Biology subjects

Snook, R. R.

Publications and source records attributed to Snook, R. R..

9 recordsLinked to original sources

bioRxiv2026

Adaptive introgression improves heat-tolerance despite barriers to gene flow: a case study in Drosophila flavomontana and Drosophila montana

As global temperatures rise and heat waves become more frequent, populations must adapt rapidly to avoid local extinctions. Adaptive introgression allows species to quickly acquire adaptive genetic material from close relatives. However, certain genomic regions, containing barrier loci, may resist introgression. We experimentally tested whether strong heat stress selection can overcome such barriers and facilitate the transfer of adaptive alleles to improve heat tolerance. We also examined whether chromosomal inversions, which can tightly link adaptive and barrier loci through reduced recombination, promote or prevent introgression. We conducted a hybridize, evolve, and re-sequence experiment by crossing the heat-sensitive D. flavomontana with the more heat-tolerant D. montana, exposing heat-selection lines to transient heat for three generations while maintaining control lines. We also mapped long-term barriers to gene flow between natural populations using a demographically explicit genome scan. The heat-selection lines exhibited approximately twice the introgression and higher male fertility under heat stress compared to control lines and the heat-sensitive parental D. flavomontana. This introgression was primarily located in colinear autosomal regions and correlated with improved heat tolerance. Some introgression occurred also in inverted autosomal regions in the heat-selection lines but not in the control lines. The X chromosome, with three overlapping inversions, resisted introgression in both heat-selection and control lines, thereby maintaining a strong species barrier. Finally, genetic barriers in the control lines significantly overlapped with long-term barriers, but this overlap was less pronounced in the heat-selection lines. Our study demonstrates that strong selection can lead to adaptive introgression despite long-standing genetic barriers. These findings highlight that introgression can serve as a rapid source of adaptive genetic material under stressful thermal conditions, potentially mitigating climate-induced population extinctions.

evolutionary biology↗

bioRxiv2021

Female fruit flies cannot protect stored sperm from high temperature damage

Recently, it has been demonstrated that heat-induced male sterility is likely to shape population persistence as climate change progresses. However, an under-explored possibility is that females may be able to successfully store and preserve sperm at temperatures that sterilise males, which could ameliorate the impact of male infertility on populations. Here, we test whether females from two fruit fly species can protect stored sperm from a high temperature stress. We find that sperm carried by female Drosophila virilis are almost completely sterilised by high temperatures, whereas sperm carried by female Zaprionus indianus show only slightly reduced fertility. Heat-shocked D. virilis females can recover fertility when allowed to remate, suggesting that the delivered heat-shock is destroying stored sperm and not directly damaging females in this species. The temperatures required to reduce fertility of mated females are substantially lower than the temperatures required to destroy mature sperm in males, suggesting that females are worse than males at protecting mature sperm. This suggests that female sperm storage is unlikely to ameliorate the impacts of high temperature fertility losses in males, and instead exacerbates fertility costs of high temperatures, representing an important determinant of population persistence during climate change.

physiology↗

bioRxiv2021

Sexual selection affects the evolution of physiological and life history traits

Sexual selection and sexual conflict are expected to affect all aspects of the phenotype, not only traits that are directly involved in reproduction. Here, we show coordinated evolution of multiple physiological and life history traits in response to long-term experimental manipulation of the mating system in populations of Drosophila pseudoobscura. Development time was extended under polyandry relative to monogamy in both sexes, potentially due to higher investment in traits linked to sexual selection and sexual conflict. Individuals (especially males) evolving under polyandry had higher metabolic rates and locomotor activity than those evolving under monogamy. Polyandry individuals also invested more in metabolites associated with increased endurance capacity and efficient energy metabolism and regulation, namely lipid and glycogen. Finally, polyandry males were less desiccation- and starvation-resistant than monogamy males, suggesting trade-offs between resistance and sexually selected traits. Our results provide experimental evidence that mating systems can impose selection that influences the evolution of non-sexual phenotypes such as development, activity, metabolism, and nutrient homeostasis.

