Showing papers by "Roger K. Butlin published in 2018"

Clines on the seashore: The genomic architecture underlying rapid divergence in the face of gene flow

Abstract: Adaptive divergence and speciation may happen despite opposition by gene flow. Identifying the genomic basis underlying divergence with gene flow is a major task in evolutionary genomics. Most approaches (e.g., outlier scans) focus on genomic regions of high differentiation. However, not all genomic architectures potentially underlying divergence are expected to show extreme differentiation. Here, we develop an approach that combines hybrid zone analysis (i.e., focuses on spatial patterns of allele frequency change) with system-specific simulations to identify loci inconsistent with neutral evolution. We apply this to a genome-wide SNP set from an ideally suited study organism, the intertidal snail Littorina saxatilis, which shows primary divergence between ecotypes associated with different shore habitats. We detect many SNPs with clinal patterns, most of which are consistent with neutrality. Among non-neutral SNPs, most are located within three large putative inversions differentiating ecotypes. Many non-neutral SNPs show relatively low levels of differentiation. We discuss potential reasons for this pattern, including loose linkage to selected variants, polygenic adaptation and a component of balancing selection within populations (which may be expected for inversions). Our work is in line with theory predicting a role for inversions in divergence, and emphasizes that genomic regions contributing to divergence may not always be accessible with methods purely based on allele frequency differences. These conclusions call for approaches that take spatial patterns of allele frequency change into account in other systems.

Inter and Intraspecific Genomic Divergence in Drosophila montana Shows Evidence for Cold Adaptation.

Abstract: The genomes of species that are ecological specialists will likely contain signatures of genomic adaptation to their niche. However, distinguishing genes related to ecological specialism from other sources of selection and more random changes is a challenge. Here, we describe the genome of Drosophila montana, which is the most extremely cold-adapted Drosophila species known. We use branch tests to identify genes showing accelerated divergence in contrasts between cold- and warm-adapted species and identify about 250 genes that show differences, possibly driven by a lower synonymous substitution rate in cold-adapted species. We also look for evidence of accelerated divergence between D. montana and D. virilis, a previously sequenced relative, but do not find strong evidence for divergent selection on coding sequence variation. Divergent genes are involved in a variety of functions, including cuticular and olfactory processes. Finally, we also resequenced three populations of D. montana from across its ecological and geographic range. Outlier loci were more likely to be found on the X chromosome and there was a greater than expected overlap between population outliers and those genes implicated in cold adaptation between Drosophila species, implying some continuity of selective process at these different evolutionary scales.

Sexes and species as rival units of niche saturation during community assembly

Abstract: Aim: Community assembly is traditionally assumed to result from speciation and colonization mediated by available niche space. This paradigm is expanded by the theory that niche space can also be saturated by intersexual adaptive divergence (ecological sexual dimorphism) when interspecific competition is relaxed. This theory (here termed ‘niche-packing equivalence’) predicts that the evolution of ecological sexual dimorphism constrains the ecological opportunity that would otherwise lead to ecological speciation or colonization, and that saturation of niches by different species constrains divergent selection for divergence between the sexes. Therefore, sexes and species are equivalent, yet antagonistic units of niche occupation. We present the most comprehensive test of the niche-packing equivalence theory at ecological time-scales (assemblage level) to date. Location: South America Major taxa studied: Liolaemus lizards. Methods: We identified 23 Liolaemus assemblages varying in species richness and sexual size dimorphism (SSD), distributed across a wide environmental range. We used mixed effects models, permutation tests and Markov Chain Monte Carlo (MCMC) regressions to quantify the relationship between SSD and species richness. We then partitioned the body size niche dimension between the sexes and amongst species, and tested for non-overlapping body size distributions. We regressed SSD and species richness of each assemblage against environmental predictors, using multi-model inference and structural equation modelling. Results: Sexual dimorphism declines with increasing species richness, and a strong signal of tension between the two remains following phylogenetic control. This pattern is accompanied by evidence of constraints on body-size partitioning amongst species and between the sexes: the two units of niche saturation tend not to overlap. However, across assemblages, species richness and SSD correlate with different environmental variables, suggesting that their tension is context-specific. Main conclusions: Our evidence supports the prediction that sexual dimorphism and species richness are alternative outcomes of adaptive radiation. However, this antagonism is mediated by a suite of environmental predictors that influence dimorphism and species richness differentially.

