciation, yet they present a unique evolutionary puzzle as both their allelic content and frequency evolve in a feedback loop. Here I detail this feedback loop and show results from a simulation study where we quantified the role of the allelic content in determining the long-term fate of the inversion. Our simulations show that recessive deleterious mutations accumulated rapidly on both arrangements with most of them being private to a given arrangement. This leads to overdominance, which can maintain the inversion polymorphism and generate strong non-adaptive divergence between arrangements. The accumulation of mutations can be mitigated by gene conversion but nevertheless usually leads to the fitness decline of at least one homokaryotype. I also detail a surprising result where we observe a shift from background selection to associative overdominance in one or both arrangements. This occurs via the branching of an arrangement into multiple highly divergent haplotypes. Overall these results highlight the dynamic features of inversions by showing how the non-adaptive evolution of allelic content can play a major role in the fate of the inversion.

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Restoring ancestral phenotypes by reduction of plasticity: a general pattern in gene expression during adaptation to new environments in Tribolium castaneum

Eva Koch, University of Sheffield

Plasticity and evolution are two processes how organisms can respond to environmental change, but how both are related and impact each other is still controversial. We studied plastic and evolutionary responses in gene expression of Tribolium castaneum (red flour beetles) after exposure to new environmental conditions that differed from ancestral conditions in temperature, humidity or both. After 20 generations of experimental evolution we could show adaptation to all stress conditions and found it to be accompanied by changes in expression. A majority of ancestral plastic responses in gene expression were reversed during long-term evolution. Evolution compensated plasticity mainly by changing mean expression (shifting intercept of reaction norm), while plasticity was preserved in terms of responding genes and direction of response. However, for genes with largest evolutionary changes in expression levels, we found that a reduction of plasticity in adapted lines contributed to divergence. We were further able to detect a positive correlation between proportion of genes with reversion of the ancestral plasticity and mean fitness per selection line suggesting that large parts of ancestral plasticity became maladaptive on the long-term.

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Identifying the genetic basis of convergent evolution between two species of fishes

James Reeve, Departmen of Marine Sciences, University of Gothenburg

The repeatability of evolution is a commonly discussed topic in population genetics. Do similar patterns of genetic diversity and genetic divergence appear across the genomes of different species that occupy the same environments? To test this questions, whole genome scans were used to identify genetic patterns associated with latitude for two species of fish from the west coast of North America; the threespine stickleback (Gasterosteus aculeatus) and the tubesnout (Aulorhynchus flavidus). Each genome scan revealed Fst and genetic diversity outliers in a given species, which were labelled as candidates loci for local adaptation. These candidates were then compared among species to determine signatures of convergent evolution. No candidates of convergent evolution were identified between the species, indicating that either these species are responding to the same environmental pressure with different genetic changes, or that some unidentified aspect of the environment is leading to divergent patterns of local adaptation. This study shows that two species under the same environmental conditions do not evolve with the same genetic changes. However, more species pairs need to be compared to know how general the genetic basis of convergent evolution is.

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Insights into sexual antagonism via female-limited X chromosome evolution

Jessica Abbott, Department of Biology, Lund University

The concept of sexual antagonism (opposite fitness effects of traits with a shared genetic basis between the sexes) has become key to our understanding of sex chromosome evolution, with the X chromosome being of particular interest for a number of reasons. X-linked loci are known to contribute to the evolution of complex traits, the X is expected to be a hotspot for sexual antagonism, and there are clear predictions regarding the dominance properties of X-linked sexually antagonistic loci. We have therefore carried out a female-limited X-chromosome (FLX) evolution experiment in Drosophila melanogaster, where expression of the wildtype X has been restricted to females for over 100 generations with the help of an FM balancer chromosome. We had two aims with this experiment: to quantify the nature and magnitude of the response to sex-specific selection on the X, and to determine whether X-linked sexually antagonistic loci are preferentially non-additive in nature. We found that body size, development time, locomotory activity and fitness changed as a result of the selection treatment, which are all traits that have previously been characterized as sexually antagonistic. We also found that whole-fly gene expression showed a signature of feminization, and that genes that have been previously characterized as sexually antagonistic were overrepresented. By comparing females that were heterozygous and homozygous for the evolved X’s we also found evidence of non-additive effects on body size and fitness. We thereby confirm many of the predictions about the genetic architecture of X-linked traits.

