Faster Rates of Molecular Sequence Evolution in Reproduction-Related Genes and in Species with Hypodermic Sperm Morphologies

Sexual selection drives the evolution of many striking behaviors and morphologies and should leave signatures of selection at loci underlying these phenotypes. However, although loci thought to be under sexual selection often evolve rapidly, few studies have contrasted rates of molecular sequence evolution at such loci across lineages with different sexual selection contexts. Furthermore, work has focused on separate sexed animals, neglecting alternative sexual systems. We investigate rates of molecular sequence evolution in hermaphroditic flatworms of the genus Macrostomum. Specifically, we compare species that exhibit contrasting sperm morphologies, strongly associated with multiple convergent shifts in the mating strategy, reflecting different sexual selection contexts. Species donating and receiving sperm in every mating have sperm with bristles, likely to prevent sperm removal. Meanwhile, species that hypodermically inject sperm lack bristles, potentially as an adaptation to the environment experienced by hypodermic sperm. Combining functional annotations from the model, Macrostomum lignano, with transcriptomes from 93 congeners, we find genus-wide faster sequence evolution in reproduction-related versus ubiquitously expressed genes, consistent with stronger sexual selection on the former. Additionally, species with hypodermic sperm morphologies had elevated molecular sequence evolution, regardless of a gene's functional annotation. These genome-wide patterns suggest reduced selection efficiency following shifts to hypodermic mating, possibly due to higher selfing rates in these species. Moreover, we find little evidence for convergent amino acid changes across species. Our work not only shows that reproduction-related genes evolve rapidly also in hermaphroditic animals, but also that well-replicated contrasts of different sexual selection contexts can reveal underappreciated genome-wide effects

The genetic basis and adult reproductive consequences of developmental thermal plasticity

Increasing temperature and thermal variability generate profound selection on populations. Given the fast rate of environmental change, understanding the role of plasticity and genetic adaptation in response to increasing temperatures is critical. This may be especially true for thermal effects on reproductive traits in which thermal fertility limits at high temperatures may be lower than for survival traits. Consequences of changing environments during development on adult phenotypes may be particularly problematic for core traits such as reproduction that begin early in development. Here we examine the consequences of developmental thermal plasticity on subsequent adult reproductive traits and its genetic basis. We used a panel of Drosophila melanogaster (the Drosophila Genetic Reference Panel; DGRP) in which male fertility performance was previously defined as either showing relatively little (status = ‘high’-performing lines) or substantial (‘low’-performing lines) decline when exposed to increasing developmental temperatures. We used a thermal reaction norm approach to quantify variation in the consequences of developmental thermal plasticity on multiple adult reproductive traits, including sex-specific responses, and to identify candidate genes underlying such variation. Developmental thermal stress impacted the means and thermal reaction norms of all reproductive traits except offspring sex ratio. Mating success declined as temperature increased with no difference between high and low lines, whereas increasing temperature resulted in declines for both male and female fertility and productivity but depended on line status. Fertility and offspring number were positively correlated within and between the sexes across lines, but males were more affected than females. We identified 933 SNPs with significant evolved genetic differentiation between high and low lines. In all, 54 of these lie within genomic windows of overall high differentiation, have significant effects of genotype on the male thermal reaction norm for productivity and are associated with 16 genes enriched for phenotypes affecting reproduction, stress responses and autophagy in Drosophila and other organisms. Our results illustrate considerable plasticity in male thermal limits on several reproductive traits following development at high temperature, and we identify differentiated loci with relevant phenotypic effects that may contribute to this population variation. While our work is on a single population, phenotypic results align with an increasing number of studies demonstrating the potential for stronger selection of thermal stress on reproductive traits, particularly in males. Such large fitness costs may have both short- and long-term consequences for the evolution of populations in response to a warming world.info:eu-repo/semantics/publishedVersio

Competition for access to mates predicts female-specific ornamentation and male investment in relative testis size

Sexually selected ornaments are highly variable and the factors that drive variation in ornament expression are not always clear. Rare instances of female‐specific ornament evolution (such as in some dance fly species) are particularly puzzling. While some evidence suggests that such rare instances represent straightforward reversals of sexual selection intensity, the distinct nature of trade‐offs between ornaments and offspring pose special constraints in females. To examine whether competition for access to mates generally favours heightened ornament expression, we built a phylogeny and conducted a comparative analysis of Empidinae dance fly taxa that display female‐specific ornaments. We show that species with more female‐biased operational sex ratios in lek‐like mating swarms have greater female ornamentation, and in taxa with more ornate females, male relative testis investment is increased. These findings support the hypothesis that ornament diversity in dance flies depends on female receptivity to mates, which is associated with contests for nutritious nuptial gifts provided by males. Moreover, our results suggest that increases in female receptivity lead to higher levels of sperm competition among males. The incidence of both heightened pre‐mating sexual selection on females and post‐mating selection on males contradicts assertions that sex‐roles are straightforwardly reversed in dance flies