Are assortative mating and genital divergence driven by reinforcement

Abstract: The evolution of assortative mating is a key part of the speciation process. Stronger assortment, or greater divergence in mating traits, between species pairs with overlapping ranges is commonly observed, but possible causes of this pattern of reproductive character displacement are difficult to distinguish. We use a multidisciplinary approach to provide a rare example where it is possible to distinguish among hypotheses concerning the evolution of reproductive character displacement. We build on an earlier comparative analysis that illustrated a strong pattern of greater divergence in penis form between pairs of sister species with overlapping ranges than between allopatric sister-species pairs, in a large clade of marine gastropods (Littorinidae). We investigate both assortative mating and divergence in male genitalia in one of the sister-species pairs, discriminating among three contrasting processes each of which can generate a pattern of reproductive character displacement: reinforcement, reproductive interference and the Templeton effect. We demonstrate reproductive character displacement in assortative mating, but not in genital form between this pair of sister species and use demographic models to distinguish among the different processes. Our results support a model with no gene flow since secondary contact and thus favor reproductive interference as the cause of reproductive character displacement for mate choice, rather than reinforcement. High gene flow within species argues against the Templeton effect. Secondary contact appears to have had little impact on genital divergence.

Genomic architecture of parallel ecological divergence: beyond a single environmental contrast

Abstract: The genetic basis of parallel ecological divergence provides important clues to the operation of natural selection and the predictability of evolution. Many examples exist where binary environmental contrasts seem to drive parallel divergence. However, this simplified view can conceal important components of parallel divergence because environmental variation is often more complex. Here, we disentangle the genetic basis of parallel divergence across two axes of environmental differentiation (crab-predation vs. wave-action and low-shore vs. high-shore habitat contrasts) in the marine snail Littorina saxatilis, a well-established natural system of parallel ecological divergence. We used whole-genome resequencing across multiple instances of these two environmental axes, at local and regional scales from Spain to Sweden. Overall, sharing of genetic differentiation is generally low but it is highly heterogeneous across the genome and increases at smaller spatial scales. We identified genomic regions, both overlapping and non-overlapping with recently described candidate chromosomal inversions, that are differentially involved in adaptation to each of the environmental axis. Thus, the evolution of parallel divergence in L. saxatilis is largely determined by the joint action of geography, history, genomic architecture and congruence between environmental axes. We argue that the maintenance of standing variation, perhaps as balanced polymorphism, and/or the re-distribution of adaptive variants via gene flow can facilitate parallel divergence in multiple directions as an adaptive response to heterogeneous environments.

Conflict between heterozygote advantage and hybrid incompatibility in haplodiploids (and sex chromosomes)

Abstract: In many diploid species the sex chromosomes play a special role in mediating reproductive isolation. In haplodiploids, where females are diploid and males haploid, the whole genome behaves similarly to the X/Z chromosomes of diploids. Therefore, haplodiploid systems can serve as a model for the role of sex chromosomes in speciation and hybridization. A previously described population of Finnish Formica wood ants displays genome-wide signs of ploidally and sexually antagonistic selection resulting from hybridization. Here, hybrid females have increased survivorship but hybrid males are inviable. To understand how the unusual hybrid population may be maintained, we developed a mathematical model with hybrid incompatibility, female heterozygote advantage, recombination, and assortative mating. The rugged fitness landscape resulting from the co-occurrence of heterozygote advantage and hybrid incompatibility results in a sexual conflict in haplodiploids, which is caused by the ploidy difference. Thus, whereas heterozygote advantage always promotes long-term polymorphism in diploids, we find various outcomes in haplodiploids in which the population stabilizes either in favor of males, females, or via maximizing the number of introgressed individuals. We discuss these outcomes with respect to the potential long-term fate of the Finnish wood ant population, and provide approximations for the extension of the model to multiple incompatibilities. Moreover, we highlight the general implications of our results for speciation and hybridization in haplodiploids versus diploids, and how the described fitness relationships could contribute to the outstanding role of sex chromosomes as hotspots of sexual antagonism and genes involved in speciation. This article is protected by copyright. All rights reserved.

