Publications by authors named "Michael G Ritchie"

81 Publications

The Pleistocene species pump past its prime: evidence from European butterfly sister species.

Mol Ecol 2021 May 15. Epub 2021 May 15.

Institute of Evolutionary Biology, University of Edinburgh, Edinburgh, EH9 3FL, UK.

The Pleistocene glacial cycles had a profound impact on the ranges and genetic make-up of organisms. Whilst it is clear that the contact zones that have been described for many sister taxa are secondary and have formed during the last interglacial, it is unclear when the taxa involved began to diverge. Previous estimates based on small numbers of loci are unreliable given the stochasticity of genetic drift and the contrasting effects of incomplete lineage sorting and gene flow on gene divergence. Here we use genome-wide transcriptome data to estimate divergence for 18 sister species pairs of European butterflies showing either sympatric or contact zone distributions. We find that in most cases species divergence predates the mid-Pleistocene transition or even the entire Pleistocene period. We also show that although post divergence gene flow is restricted to contact zone pairs, they are not systematically younger than sympatric pairs. This suggests that contact zones are not limited to the initial stages of the speciation process, but can involve notably old taxa. Finally, we show that mitochondrial and nuclear divergence are only weakly correlated and mitochondrial divergence is higher for contact-zone pairs.
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http://dx.doi.org/10.1111/mec.15981DOI Listing
May 2021

Sex-specific responses to cold in a very cold-tolerant, northern Drosophila species.

Heredity (Edinb) 2021 Apr 28;126(4):695-705. Epub 2021 Jan 28.

Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland.

Organisms can plastically alter resource allocation in response to changing environmental factors. For example, in harsh conditions, organisms are expected to shift investment from reproduction toward survival; however, the factors and mechanisms that govern the magnitude of such shifts are relatively poorly studied. Here we compared the impact of cold on males and females of the highly cold-tolerant species Drosophila montana at the phenotypic and transcriptomic levels. Although both sexes showed similar changes in cold tolerance and gene expression in response to cold treatment, indicating that the majority of changes are concordant between the sexes, we identified a clear reduction in sexually dimorphic gene expression, suggesting that preparing for the colder season involves reducing investment in sex-specific traits. This reduction was larger in males than females, as expected if male sexual traits are more condition-dependent than female traits, as predicted by theory. Gene expression changes were primarily associated with shifts in metabolic profile, which likely play a role in increasing cold tolerance. Finally, we found that the expression of immune genes was reduced following cold treatment, suggesting that reduced investment in costly immune function may be important in helping flies survive colder periods.
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http://dx.doi.org/10.1038/s41437-020-00398-2DOI Listing
April 2021

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

Mol Ecol 2021 02 23;30(4):973-986. Epub 2020 Dec 23.

Department of Anatomy, University of Otago, Dunedin, New Zealand.

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.
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http://dx.doi.org/10.1111/mec.15775DOI Listing
February 2021

Within-population sperm competition intensity does not predict asymmetry in conpopulation sperm precedence.

Philos Trans R Soc Lond B Biol Sci 2020 12 19;375(1813):20200071. Epub 2020 Oct 19.

Department of Zoology, Stockholm University, Stockholm 106-91, Sweden.

Postcopulatory sexual selection can generate evolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilization success diverge between populations, postmating prezygotic (PMPZ) barriers to gene flow may evolve. Conspecific sperm precedence is a form of PMPZ isolation thought to evolve early during speciation yet has mostly been studied between species. Here we show conpopulation sperm precedence (CpSP) between populations. Using Pool-seq genomic data we estimate divergence times and ask whether PMPZ isolation evolved in the face of gene flow. We find models incorporating gene flow fit the data best indicating populations experienced considerable gene flow during divergence. We find CpSP is asymmetric and mirrors asymmetry in non-competitive PMPZ isolation, suggesting these phenomena have a shared mechanism. However, we show asymmetry is unrelated to the strength of postcopulatory sexual selection acting within populations. We tested whether overlapping foreign and coevolved ejaculates within the female reproductive tract altered fertilization success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of PMPZ isolation. We suggest that instead cryptic female choice or mutation-order divergence may drive divergence of postcopulatory phenotypes resulting in PMPZ isolation. This article is part of the theme issue 'Fifty years of sperm competition'.
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http://dx.doi.org/10.1098/rstb.2020.0071DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7661444PMC
December 2020

Dinner and a show: The role of male copulatory courtship song and female blood-feeding in the reproductive success of Lutzomyia longipalpis from Lapinha, Brazil.