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The succession of ecological divergence and reproductive isolation in adaptive radiations

Jörgen Ripa, Department of Biology, Lund University

Adaptive radiation, the rapid generation of many species, is an important source of biodiversity and a major constituent of the tree of life. Despite substantial progress, there is still no general theory of the processes and mechanisms of radiations of entire clades, nor a full understanding why some of them are more speciose than others. Here we use a versatile but detailed model of diversification through adaptive radiation, tracking the evolution from a single ancestral species to a fully diversified clade. In our model, evolving clades exploit all ecological opportunities long before reproductive isolation is completed for any of the incipient species. The generation of bona fide biological species, if ever completely attained, happens relatively late during the cladogenesis and is preceded by recurring hybridization events. This decoupling of ecological diversification and reproductive isolation shows that adaptive radiations are not necessarily a sequence of well-defined and isolated speciation events. The single speciation perspective is insufficient for an accurate understanding because an adaptive radiation is the joint evolution of an entire ecological community. Our results also have important implications for how we interpret phylogenetic data and the prevalence of sexual selection as an important reproductive barrier between recently radiated species.

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Genetic trade-offs in reproductive plasticity to hot and cold periods govern responses to temperature fluctuations

Mads Fristrup Schou, Department of Biology, Molecular Ecology and Evolution Lab, Lund University

Substantial efforts have been made to understand how animals cope with extreme temperatures, especially since the realisation that there is accelerated climatic warming. However, such focus has meant that little is known about the evolutionary potential of populations to cope with both highs and lows in temperature, especially in species occupying arid, tropical regions and during critical periods such as reproduction. This is particularly important as species in hotter areas experience greater temperature fluctuations, an effect that is expected to increase in the future. Here we use a unique system, the ostrich, Struthio camelus, where 20 years of data on reproductive success has been collected from controlled breeding attempts under natural temperature conditions (-5 to 45ºC) in South Africa. We found that plasticity in female egg laying behaviour had a significant genetic component and was positively related to annual reproductive success suggesting potential for evolutionary adaptation. However, cold and hot tolerance were tightly interlinked by a negative genetic correlation, that may hinder evolutionary response to selection for thermal plasticity but maintain genetic variation. Our results suggest that the ability of species to respond to increasing temperature fluctuations may be governed by the genetic integration of cold and heat tolerance mechanisms.

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Seascape and gene-scape of eelgrass

Marlene Jahnke, Department of Marine Sciences, University of Gothenburg

The eelgrass Zostera marina is an important foundation species of coastal areas in the Northern Hemisphere, but is continuing to decline. The development of new management tools is therefore urgent in order to prioritize limited resources for protecting meadows most vulnerable to local extinctions and identifying most valuable present and historic meadows to protect and restore, respectively. We used
Lagrangian biophysical modelling and population genetic methods to assess connectivity and health of the meta-population. Both approaches were in very good agreement, and adding demographic modelling based on the genetic and biophysical data, we are able to assess the past, present and future to identify especially vulnerable and valuable meadows. The combination of methods allows the assessment of different temporal and spatial scales at the same time, as well as s ranking of specific meadows according to key genetic, demographic and ecological metrics. We exemplify it’s versatility as a management guide for eelgrass along the Swedish west coast by addressing the key management questions of: How bad is the current state of an area?; How can we best identify MUs?; and Which meadows should be restored or protected?

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Are life-history trade-offs really based on energy allocation?