evolutionary biology↗

bioRxiv2021

Experimental sexual selection reveals rapid divergence in male and female reproductive transcriptomes and their interactions

Postcopulatory interactions between the sexes in internally fertilizing species elicits both sexual conflict and sexual selection. Macroevolutionary and comparative studies have linked these processes to rapid transcriptomic evolution in sex-specific tissues and substantial transcriptomic postmating responses in females, patterns of which are altered when mating between reproductively isolated species. Here we test multiple predictions arising from sexual selection and conflict theory about the evolution of sex-specific and tissue-specific gene expression and the postmating response at the microevolutionary level. Following over 150 generations of experimental evolution under either reduced (enforced monogamy) or elevated (polyandry) sexual selection in Drosophila pseudoobscura, we found a substantial effect of sexual selection treatment on transcriptomic divergence in virgin male and female reproductive tissues (testes, male accessory glands, the female reproductive tract and ovaries). Sexual selection treatment also had a dominant effect on the postmating response, particularly in the female reproductive tract - the main arena for sexual conflict - compared to ovaries. This affect was asymmetric with monandry females typically showing more postmating responses than polyandry females, with enriched gene functions varying across treatments. The evolutionary history of the male partner had a larger effect on the postmating response of monandry females, but females from both sexual selection treatments showed unique patterns of gene expression and gene function when mating with males from the alternate treatment. Our microevolutionary results mostly confirm comparative macroevolutionary predictions on the role of sexual selection on transcriptomic divergence and altered gene regulation arising from divergent coevolutionary trajectories between sexual selection treatments.

evolutionary biology↗

bioRxiv2020

Experimental evolution confirms signatures of sexual selection in genomic divergence.

Comparative genomics has contributed to the growing evidence that sexual selection is an important component of evolutionary divergence and speciation. Divergence by sexual selection is implicated in faster rates of divergence of the X chromosome and of genes thought to underlie sexually selected traits, including genes that are sex-biased in expression. However, accurately inferring the relative importance of complex and interacting forms of natural selection, demography and neutral processes which occurred in the evolutionary past is challenging. Experimental evolution provides an opportunity to apply controlled treatments for multiple generations and examine the consequent genomic divergence. Here we altered sexual selection intensity, elevating sexual selection in polyandrous lines and eliminating it in monogamous lines, and examined patterns of divergence in the genome of Drosophila pseudoobscura after more than 160 generations of experimental evolution. Divergence is not uniform across the genome but concentrated in "islands", many of which contain candidate genes implicated in mating behaviours and other sexually selected phenotypes. These are more often seen on the X chromosome, which shows divergence greater than neutral expectations. There are characteristic signatures of selection seen in these regions, with lower diversity and greater FST on the X chromosome than the autosomes, and differences in diversity on the autosomes between selection regimes. Reduced Tajimas D implies that selective sweeps have occurred within some of the divergent regions, despite considerable recombination. These changes are associated with both differential gene expression between the lines and sex-biased gene expression within the lines. Our results are very similar to those thought to implicate sexual selection in divergence in natural populations, and hence provide experimental support for the likely role of sexual selection in driving such types of genetic divergence, but also illustrate how variable outcomes can be for different genomic regions. Impact SummaryHow does sexual selection contribute to the divergence of genomes? It is often thought that sexual selection is a potent force in evolutionary divergence, but finding signatures of sexual selection in the genome is not straight-forward, and has been quite controversial recently. Here we used experimental evolution to allow replicate populations of fruit fly to evolve under relaxed or strengthened sexual selection for over 160 generations, then sequenced their genomes to see how they had diverged. The features we find are very similar to those reported in populations of natural species thought to be under strong sexual selection. We found that genomic divergence was concentrated in small patches of the genome rather than widespread. These are more often seen on the X chromosome, which overall shows especially elevated divergence. There are also characteristic signatures of selection seen in these regions, with lower genetic diversity suggesting that selection was strong in these regions. The changes are associated with both differential gene expression between the lines and sex-biased gene expression within the lines. Many of the patches of divergence also contain candidate genes implicated in mating behaviours and other sexually selected phenotypes. Our results provide experimental support for the likely role of sexual selection in driving such types of genetic divergence.