Purifying selection in corvids is less efficient on islands

Funding was provided by the European Research Council (ERCStG-336536 FuncSpecGen to J.B.W.W.), the Swedish Research Council Vetenskapsrådet (621-2013-4510 to J.B.W.W.), the Knut and Alice Wallenberg Foundation (to J.B.W.W.), the Lawski foundation (to V.E.K. and J.B.W.W.), the German Research Foundation (KU 3402/1-1 to V.E.K.), the UK’s Biotechnology and Biological Sciences Research Council (BB/G023913/2 to C.R.), and the New Zealand Marsden Fund (to G.R.H.).Theory predicts that deleterious mutations accumulate more readily in small populations. As a consequence, mutation load is expected to be elevated in species where life-history strategies and geographic or historical contingencies reduce the number of reproducing individuals. Yet, few studies have empirically tested this prediction using genome-wide data in a comparative framework. We collected whole-genome sequencing data for 147 individuals across seven crow species (Corvus spp.). For each species, we estimated the distribution of fitness effects of deleterious mutations and compared it with proxies of the effective population size Ne. Island species with comparatively smaller geographic range sizes had a significantly increased mutation load. These results support the view that small populations have an elevated risk of mutational meltdown, which may contribute to the higher extinction rates observed in island species.Publisher PDFPeer reviewe

A genome-wide investigation of adaptive signatures in protein-coding genes related to tool behaviour in New Caledonian and Hawaiian crows

Funding: A David Phillips Fellowship to C.R. from the UK’s Biotechnology and Biological Sciences Research Council (BBSRC; grant BB/G023913/2). Further funding for personnel and data generation of the remaining species was provided by the European Research Council (ERCStG-336536 FuncSpecGen to J.B.W.W.), the Swedish Research Council Vetenskapsrådet (621-2013-4510 to J.B.W.W.), the Knut and Alice Wallenberg Foundation (to J.B.W.W.), the Lawski foundation (to V.E.K. and J.B.W.W.) and the German Research Foundation (KU 3402/1-1 to V.E.K.). A Marsden Fund Grant to G.R.H., R.D.G. and N.J.G. from the Royal Society of New Zealand (UOA1208), a Japanese Society for Promotion of Science Postdoctoral Fellowship (H.A.), together with funding from University of Auckland (G.R.H. and R.D.G.), the Department of Linguistic and Cultural Evolution at the Max Planck Institute for the Science of Human History, and University of Otago (N.J.G.). N.D. acknowledges funding from the Swiss National Science Foundation (P2SKP3_165031 and P300PA_177845) and the Carl Tryggers Foundation.Very few animals habitually manufacture and use tools. It has been suggested that advanced tool behaviour co-evolves with a suite of behavioural, morphological and life-history traits. In fact, there are indications for such an adaptive complex in tool-using crows (genus Corvus species). Here, we sequenced the genomes of two habitually tool-using and ten non-tool-using crow species to search for genomic signatures associated with a tool-using lifestyle. Using comparative genomic and population genetic approaches, we screened for signals of selection in protein-coding genes in the tool-using New Caledonian and Hawaiian crows. While we detected signals of recent selection in New Caledonian crows near genes associated with bill morphology, our data indicate that genetic changes in these two lineages are surprisingly subtle, with little evidence at present for convergence. We explore the biological explanations for these findings, such as the relative roles of gene regulation and protein-coding changes, as well as the possibility that statistical power to detect selection in recently diverged lineages may have been insufficient. Our study contributes to a growing body of literature aiming to decipher the genetic basis of recently evolved complex behaviour.PostprintPeer reviewe

Assessing Recent Selection and Functionality at Long Non-Coding RNA Loci in the Mouse Genome

This work was supported by the Biotechnology and Biological Sciences Research Council and The Wellcome Trust. A.N. was supported by the Swiss National Science Foundation (Grant: PZ00P3_142636). H.K. was supported by the European Research Council Starting (Grant: 242597, SexGenTransEvolution) and the Swiss National Science Foundation (Grants: 130287 and 146474).Long noncoding RNAs (lncRNAs) are one of the most intensively studied groups of noncoding elements. Debate continues over what proportion of lncRNAs are functional or merely represent transcriptional noise. Although characterization of individual lncRNAs has identified approximately 200 functional loci across the Eukarya, general surveys have found only modest or no evidence of long-term evolutionary conservation. Although this lack of conservation suggests that most lncRNAs are nonfunctional, the possibility remains that some represent recent evolutionary innovations. We examine recent selection pressures acting on lncRNAs in mouse populations. We compare patterns of within-species nucleotide variation at approximately 10,000 lncRNA loci in a cohort of the wild house mouse, Mus musculus castaneus, with between-species nucleotide divergence from the rat (Rattus norvegicus). Loci under selective constraint are expected to show reduced nucleotide diversity and divergence. We find limited evidence of sequence conservation compared with putatively neutrally evolving ancestral repeats (ARs). Comparisons of sequence diversity and divergence between ARs, protein-coding (PC) exons and lncRNAs, and the associated flanking regions, show weak, but significantly lower levels of sequence diversity and divergence at lncRNAs compared with ARs. lncRNAs conserved deep in the vertebrate phylogeny show lower within-species sequence diversity than lncRNAs in general. A set of 74 functionally characterized lncRNAs show levels of diversity and divergence comparable to PC exons, suggesting that these lncRNAs are under substantial selective constraints. Our results suggest that, in mouse populations, most lncRNA loci evolve at rates similar to ARs, whereas older lncRNAs tend to show signals of selection similar to PC genes.PostprintPeer reviewe