Martin Lind, Department of Ecology and Genetics, Animal Ecology, Uppsala University

Classic theory upholds that energy trade-offs between reproduction and somatic maintenance underpin the evolution of ageing and lifespan. In contrast, the developmental theory of ageing (DTA) suggests that organismal senescence is caused by suboptimal gene expression in adulthood due to decline in selection gradients with age. The DTA predicts that age-specific optimisation of gene expression can improve survival without fitness costs. Here we investigated consequences for survival, reproduction, egg size and fitness of early-life, adulthood and post-reproductive onset of RNAi knockdown of five “longevity” genes involved in key biological processes in Caenorhabditis elegans. Downregulation of these genes in adulthood and/or during post-reproductive period improves survival, while there was little evidence for a link between impaired reproduction and extended lifespan. Our findings demonstrate that suboptimal gene expression levels after sexual maturation contribute to ageing directly rather than through competitive energy trade-offs between reproduction and somatic maintenance, thus supporting the new theory. Therefore, optimisation of gene expression in adult organisms can simultaneously ameliorate ageing and increase fitness.

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Local adaptation to seasonal cues in a range-expanding butterfly

Mats Ittonen, Department of Zoology, Stockholm University

Range-expanding populations need to adapt to new environments, but lack of genetic variation in marginal populations as well as maladaptive gene flow from the core range may hinder adaptation. Previous studies on adaptation in expanding populations have mainly focused on dispersal ability, while less is known about important life history traits such as seasonal timing in response to photoperiod. Using controlled laboratory experiments we show that populations of the range expanding wall brown butterfly, Lasiommata megera, have, on a relatively small spatial scale, adapted locally to photoperiodic seasonal cues. In long day treatments, caterpillars from the northern range margin in central Sweden were more likely to enter diapause than caterpillars from southern Sweden. Although temperature also affected diapause induction, there were no signs of similar differentiation among populations in the response to temperature. Northern range margin populations seem to have rapidly evolved their response to photoperiod to match local season length and photoperiodic conditions. This is a crucial adaptation for correct life cycle timing and is in many insects likely to be important for successful colonization of novel areas during range expansions across latitudes.

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Misinformation in a New Climate: Evolution of seasonal polyphenism under climate change

Matthew Nielsen, Department of Zoology, Stockholm University

Many organisms use photoperiod as a cue for seasonal changes, but photoperiod has remained unchanged as temperatures have increased over recent decades, creating a potential cue-environment mismatch. We studied whether evolution has corrected for this mismatch in Colias eurytheme butterflies, a species that uses photoperiod as a cue for thermoregulatory color plasticity. Using the contemporary population, we reconstructed a past study from the 1970s of the photoperiodic reaction norm for these butterflies' wing color. We found these butterflies have gotten brighter at short photoperiods over the last ~50 years, but remained unchanged at long photoperiods. This change corresponds to increased spring temperatures but little change in summer temperatures at our field site, indicating the potential for evolution to, at least partially, correct for the photoperiod-temperature mismatch created by climate change.

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Is phenotypic plasticity the leader of adaptive evolution?

Miguel Brun-Usan, Department of Biology, Evolutionary ecology, Lund University

Adaptive evolution would be highly favoured if new phenotypic variation is well aligned with adaptive demands. This possibility is often neglected because we lack a mechanistic explanation about how that would be possible. In this work, we provide such an explanation; development can turn random genetic variation into adaptive phenotypic variation if two requirements are met:
First, the phenotypic consequences of genetic mutations and environmental perturbations must be non-independent, so that selecting for plasticity could affect how organisms respond to genetic variation and vice versa. By means of different models of development, we demonstrate that this is generally the case.
Second, natural selection must be more efficient in adapting plasticity than in adapting the genotype-phenotype map. We show that this is, indeed, a widespread phenomenon: Selection for plasticity is typically fine-grained (and efficient) because individuals experience different environments during their lifetime and are selected on the basis of that within-lifetime variation. Conversely, selection on responses to genetic variation is generally coarse-grained and less efficient.
The emerging picture is that adaptive phenotypic variation (aligned with the environmental requirements) is first acquired through plasticity due to the efficient selection on it, and then is transferred to the genotype-phenotype map due to developmental linkage.