Infect Genet Evol 2020 11 5;85:104470. Epub 2020 Aug 5.

Centre for Biological Diversity, School of Biology, University of St Andrews, Fife KY169TH, UK.

Lutzomyia longipalpis is the main vector of visceral Leishmaniasis in the Americas and is composed of a species complex. Males of this sand-fly produce acoustic signals during copulation and different patterns are observed among Brazilian populations. Such acoustic signals are commonly involved in species recognition. However, since the song is only produced during copulation it is not clear how it affects mating success or contributes to sexual isolation. Another aspect that may affect reproductive success is the presence of food. Since hematophagy is such an important aspect of L. longipalpis biology, we wanted to test if blood-feeding can influence the reproductive behaviour of this insect. We performed crossing experiments removing males' wings (silencing them) and playing back either the homo-specific or the hetero-specific song to either unfed or blood-fed females. Our results showed that both songs and blood-feeding affect insemination success, but not the frequency of copulation. In trials where females were not blood-fed song clearly affected insemination; males with wings, and males with homo-specific song playback had a higher insemination success than wingless males (no song) and trials with hetero-specific song. Blood-feeding females prior to the trials increased insemination in all groups including the control group which suggests that mating happens simultaneously with, or immediately after, the blood meal. Blood-fed females also seemed to discriminate less against the wrong song or the lack of song (wingless) one day after feeding, however trials with the correct song still had higher insemination rates. Altogether, our results show that both the male copulatory courtship songs and female blood-feeding are important for reproductive success and as such are important components of the sexual behaviour of L. longipalpis.
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http://dx.doi.org/10.1016/j.meegid.2020.104470DOI Listing
November 2020

Genomic Analysis of European Drosophila melanogaster Populations Reveals Longitudinal Structure, Continent-Wide Selection, and Previously Unknown DNA Viruses.

Mol Biol Evol 2020 09;37(9):2661-2678

The European Drosophila Population Genomics Consortium (DrosEU).

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.
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http://dx.doi.org/10.1093/molbev/msaa120DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7475034PMC
September 2020

Sexual selection and population divergence III: Interspecific and intraspecific variation in mating signals.

J Evol Biol 2020 07 27;33(7):990-1005. Epub 2020 Apr 27.

Centre for Biological Diversity, School of Biology, University of St Andrews, Fife, UK.

A major challenge for studying the role of sexual selection in divergence and speciation is understanding the relative influence of different sexually selected signals on those processes in both intra- and interspecific contexts. Different signals may be more or less susceptible to co-option for species identification depending on the balance of sexual and ecological selection acting upon them. To examine this, we tested three predictions to explain geographic variation in long- versus short-range sexual signals across a 3,500 + km transect of two related Australian field cricket species (Teleogryllus spp.): (a) selection for species recognition, (b) environmental adaptation and (c) stochastic divergence. We measured male calling song and male and female cuticular hydrocarbons (CHCs) in offspring derived from wild populations, reared under common garden conditions. Song clearly differentiated the species, and no hybrids were observed suggesting that hybridization is rare or absent. Spatial variation in song was not predicted by geography, genetics or climatic factors in either species. In contrast, CHC divergence was strongly associated with an environmental gradient supporting the idea that the climatic environment selects more directly upon these chemical signals. In light of recently advocated models of diversification via ecological selection on secondary sexual traits, the different environmental associations we found for song and CHCs suggest that the impact of ecological selection on population divergence, and how that influences speciation, might be different for acoustic versus chemical signals.
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http://dx.doi.org/10.1111/jeb.13631DOI Listing
July 2020

Field cricket genome reveals the footprint of recent, abrupt adaptation in the wild.

Evol Lett 2020 Feb 19;4(1):19-33. Epub 2019 Dec 19.