The Genome and Methylome of a Beetle with Complex Social Behavior,Nicrophorus vespilloides(Coleoptera: Silphidae)

Testing for conserved and novelmechanisms underlying phenotypic evolution requires a diversity of genomes available for comparisonspanning multiple independent lineages. For example, complex social behavior in insects has been investigated primarily witheusocial lineages, nearly all of which are Hymenoptera. If conserved genomic influences on sociality do exist, we need data from awider range of taxa that also vary in their levels of sociality. Here,we present the assembled and annotated genome of the subsocialbeetle Nicrophorus vespilloides, a species long used to investigate evolutionary questions of complex social behavior. We used thisgenome to address two questions. First, do aspects of life history, such as using a carcass to breed, predict overlap in gene modelsmore strongly than phylogeny? We found that the overlap in gene models was similar between N. vespilloides and all other insectgroups regardless of life history. Second, like other insects with highly developed social behavior but unlike other beetles, doesN. vespilloides have DNA methylation?We found strong evidence for an active DNA methylation system. The distribution of methylationwassimilar to other insects with exons having themostmethylatedCpGs. Methylation status appears highly conserved; 85%of themethylated genes in N. vespilloides are alsomethylated in the hymentopteran Nasonia vitripennis. The addition of this genomeadds a coleopteran resource to answer questions about the evolution and mechanistic basis of sociality and to address questionsabout the potential role of methylation in social behavior

Genomic analysis of European Drosophila melanogaster populations reveals longitudinal structure, continent-wide selection, and previously unknown DNA viruses

Genetic variation is the fuel of evolution, with standing genetic variation especially important for short-term evolution and local adaptation. To date, studies of spatiotemporal patterns of genetic variation in natural populations have been challenging, as comprehensive sampling is logistically difficult, and sequencing of entire populations costly. Here, we address these issues using a collaborative approach, sequencing 48 pooled population samples from 32 locations, and perform the first continent-wide genomic analysis of genetic variation in European Drosophila melanogaster. Our analyses uncover longitudinal population structure, provide evidence for continent-wide selective sweeps, identify candidate genes for local climate adaptation, and document clines in chromosomal inversion and transposable element frequencies. We also characterize variation among populations in the composition of the fly microbiome, and identify five new DNA viruses in our samples.Publisher PDFPeer reviewe

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

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. 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 look for evidence of accelerated divergence between D. montana and D. virilis, a previously sequenced relative, and 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. We also re-sequenced three populations of D. montana from 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

As the crow, flies : identifying genomic loci contributing to adaptation in Drosophila and the corvid radiation

Identifying loci that contribute to adaptive traits is an important goal of evolutionary biology. I take a comparative genomic approach to identify loci that have responded to divergent selection. First I consider the challenges of identifying consistent genomic responses to selection during experimental evolution. I use population genetic simulations to show that commonly applied statistical tests perform poorly and identify superior methods. These will also be useful in comparing allele frequencies in other contexts. Next I analyse whole genome data from an experimental evolution study of Drosophila pseudoobscura evolving under altered mating systems. I find that around 300 SNPs show consistent allele frequency differences between experimental treatments. These are clustered in genomic regions which also show signatures of selective sweeps or background selection. These regions contain genes with mutant phenotypes related to changes already documented in this system. In another chapter I use a novel approach to identify markers potentially influencing female re-mating rate among lines of D. pseudoobscura. I use simulations to show that there are more fixed differences between extreme pairs of isofemale lines from different populations than expected by chance. Many of the genes are implicated in female mating behaviour in other studies. I then focus on local adaptation in wild Drosophila montana populations. I use Bayesian methods to relate genetic and environmental differentiation among populations. Finally, I take a broader comparative approach using multiple genomes from 14 species of crow to identify potential signatures of selection in the New Caledonian (NC) (Corvus moneduloides) and Hawai’ian crow (Corvus hawaiiensis) lineages. The NC and, more recently, Hawai’ian crows are of great interest for their unusual tool-using foraging behaviour. I find only modest evidence for greater rates of molecular evolution at coding regions within these lineages. This thesis applies novel techniques to genomic data to identify candidate loci for evolutionary divergence in these different systems and highlight analytical methods that will be generally useful in other systems