evolutionary biology↗

bioRxiv2020

Seminal fluid protein divergence among populations exhibiting postmating prezygotic reproductive isolation

Despite holding a central role for fertilisation success, reproductive traits often show elevated rates of evolution and diversification. The rapid evolution of seminal fluid proteins (Sfps) within populations is predicted to cause mis-signalling between the male ejaculate and female reproductive tract between populations resulting in postmating prezygotic (PMPZ) isolation. Crosses between populations of Drosophila montana show PMPZ isolation in the form of reduced fertilisation success in both noncompetitive and competitive contexts. Here we test whether male ejaculate proteins deriving from either the accessory glands or the ejaculatory bulb differ between populations using liquid chromatography tandem mass spectrometry. We find more than 150 differentially abundant proteins between populations which may contribute to PMPZ isolation. These proteins include a number of proteases and peptidases, and several orthologs of D. melanogaster Sfps, all known to mediate fertilisation success and which mimic PMPZ isolation phenotypes. Males of one population typically produced greater quantities of Sfps and the strongest PMPZ isolation occurs in this direction. The accessory glands and ejaculatory bulb have different functions and the ejaculatory bulb contributes more to population differences than the accessory glands. Proteins with a secretory signal, but not Sfps, evolve faster than non-secretory proteins although the conservative criteria used to define Sfps may have impaired the ability to identify rapidly evolving proteins. We take advantage of quantitative proteomics data from three Drosophila species to determine shared and unique functional enrichments of Sfps that could be subject to selection between taxa and subsequently mediate PMPZ isolation. Our study provides the first high throughput quantitative proteomic evidence showing divergence of reproductive proteins implicated in the emergence of PMPZ isolation between populations. IMPACT SUMMARYIdentifying traits that prevent successful interbreeding is key to understanding early stages of the formation of new species, or speciation. Reproductive isolation arising prior to and during fertilisation frequently involves differences in how the sexes interact. In internally fertilising taxa, such interactions are mediated between the female reproductive tract where fertilisation occurs and the receipt of the ejaculate necessary for fertilisation. Because ejaculate proteins are at least partially responsible for these interactions, differences in male ejaculate protein composition could negatively impact fertilisation success, generating reproductive isolation. While the biological classes of ejaculate proteins are shared across all animal taxa, proteins that are secreted by males tend to show rapid evolution in gene expression and genetic sequence. Thus, reproductive proteins are suggested as prime targets facilitating reproductive isolation that arises after mating but before fertilisation (PostMating PreZygotic or PMPZ isolation). Most research on PMPZ isolation has focussed on differences between species for which it is not possible to determine the causative and temporal order of early speciation processes. Here, we test whether populations that exhibit few genetic differences but show strong PMPZ isolation also exhibit variation in ejaculate composition using quantitative high throughput proteomic analyses. We find a number of proteins are differentially abundant between populations including several known to impact fertilisation success in other species. We show that secreted proteins are evolving at an elevated rate, implicating their potential role in PMPZ isolation. We test divergence in ejaculate composition between species, finding a core set of functions that were conserved across species which last shared a common ancestor more than 40 million years ago along with species-specific investment. This work highlights the divergent evolution of reproductive proteins which may contribute to barriers between populations within a species early during speciation, extendable to similar analyses in other taxa in the future.