School of Biology University of St Andrews St Andrews Fife KY16 9TH United Kingdom.

Evolutionary adaptation is generally thought to occur through incremental mutational steps, but large mutational leaps can occur during its early stages. These are challenging to study in nature due to the difficulty of observing new genetic variants as they arise and spread, but characterizing their genomic dynamics is important for understanding factors favoring rapid adaptation. Here, we report genomic consequences of recent, adaptive song loss in a Hawaiian population of field crickets (). A discrete genetic variant, , appeared and spread approximately 15 years ago. erases sound-producing veins on male wings. These silent flatwing males are protected from a lethal, eavesdropping parasitoid fly. We sequenced, assembled and annotated the cricket genome, produced a linkage map, and identified a quantitative trait locus covering a large region of the X chromosome. Gene expression profiling showed that is associated with extensive genome-wide effects on embryonic gene expression. We found that flatwing male crickets express feminized chemical pheromones. This male feminizing effect, on a different sexual signaling modality, is genetically associated with the genotype. Our findings suggest that the early stages of evolutionary adaptation to extreme pressures can be accompanied by greater genomic and phenotypic disruption than previously appreciated, and highlight how abrupt adaptation might involve suites of traits that arise through pleiotropy or genomic hitchhiking.
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http://dx.doi.org/10.1002/evl3.148DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7006468PMC
February 2020

Purifying Selection in Corvids Is Less Efficient on Islands.

Mol Biol Evol 2020 02;37(2):469-474

Department of Evolutionary Biology, Uppsala University, Uppsala, Sweden.

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.
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http://dx.doi.org/10.1093/molbev/msz233DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6993847PMC
February 2020

Selection for reproduction under short photoperiods changes diapause-associated traits and induces widespread genomic divergence.

J Exp Biol 2019 10 17;222(Pt 20). Epub 2019 Oct 17.

Department of Biological and Environmental Science, University of Jyväskylä, 40014 Jyväskylä, Finland.

The incidence of reproductive diapause is a critical aspect of life history in overwintering insects from temperate regions. Much has been learned about the timing, physiology and genetics of diapause in a range of insects, but how the multiple changes involved in this and other photoperiodically regulated traits are inter-related is not well understood. We performed quasinatural selection on reproduction under short photoperiods in a northern fly species, , to trace the effects of photoperiodic selection on traits regulated by the photoperiodic timer and/or by a circadian clock system. Selection changed several traits associated with reproductive diapause, including the critical day length for diapause (CDL), the frequency of diapausing females under photoperiods that deviate from daily 24 h cycles and cold tolerance, towards the phenotypes typical of lower latitudes. However, selection had no effect on the period of free-running locomotor activity rhythm regulated by the circadian clock in fly brain. At a genomic level, selection induced extensive divergence from the control line in 16 gene clusters involved in signal transduction, membrane properties, immunologlobulins and development. These changes resembled those detected between latitudinally divergent populations in the wild and involved SNP divergence associated with several genes linked with diapause induction. Overall, our study shows that photoperiodic selection for reproduction under short photoperiods affects diapause-associated traits without disrupting the central clock network generating circadian rhythms in fly locomotor activity.
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http://dx.doi.org/10.1242/jeb.205831DOI Listing
October 2019

Evolution and diversity of the courtship repertoire in the Drosophila montium species group (Diptera: Drosophilidae).

J Evol Biol 2019 10 22;32(10):1124-1140. Epub 2019 Aug 22.

Department of Entomology, College of Agriculture, South China Agricultural University, Guangzhou, China.