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Parallelism and plasticity in the adaptive radiation of Anolis lizards

Nathalie Feiner, Department of Biology, Evolutionary ecology, Lund University

Darwin described evolution as the source of ‘endless forms’. However, a closer look reveals that evolution is often on repeat. While such parallel evolution typically relies on similarities in selective pressures, it also depends on the developmental processes that make phenotypes available to selection. One of these processes is developmental plasticity, which may be particularly conducive to parallel evolution. Anolis lizards offer the opportunity to put this role of developmental bias to the test. Following colonization of the four Greater Antillean islands, Anolis lizards independently and repeatedly evolved six ecomorphs that are well adapted to running or climbing in different microhabitats. By quantifying the morphology of the locomotor apparatus of 95 species, we find a moderate, but consistent, parallelism between ecomorphs evolving on the four islands. However, we find limited support for an alignment between these morphological differences between ecomorphs and the morphological changes in lizards reared in different microhabitats. Furthermore, our experiments suggest that plastic responses are not increasing locomotor performance and therefore unlikely to guide adaptive evolution. Although environmental effects on bone growth are considered promising candidates for plasticity-driven evolution, plasticity is not taking the lead in the adaptive radiation of Anolis ecomorphs.

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The effects of complex life-cycles on evolutionary diversification

Paula Vasconcelos, Department of Ecology and Genetics, Animal Ecology, Uppsala University

Complex life-cycles in which organisms undergo ontogenetic niche shifts couple different habitats that each host a life stage. Competition for resources in such organisms is mediated by separate traits in the different life-stages, so ecological opportunities for diversification due to disruptive selection can be present at the juvenile stage, the adult stage, or both. We investigate a consumer-resource model of a species with a life-cycle consisting of two life-stages. Juveniles feed on two juvenile-specific resources with juvenile-specific feeding-efficiencies, and adults feed on two adult-specific resources with adult-specific feeding-efficiencies. This system presents alternate equilibria, one juvenile-dominated and another adult-dominated, and which state the system exhibits depends on resource productivity and consumer efficiency. We find that disruptive selection can occur at the juvenile stage, the adult stage, or both simultaneously; diversification through evolutionary branching is more likely in the dominating stage, as that is the one in which competition is stronger; and the endpoints of the evolutionary dynamics are either one generalist phenotype at both stages, two coexisting phenotypes specialized for different resources at one stage but generalists at the other, or two phenotypes that are specialized for different resources at both stages.

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Inbreeding avoidance in animals: a meta-analysis

Raissa de Boer, Department of Zoology, Stockholm University

It is often assumed that animals should avoid inbreeding because of inbreeding depression. Yet, theoretical studies show that the inclusive fitness benefits of inbreeding can lead to tolerance or even preference of inbreeding. Despite many years of experimental research it remains unclear how common different inbreeding strategies are. Here, we performed a large meta - analysis of experimental studies. We show that over 139 experimental studies of 88 animal species, inbreeding tolerance and preference are equally common as inbreeding avoidance and identify interesting patterns across animals.

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The evolutionary significance of structural genomic variation

Rebekah Oomen1,2, Claire Mérot, Anna Tigano, and Maren Wellenreuther

1. Centre for Ecological and Evolutionary Synthesis, University of Oslo, Blindernveien 31, 0371 Oslo, Norway
2. Centre for Coastal Research, University of Agder, Universitetsveien 25, 4630 Kristiansand, Norway

Structural genomic variants (SVs) are ubiquitous and play a major role in adaptation and speciation. Comparative and, later, population genomics have mainly focused on gene duplications and large-effect inversions, respectively, in addition to single nucleotide polymorphisms (SNPs). Yet, the full spectrum of SVs, including copy number variants (e.g., indels, repeats, duplications) and balanced chromosomal rearrangements (e.g., translocations, fissions/fusions, inversions) of various sizes, appears to comprise more standing genetic variation than SNPs but has not been widely integrated into population genomic analyses. A lack of common framework for studying all SVs is hampering progress towards a more systematic assessment of their evolutionary significance. We review how different types of SVs affect ecological and evolutionary processes at different levels of biological organization. We attempt to unify investigations of SVs across systems by clarifying definitions and making recommendations for future studies, including a roadmap for the cataloguing and integration of SVs in eco-evolutionary studies. In doing so, we lay the foundation for population genomic, theoretical, and experimental approaches to understanding how the full spectrum of SVs impacts ecological and evolutionary processes.