Hybridizing wood ants allow testing for natural selection at candidate barrier loci underlying speciation

Abstract: The current aim of speciation research is to pin-point which genomic regions serve as barriers for gene flow and drive divergence during speciation. At the barrier loci, natural selection is assumed to act against gene flow. Many current approaches, however, rely on indirect measures of gene flow and natural selection. Here we present a system to test the action of natural selection at candidate barrier loci in a natural population. We utilize haplodiploidy to identify candidate barrier loci between two wood ant species and combine survival analysis with SNP genotyping to test for natural selection acting at candidate barrier loci. We find multiple candidate loci distributed over a large part of the genome displaying signatures of natural selection. Surprisingly, however, we find that a proportion of the barrier loci show leakage between data sets collected in 2004 and 2014. We also show that, on average selection favored introgression at candidate barrier loci in year 2014. We discuss reasons for barrier leakage, including environment-dependent selection, formation of compatible combinations of parental alleles and recombination breaking associations between causal and hitchhiking loci. Integrating data on survival allows us to move beyond genome scan studies, bringing additional evidence for natural selection acting in genomic islands of divergence.

Inter- and intra-specific genomic divergence in Drosophila montana shows evidence for cold adaptation

Abstract: The genomes of species that are ecological specialists will likely contain signatures of genomic adaptation to their niche. However, distinguishing genes related to their ecological specialism from other sources of selection and more random changes is a challenge. Here we describe the genome of Drosophila montana, the most extremely cold-adapted Drosophila species. We describe the genome, which is similar in size and gene content to most Drosophila species. We look for evidence of accelerated divergence from a previously sequenced relative, and do not find strong evidence for divergent selection on coding sequence variation. We use branch tests to identify genes showing accelerated divergence in contrasts between cold- and warm adapted species and identify about 250 genes that show differences, possibly driven by a lower synonymous substitution rate in cold-adapted species. Divergent genes are involved in a variety of functions, including cuticular and olfactory processes. We also re-sequenced three populations of D. montana representing its ecological and geographic range. Outlier loci were more likely to be found on the X chromosome and there was a greater than expected overlap between population outliers and those genes implicated in cold adaptation between Drosophila species, implying some continuity of selective process at these different evolutionary scales.

Phylogenomics of the adaptive radiation of Triturus newts supports gradual ecological niche expansion towards an incrementally aquatic lifestyle

Abstract: Understanding the course of eco-morphological evolution in adaptive radiations is challenging as the phylogenetic relationships among the species involved are typically difficult to resolve. Newts of the genus Triturus (marbled and crested newts) are a well-studied case: they exhibit substantial variation in the number of trunk vertebrae (NTV) and a higher NTV corresponds to a longer annual aquatic period. Because the Triturus phylogeny is still unresolved, the evolutionary pathway for NTV and annual aquatic period is unclear. To resolve the phylogeny of Triturus, we generate a c. 6,000 transcriptome-derived marker data set using a custom target enrichment probe set, and conduct phylogenetic analyses including: 1) data concatenation with RAxML, 2) gene tree summary with ASTRAL, and 3) species tree estimation with SNAPP. All analyses consistently result in the same, highly supported topology. Our new phylogenetic hypothesis only requires the minimal number of inferred changes in NTV count to explain the NTV radiation observed today. This suggests that, while diversification in body shape allowed ecological expansion in Triturus to encompass an increasingly aquatic life style, body shape evolution was phylogenetically constrained.