Changes in elements of courtship behaviour can influence sexual isolation between species. Large-scale analyses of changes, including loss and gain of courtship elements, across a relatively complete phylogenetic group are rare but needed to understand the significance of such changes, for example whether the gain and loss of courtship elements are essentially arbitrary or equally reversible. In most species of Drosophila, courtship, including singing, mainly occurs before mounting as premounting courtship. The Drosophila montium species group is unusual because loss of premounting courtship and gain of post-mounting one has been detected in this group. Here, we provide an extensive analysis on the courtship repertoire and songs of 42 species in this group. Synchronously captured video and audio recordings were analysed to describe courtship patterns and male courtship songs, and changes were analysed in a phylogenetic context. Ancestral state reconstruction suggests that a gain of post-mounting courtship singing at the ancestor of this species group has been accompanied by a concurrent decrease in the incidence of premounting courtship singing and has led to subsequent further decrease and eventually complete loss of premounting courtship song in several lineages. Alongside this evolutionary trend towards post-mounting courtship, sine song and a special type of "high pulse repetition song" have become more widely used for courtship during species diversification in the montium group. It is likely that the elaboration of post-mounting courtship behaviours is associated with changes in the relative importance of pre- and post-mounting components of mating systems, such as sperm competition or cryptic female choice.
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http://dx.doi.org/10.1111/jeb.13515DOI Listing
October 2019

Social effects on fruit fly courtship song.

Ecol Evol 2019 Jan 10;9(1):410-416. Epub 2018 Dec 10.

School of Biology, Centre for Biological Diversity University of St Andrews St Andrews UK.

Courtship behavior in has often been described as a classic innate behavioral repertoire, but more recently extensive plasticity has been described. In particular, prior exposure to acoustic signals of con- or heterspecific males can change courtship traits in both sexes that are liable to be important in reproductive isolation. However, it is unknown whether male courtship song itself is socially plastic. We examined courtship song plasticity of two species in the subgroup. Sexual isolation between the species is influenced by two male song traits, the interpulse interval (IPI) and sinesong frequency (SSF). Neither of these showed plasticity when males had prior experience of con- and heterospecific social partners. However, males of both species produced longer bursts of song during courtship when they were exposed to social partners (either con- or heterospecific) than when they were reared in isolation. carrying mutations affecting short- or medium-term memory showed a similar response to the social environment, not supporting a role for learning. Our results demonstrate that the amount of song a male produces during courtship is plastic depending on the social environment, which might reflect the advantage of being able to respond to variation in intrasexual competition, but that song structure itself is relatively inflexible, perhaps due to strong selection against hybridization.
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http://dx.doi.org/10.1002/ece3.4759DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6342107PMC
January 2019

Behavioural mechanisms of sexual isolation involving multiple modalities and their inheritance.

J Evol Biol 2019 03 21;32(3):243-258. Epub 2018 Dec 21.

Centre for Biological Diversity, School of Biology, University of St Andrews, Fife, UK.

Speciation research dissects the genetics and evolution of reproductive barriers between parental species. Hybrids are the "gatekeepers" of gene flow, so it is also important to understand the behavioural mechanisms and genetics of any potential isolation from their parental species. We tested the role of multiple behavioural barriers in reproductive isolation among closely related field crickets and their hybrids (Teleogryllus oceanicus and Teleogryllus commodus). These species hybridize in the laboratory, but the behaviour of hybrids is unusual and there is little evidence for gene flow in the wild. We found that heterospecific pairs exhibited reduced rates of courtship behaviour due to discrimination by both sexes, and that this behavioural isolation was symmetrical. However, hybrids were not sexually selected against and exhibited high rates of courtship behaviour even though hybrid females are sterile. Using reciprocal hybrid crosses, we characterized patterns of interspecific divergence and inheritance in key sexual traits that might underlie the mating patterns we found: calling song, courtship song and cuticular hydrocarbons (CHCs). Song traits exhibited both sex linkage and transgressive segregation, whereas CHCs exhibited only the latter. Calculations of the strength of isolation exerted by these sexual traits suggest that close-range signals are as important as long-distance signals in contributing to interspecific sexual isolation. The surprisingly weak mating barriers observed between hybrids and parental species highlight the need to examine reproductive isolating mechanisms and their genetic bases across different potential stages of introgressive hybridization.
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http://dx.doi.org/10.1111/jeb.13408DOI Listing
March 2019

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

Genome Biol Evol 2018 08 1;10(8):2086-2101. Epub 2018 Aug 1.

Center for Biological Diversity, School of Biology, University of St. Andrews, Fife, United Kingdom.

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.
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http://dx.doi.org/10.1093/gbe/evy147DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC6107330PMC
August 2018

Opposing patterns of intraspecific and interspecific differentiation in sex chromosomes and autosomes.