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The evolutionary developmental biology of a female polymorphism in anolis lizards

Robin Pranter, Department of Biology, Lund University

Animal color patterns are ecologically significant but developmentally complex traits. By understanding how they develop we can predict why some patterns evolve while others do not. The brown anole lizard has a female polymorphism; some females have a chevron pattern while others have a diamond-shaped pattern. Here, I show that the morphs are inherited by a single biallelic Mendelian locus and identify the gene responsible for this pattern polymorphism. The gene encodes coiled-coil domains which are known to regulate cell migration, suggesting that the pattern form as the neural crest cells that will become chromatophores (cells containing pigments and/or structural color) migrate to their locations in the skin. To test this hypothesis and to identify effector genes, I studied differential gene expression in the developing skin between the two morphs, traced their expression through embryonic development and observed their spatial expression patterns in the developing embryos. Six genes are differentially expressed. Several of the investigated genes have interesting expression patterns seemingly relevant for the directionality and spatial constraint of the color patterns.

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Strong reproductive isolation in Littorina

Roger Butlin, Department of Animal and Plant Sciences, University of Sheffield and Department of Marine Sciences, University of Gothenburg

Strong reproductive isolation and the completion of speciation are thought to require the coupling of multiple barriers to gene flow. How this is achieved remains largely unknown with much speciation research focused on the first barriers to evolve, for example in response to divergent natural selection. In Littorina saxatilis, divergent ecotypes show a genome-wide barrier to gene flow but reproductive isolation is far from complete. Here, we contrast this pattern with the relationship between L. saxatilis and its sister species L. arcana. Despite an apparent lack of ecological differentiation between these species, and intimate sympatry, we show that reproductive isolation between them is now complete, or very nearly so. Demographic models suggest that they did exchange genes in the past. We speculate about how speciation has been completed in this case.

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Genomic divergence in ecotypes of Atlantic cod: impact of structural variants, degree of gene flow and local adaptation

Sissel Jentoft, CEES, University of Oslo

Genomic tools have in the recent past given us new and valuable insight into the important role of structural variants in maintaining genomic divergence despite high connectivity in marine systems. For the iconic Atlantic cod (Gadus morhua) – one of the most economically important fish species distributed throughout the North Atlantic Ocean – three large genomic inversions (on LG1, 2, and 7) have been found to discriminate between two well-known ecotypes of Atlantic cod: the migratory North East Arctic cod (NEA) and the non-migratory Norwegian Coastal (NC) cod. The NEA cod migrates from feeding grounds in the Barents Sea to the coast of Norway to spawn, whereas the Norwegian coastal cod stays in warmer, shallower water all year round. The two cod ecotypes also differ in other life-history parameters, e.g., age and size at maturity and size distribution. Whether these ecotypes should be defined as genetically distinct populations, however, is still an ongoing debate.
To further infer the impact of these inversions on local adaptation and separation of the two ecotypes at the genome-wide level, we characterize the degree of gene flow between non-migratory NC cod and migratory NEA cod along a North-South latitudinal and temperature gradient with high-to-low degrees of overlap in spawning areas. These analyses indicate genome-wide differentiation, in addition to the chromosomal inversions, where the degree of gene flow is less prominent.

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Unfolding the elusive migratory direction genes in the willow warbler genome

Staffan Bensch, Department of Biology, Molecular Ecology and Evolution Lab, Lund University

Understanding the genetic architecture of the migratory program is a research field in its infancy - no gene has so far been conclusively identified as linked to the expression of the migratory phenotype. The willow warbler Phylloscopus trochilus has two migratory divides located in central Scandinavia and south of the Baltic Sea. Smaller and greener birds of the subspecies trochilus breed in southern Scandinavia and migrate towards SW for wintering in western Africa whereas larger, grayer birds of the subspecies acredula breed in northern Scandinavia and Finland and migrate towards SE for wintering in east and south Africa. Absence of differences at neutral loci between the subspecies suggested that the phenotypic trait differences have evolved within the last 10,000 years during the process of postglacial colonization of northern Europe. New data from whole genome resequencing and genotyped birds with geolocator tracks from the Scandinavian hybrid zone demonstrate that finding genes involved in the migratory program is challenging, but that the willow warbler system provides promising directions of research that might finally lead to a breakthrough in this field.