evolutionary biology↗

bioRxiv2020

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

Postcopulatory sexual selection can generate coevolutionary arms races between the sexes resulting in the rapid coevolution of reproductive phenotypes. As traits affecting fertilisation success diverge between populations postmating prezygotic barriers to gene flow may evolve. Conspecific sperm precedence is a form of such isolation thought to evolve early during speciation yet has mostly been studied between species. Here we show conpopulation sperm precedence between Drosophila montana populations. Using genomic data to estimate divergence times and patterns of gene flow between populations, we show gene flow has played a considerable role during divergence. We find conpopulation sperm precedence is asymmetric and is concordant with asymmetry in non-competitive postmating prezygotic reproductive isolation. These results suggest these phenomena have a shared mechanism, but we show that this 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 fertilisation success but found no effect. Our results show that neither time since divergence nor sperm competitiveness predicts the strength of postmating prezygotic reproductive isolation. We suggest that divergence of postcopulatory phenotypes resulting in postmating prezygotic isolation is potentially driven by cryptic female choice, or mutation order divergence.

evolutionary biology↗

bioRxiv2018

Reinforcement targets sexual or postmating prezygotic reproductive barriers depending on species abundance and population history

The impact of different reproductive barriers on species or population isolation may vary in different stages of speciation depending on evolutionary forces acting within species and through species interactions. Genetic incompatibilities between interacting species are expected to reinforce prezygotic barriers in sympatric populations and create character displacement between conspecific populations living within and outside the area of sympatry. The outcome of reinforcement has been suggested to be affected by the strength of postzygotic barriers, the history of species coexistence, and the impact of species abundancies on females discrimination against heterospecific males. We tested these predictions in Drosophila montana and Drosophila flavomontana populations from different geographic regimes. All barriers between D. montana females and D. flavomontana males were extremely strong, while in the reciprocal cross postzygotic isolation was less effective and the target of reinforcement varied according to population type. In long-established sympatric populations, where D. flavomontana is abundant, reinforcement targeted sexual isolation, and in populations, where this species is a new invader and rare, reinforcement targeted postmating prezygotic barriers. Reinforcement of these barriers also created respective barriers between different D. flavomontana populations. These findings show that interspecies interactions have far-reaching effects on strengthening species barriers and promoting speciation.

evolutionary biology↗

bioRxiv2018

Sexual selection rewires reproductive protein networks

Polyandry drives postcopulatory sexual selection (PCSS), resulting in rapid evolution of male ejaculate traits. Critical to male and female fitness, the ejaculate is known to contain rapidly evolving seminal fluid proteins (SFPs) produced by specialized male secretory accessory glands. The evidence that rapid evolution of some SFPs is driven by PCSS, however, is indirect, based on either plastic responses to changes in the sexual selection environment or correlative macroevolutionary patterns. Moreover, such studies focus on SFPs that represent but a small component of the accessory gland proteome. Neither how SFPs function with other reproductive proteins, nor how PCSS influences the underlying secretory tissue adaptations and content of the accessory gland, has been addressed at the level of the proteome. Here we directly test the hypothesis that PCSS results in rapid evolution of the entire male accessory gland proteome and protein networks by taking a system-level approach, combining divergent experimental evolution of PCSS in Drosophila pseudoobscura (Dpse), high resolution mass spectrometry (MS) and proteomic discovery, bioinformatics and population genetic analyses. We demonstrate that PCSS influences the abundance of over 200 accessory gland proteins, including SFPs. A small but significant number of these proteins display molecular signatures of positive selection. Divergent PCSS also results in fundamental and remarkably compartmentalized evolution of accessory gland protein networks in which males subjected to strong PCSS invest in protein networks that serve to increase protein production whereas males subjected to relaxed PCSS alters protein networks involved in protein surveillance and quality. These results directly demonstrate that PCSS is a key evolutionary driver that shapes not only individual reproductive proteins, but rewires entire reproductive protein networks.\n\nThe abbreviations used are

evolutionary biology↗