Mol Ecol 2018 10 10;27(19):3905-3924. Epub 2018 Jun 10.

Centre for Biological Diversity, School of Biology, University of St Andrews, St Andrews, UK.

Linking intraspecific and interspecific divergence is an important challenge in speciation research. X chromosomes are expected to evolve faster than autosomes and disproportionately contribute to reproductive barriers, and comparing genetic variation on X and autosomal markers within and between species can elucidate evolutionary processes that shape genome variation. We performed RADseq on a 16 population transect of two closely related Australian cricket species, Teleogryllus commodus and T. oceanicus, covering allopatry and sympatry. This classic study system for sexual selection provides a rare exception to Haldane's rule, as hybrid females are sterile. We found no evidence of recent introgression, despite the fact that the species coexist in overlapping habitats in the wild and interbreed in the laboratory. Putative X-linked loci showed greater differentiation between species compared with autosomal loci. However, population differentiation within species was unexpectedly lower on X-linked markers than autosomal markers, and relative X-to-autosomal genetic diversity was inflated above neutral expectations. Populations of both species showed genomic signatures of recent population expansions, but these were not strong enough to account for the inflated X/A diversity. Instead, most of the excess polymorphism on the X could better be explained by sex-biased processes that increase the relative effective population size of the X, such as interspecific variation in the strength of sexual selection among males. Taken together, the opposing patterns of diversity and differentiation at X versus autosomal loci implicate a greater role for sex-linked genes in maintaining species boundaries in this system.
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http://dx.doi.org/10.1111/mec.14725DOI Listing
October 2018

Sexual selection predicts species richness across the animal kingdom.

Proc Biol Sci 2018 05;285(1878)

Centre for Biological Diversity, School of Biology, University of St Andrews, St Andrews, UK

Our improving knowledge of the animal tree of life consistently demonstrates that some taxa diversify more rapidly than others, but what contributes to this variation remains poorly understood. An influential hypothesis proposes that selection arising from competition for mating partners plays a key role in promoting speciation. However, empirical evidence showing a link between proxies of this sexual selection and species richness is equivocal. Here, we collected standardized metrics of sexual selection for a broad range of animal taxa, and found that taxonomic families characterized by stronger sexual selection on males show relatively higher species richness. Thus, our data support the hypothesis that sexual selection elevates species richness. This could occur either by promoting speciation and/or by protecting species against extinction.
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http://dx.doi.org/10.1098/rspb.2018.0173DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5966593PMC
May 2018

Differential gene expression is not required for facultative sex allocation: a transcriptome analysis of brain tissue in the parasitoid wasp .

R Soc Open Sci 2018 Feb 21;5(2):171718. Epub 2018 Feb 21.

School of Biology, University of St Andrews, Greenside Place, St Andrews KY16 9TH, UK.

Whole-transcriptome technologies have been widely used in behavioural genetics to identify genes associated with the performance of a behaviour and provide clues to its mechanistic basis. Here, we consider the genetic basis of sex allocation behaviour in the parasitoid wasp . Female facultatively vary their offspring sex ratio in line with Hamilton's theory of local mate competition (LMC). A single female or 'foundress' laying eggs on a patch will lay just enough sons to fertilize her daughters. As the number of 'foundresses' laying eggs on a patch increases (and LMC declines), females produce increasingly male-biased sex ratios. Phenotypic studies have revealed the cues females use to estimate the level of LMC their sons will experience, but our understanding of the genetics underlying sex allocation is limited. Here, we exposed females to three foundress number conditions, i.e. three LMC conditions, and allowed them to oviposit. mRNA was extracted from only the heads of these females to target the brain tissue. The subsequent RNA-seq experiment confirmed that differential gene expression is not associated with the response to sex allocation cues and that we must instead turn to the underlying neuroscience to reveal the underpinnings of this impressive behavioural plasticity.
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http://dx.doi.org/10.1098/rsos.171718DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5830769PMC
February 2018

Increased socially mediated plasticity in gene expression accompanies rapid adaptive evolution.