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The potential for rapid evolution to increase ecosystem resilience to climate change: A call to action.

Steve Palumbi, Hopkins Marine Station, Stanford University, USA

In the face of rapid changes in climate, many species are faced with the need to migrate, acclimate, or adapt. To understand the potential of novel environmental stress to drive evolution towards climate resilience, we have been concentrating on three aspects of adaptability in ecosystems, with particular focus on coral reefs. First is the level of phenotypic and genetic variation in traits affected by climate: in this case the key trait is heat sensitivity of the coral-algal symbiosis. The second is the level of selection and the level of response in modeled populations, particularly whether schemes for assisted evolution are likely to significantly improve evolutionary outcomes. The third is the genomic architecture of heat sensitivity and its possible role in reducing genetic load for heat sensitive traits affected by many loci. I will illustrate our approach to these levels with field surveys of Palau reefs for individual corals with heat resistance, eco-evolutionary models of population stability with different levels of genetic variation, and genome-wide explorations of SNPs responsible for heat resistant traits and their linkage. Many other ecosystems are also at severe risk due to future climate change, and evolutionary science is poised to be able to help show which traits, species, and ecosystems may be able to substantially evolve.

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Phylogenetically conserved modules of gene expression help explain host plant memory in butterflies

Sören Nylin, Department of Zoology, Stockholm University

The proximate mechanisms explaining phylogenetic patterns of insect-plant associations are not well understood. We propose that host plant adaptations can profitably be understood as host-specific modules of co-expressed genes, evolving over time after first colonization of a novel host. We performed a phylogenetically informed genomics study of four related butterfly species in Polygonia and Nymphalis, rearing larvae on the hosts Urtica, Salix and Ribes. Gene expression on the respective host plants was similar across species; in the case of the ancestral host Urtica this included two butterflies for which it is no longer a host. We found distinct and almost mutually exclusive modules of gene expression on Urtica and Ribes, suggestive of alternative developmental pathways that might explain specialization on Ribes in a clade of North American Polygonia. Gene expression on Salix in contrast showed much overlap with the other two hosts, so that this plant may have provided an evolutionary bridge from Urtica, over Salix, to the most recent colonization of Ribes. We conclude that the study of modularity in gene expression is a powerful tool in explaining insect-plant association dynamics, and that conserved modules may help explain the host plant “memory” allowing recurrence of ancestral hosts.

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Evidence of Adaptation and Maladaptation in a California oak species, Quercus lobata

Victoria L. Sork, Department of Ecology and Evolutionary Biology, University of California Los Angeles

The ability of plants to grow well where they grow is fundamental to the fitness of the individual. For long-lived tree species, the climate environment of a newly established seedling may change significantly during the time it develops into a reproductive adult. Such temporal changes may influence how trees adapt to the local climates and, at the same time, climate differences across a species range may shape how populations adapt to the local climates. Our research group has utilized multiple approaches to gather evidence for local adaptation in natural populations of a California endemic oak species, Quercus lobata. First, we have conducted landscape genomic analysis of trees sampled throughout the species range to identify associations between genetic and climatic gradients. Second, we measured genetic differentiation and phenotypic plasticity measured on families gathered species-wide maternal trees grown in two common gardens to test the extent to which drought-related traits differ across climate gradients. A particularly unexpected result is that Q. lobata shows an adaptational lag in relative growth rates in association with current climates. Third, we investigated climate-associated epigenetic patterns for its potential role in local adaptation by assessing DNA methylation in natural populations and in their progeny grown in two common gardens. Fourth, we studied experimentally treated young seedlings to demonstrate population differences in gene expression response to soil drying treatments. Throughout these studies, we have found genes and traits that are correlated with tree response to climate. Collectively, these finding provide compelling evidence of local adaptation in a long-lived tree species, with the surprising result that some populations may be out of sync with current climate.

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Evolution in Sweden 2020 Abstracts-talks

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