Ecol Lett 2018 04 14;21(4):546-556. Epub 2018 Feb 14.

Centre for Biological Diversity, University of St Andrews, St Andrews, KY16 9TH, UK.

Recent theory predicts that increased phenotypic plasticity can facilitate adaptation as traits respond to selection. When genetic adaptation alters the social environment, socially mediated plasticity could cause co-evolutionary feedback dynamics that increase adaptive potential. We tested this by asking whether neural gene expression in a recently arisen, adaptive morph of the field cricket Teleogryllus oceanicus is more responsive to the social environment than the ancestral morph. Silent males (flatwings) rapidly spread in a Hawaiian population subject to acoustically orienting parasitoids, changing the population's acoustic environment. Experimental altering crickets' acoustic environments during rearing revealed broad, plastic changes in gene expression. However, flatwing genotypes showed increased socially mediated plasticity, whereas normal-wing genotypes exhibited negligible expression plasticity. Increased plasticity in flatwing crickets suggests a coevolutionary process coupling socially flexible gene expression with the abrupt spread of flatwing. Our results support predictions that phenotypic plasticity should rapidly evolve to be more pronounced during early phases of adaptation.
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http://dx.doi.org/10.1111/ele.12920DOI Listing
April 2018

Identifying consistent allele frequency differences in studies of stratified populations.

Methods Ecol Evol 2017 12 15;8(12):1899-1909. Epub 2017 Jun 15.

Centre for Biological Diversity Sir Harold Mitchell Building University of St Andrews St Andrews, Scotland United Kingdom.

With increasing application of pooled-sequencing approaches to population genomics robust methods are needed to accurately quantify allele frequency differences between populations. Identifying consistent differences across stratified populations can allow us to detect genomic regions under selection and that differ between populations with different histories or attributes. Current popular statistical tests are easily implemented in widely available software tools which make them simple for researchers to apply. However, there are potential problems with the way such tests are used, which means that underlying assumptions about the data are frequently violated.These problems are highlighted by simulation of simple but realistic population genetic models of neutral evolution and the performance of different tests are assessed. We present alternative tests (including Generalised Linear Models [GLMs] with quasibinomial error structure) with attractive properties for the analysis of allele frequency differences and re-analyse a published dataset.The simulations show that common statistical tests for consistent allele frequency differences perform poorly, with high false positive rates. Applying tests that do not confound heterogeneity and main effects significantly improves inference. Variation in sequencing coverage likely produces many false positives and re-scaling allele frequencies to counts out of a common value or an effective sample size reduces this effect.Many researchers are interested in identifying allele frequencies that vary consistently across replicates to identify loci underlying phenotypic responses to selection or natural variation in phenotypes. Popular methods that have been suggested for this task perform poorly in simulations. Overall, quasibinomial GLMs perform better and also have the attractive feature of allowing correction for multiple testing by standard procedures and are easily extended to other designs.
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http://dx.doi.org/10.1111/2041-210X.12810DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5726381PMC
December 2017

Mating system manipulation and the evolution of sex-biased gene expression in Drosophila.

Nat Commun 2017 12 12;8(1):2072. Epub 2017 Dec 12.

Centre for Biological Diversity, School of Biology, University of St Andrews, Fife, St Andrews, KY16 9TH, UK.

Sex differences in dioecious animals are pervasive and result from gene expression differences. Elevated sexual selection has been predicted to increase the number and expression of male-biased genes, and experimentally imposing monogamy on Drosophila melanogaster has led to a relative feminisation of the transcriptome. Here, we test this hypothesis further by subjecting another polyandrous species, D. pseudoobscura, to 150 generations of experimental monogamy or elevated polyandry. We find that sex-biased genes do change in expression but, contrary to predictions, there is usually masculinisation of the transcriptome under monogamy, although this depends on tissue and sex. We also identify and describe gene expression changes following courtship experience. Courtship often influences gene expression, including patterns in sex-biased gene expression. Our results confirm that mating system manipulation disproportionately influences sex-biased gene expression but show that the direction of change is dynamic and unpredictable.
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http://dx.doi.org/10.1038/s41467-017-02232-6DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5727229PMC
December 2017

Asymmetric paternal effect on offspring size linked to parent-of-origin expression of an insulin-like growth factor.

Ecol Evol 2017 06 15;7(12):4465-4474. Epub 2017 May 15.

Instituto de Ecología Universidad Nacional Autónoma de México México City Mexico.

Sexual reproduction brings together reproductive partners whose long-term interests often differ, raising the possibility of conflict over their reproductive investment. Males that enhance maternal investment in their offspring gain fitness benefits, even if this compromises future reproductive investment by iteroparous females. When the conflict occurs at a genomic level, it may be uncovered by crossing divergent populations, as a mismatch in the coevolved patterns of paternal manipulation and maternal resistance may generate asymmetric embryonic growth. We report such an asymmetry in reciprocal crosses between populations of the fish . We also show that a fragment of a gene which can influence embryonic growth (Insulin-Like Growth Factor 2; ) exhibits a parent-of-origin methylation pattern, where the maternally inherited allele has much more 5' cytosine methylation than the paternally inherited allele. Our findings suggest that male manipulation of maternal investment may have evolved in fish, while the parent-of-origin methylation pattern appears to be a potential candidate mechanism modulating this antagonistic coevolution process. However, disruption of other coadaptive processes cannot be ruled out, as these can lead to similar effects as conflict.
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http://dx.doi.org/10.1002/ece3.3025DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5478053PMC
June 2017

Inducing Cold-Sensitivity in the Frigophilic Fly Drosophila montana by RNAi.

PLoS One 2016 10;11(11):e0165724. Epub 2016 Nov 10.

Centre for Biological Diversity, School of Biology, University of St Andrews, Fife, United Kingdom.

Cold acclimation is a critical physiological adaptation for coping with seasonal cold. By increasing their cold tolerance individuals can remain active for longer at the onset of winter and can recover more quickly from a cold shock. In insects, despite many physiological studies, little is known about the genetic basis of cold acclimation. Recently, transcriptomic analyses in Drosophila virilis and D. montana revealed candidate genes for cold acclimation by identifying genes upregulated during exposure to cold. Here, we test the role of myo-inositol-1-phosphate synthase (Inos), in cold tolerance in D. montana using an RNAi approach. D. montana has a circumpolar distribution and overwinters as an adult in northern latitudes with extreme cold. We assessed cold tolerance of dsRNA knock-down flies using two metrics: chill-coma recovery time (CCRT) and mortality rate after cold acclimation. Injection of dsRNAInos did not alter CCRT, either overall or in interaction with the cold treatment, however it did induced cold-specific mortality, with high levels of mortality observed in injected flies acclimated at 5°C but not at 19°C. Overall, injection with dsRNAInos induced a temperature-sensitive mortality rate of over 60% in this normally cold-tolerant species. qPCR analysis confirmed that dsRNA injection successfully reduced gene expression of Inos. Thus, our results demonstrate the involvement of Inos in increasing cold tolerance in D. montana. The potential mechanisms involved by which Inos increases cold tolerance are also discussed.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0165724PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5104470PMC
June 2017

Transparency and reproducibility in evolutionary research.

J Evol Biol 2016 07;29(7):1296-7

Journal of Evolutionary Biology.

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http://dx.doi.org/10.1111/jeb.12894DOI Listing
July 2016

Quantitative Trait Locus Analysis of Mating Behavior and Male Sex Pheromones in Nasonia Wasps.

G3 (Bethesda) 2016 06 1;6(6):1549-62. Epub 2016 Jun 1.

Evolutionary Genetics, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen 9700CC, The Netherlands

A major focus in speciation genetics is to identify the chromosomal regions and genes that reduce hybridization and gene flow. We investigated the genetic architecture of mating behavior in the parasitoid wasp species pair Nasonia giraulti and Nasonia oneida that exhibit strong prezygotic isolation. Behavioral analysis showed that N. oneida females had consistently higher latency times, and broke off the mating sequence more often in the mounting stage when confronted with N. giraulti males compared with males of their own species. N. oneida males produce a lower quantity of the long-range male sex pheromone (4R,5S)-5-hydroxy-4-decanolide (RS-HDL). Crosses between the two species yielded hybrid males with various pheromone quantities, and these males were used in mating trials with females of either species to measure female mate discrimination rates. A quantitative trait locus (QTL) analysis involving 475 recombinant hybrid males (F2), 2148 reciprocally backcrossed females (F3), and a linkage map of 52 equally spaced neutral single nucleotide polymorphism (SNP) markers plus SNPs in 40 candidate mating behavior genes revealed four QTL for male pheromone amount, depending on partner species. Our results demonstrate that the RS-HDL pheromone plays a role in the mating system of N. giraulti and N. oneida, but also that additional communication cues are involved in mate choice. No QTL were found for female mate discrimination, which points at a polygenic architecture of female choice with strong environmental influences.
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http://dx.doi.org/10.1534/g3.116.029074DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4889652PMC
June 2016

Postmating-prezygotic isolation between two allopatric populations of Drosophila montana: fertilisation success differs under sperm competition.

Ecol Evol 2016 Mar 16;6(6):1679-91. Epub 2016 Feb 16.

Department of Ecology and Evolution University of Lausanne Biophore Building Lausanne 1015 Switzerland.

Postmating but prezygotic (PMPZ) interactions are increasingly recognized as a potentially important early-stage barrier in the evolution of reproductive isolation. A recent study described a potential example between populations of the same species: single matings between Drosophila montana populations resulted in differential fertilisation success because of the inability of sperm from one population (Vancouver) to penetrate the eggs of the other population (Colorado). As the natural mating system of D. montana is polyandrous (females remate rapidly), we set up double matings of all possible crosses between the same populations to test whether competitive effects between ejaculates influence this PMPZ isolation. We measured premating isolation in no-choice tests, female fecundity, fertility and egg-to-adult viability after single and double matings as well as second-male paternity success (P2). Surprisingly, we found no PMPZ reproductive isolation between the two populations under a competitive setting, indicating no difficulty of sperm from Vancouver males to fertilize Colorado eggs after double matings. While there were subtle differences in how P2 changed over time, suggesting that Vancouver males' sperm are somewhat less competitive in a first-male role within Colorado females, these effects did not translate into differences in overall P2. Fertilisation success can thus differ dramatically between competitive and noncompetitive conditions, perhaps because the males that mate second produce higher quality ejaculates in response to sperm competition. We suggest that unlike in more divergent species comparisons, where sperm competition typically increases reproductive isolation, ejaculate tailoring can reduce the potential for PMPZ isolation when recently diverged populations interbreed.
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http://dx.doi.org/10.1002/ece3.1995DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4801965PMC
March 2016

Preparing for Winter: The Transcriptomic Response Associated with Different Day Lengths in Drosophila montana.

G3 (Bethesda) 2016 05 3;6(5):1373-81. Epub 2016 May 3.

Department of Biological and Environmental Science, University of Jyväskylä, FI-40014, Finland.

At northern latitudes, the most robust cue for assessing the onset of winter is the shortening of day lengths. Many species use day length as a cue to increase their cold tolerance and/or enter into diapause, but little is known about changes in gene expression that occur under different day lengths. We investigate the gene expression changes associated with differences in light/dark cycles in Drosophila montana, a northerly distributed species with a strong adult photoperiodic reproductive diapause. To examine gene expression changes induced by light both prior to and during diapause, we used both nondiapausing and diapausing flies. We found that the majority of genes that are differentially expressed between different day lengths in nondiapausing and diapausing flies differ. However, the biological processes involved were broadly similar. These included neuron development and metabolism, which are largely consistent with an increase in cold tolerance previously observed to occur in these flies. We also found that many genes associated with reproduction change in expression level between different day lengths, suggesting that D. montana use changes in day length to cue changes in reproduction both before and after entering into diapause. Finally, we also identified several interesting candidate genes for light-induced changes including Lsp2, para, and Ih.
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http://dx.doi.org/10.1534/g3.116.027870DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4856088PMC
May 2016

JEB Editorial 2016.

J Evol Biol 2016 Mar;29(3):472

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http://dx.doi.org/10.1111/jeb.12841DOI Listing
March 2016