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Rayner, J. G.

Publications and source records attributed to Rayner, J. G..

6 recordsLinked to original sources

Ecological genomics of a novel host-parasitoid arms-race in nature

Novel antagonistic interactions between species are expected to drive especially rapid coevolution. However, little is known about the genomic basis of such coevolution in nature because novel inter-specific interactions are rarely observed. Here, we study two species that recently came into first contact in Hawaii, the parasitoid fly Ormia ochracea and its cricket host Teleogryllus oceanicus. The fly locates crickets acoustically using their song, and parasitism usually results in host death. In response, protective male-silencing mutations have rapidly spread through cricket populations over the last [~]25 years, imposing novel selective pressure on flies. By integrating population genomic analyses of 358 re-sequenced flies with field surveys of selection imposed by host adaptations, we discover genomic signatures of recent selective sweeps driven by host adaptations, indicative of escalating arms-race dynamics. This evolutionary response is occurring despite severely depleted genetic variation after bottlenecks in Hawaiian fly populations. Comparative analyses suggest that the genomic substrate of modern-day, rapid counter-adaptation in O. ochracea has been under positive selection on intermediate and long-term timescales across parasitoid flies. Our findings thus support predictions of influential arms race coevolution models and illustrate the current and ancient genomic bases of counteradaptation in nature.

evolutionary biology↗

Interacting effects of sex and age on immune responses in a polygynous bat with male-biased mortality

O_LIBats have attracted considerable interest for their extraordinary longevity and ability to withstand infection by a range of pathogens without major harm. Yet, little is known about the relationship between these two characteristics, or the extent to which they vary between individuals of the same species. C_LIO_LIWe investigated sources of immune variation in wild greater spear-nosed bats, Phyllostomus hastatus, via transcriptome sequencing of blood samples before and after ex vivo exposure to lipopolysaccharide, a membrane component of gram-negative bacteria. This species exhibits an extreme harem-polygynous mating system and strongly male-biased mortality, offering the valuable opportunity to explore sources of individual variation in immunity and its relation to ageing. We assessed immune variation across both sexes, males of contrasting social status, and the full range of ages in each sex. C_LIO_LIWe observe striking immune variation associated with sex and age, with males and older bats mounting stronger inflammatory responses. These two factors interacted significantly, revealing male-biased slopes of age-related variation in immunity, the magnitude of which is consistent with male-biased ageing, supporting the predicted association between immunity and ageing. C_LIO_LIWe did not observe substantial differences in immune responses between males of harem-controlling or subordinate bachelor status. This contrasts with prior research, particularly in primates, potentially raising questions about the taxonomic generality of socially mediated immune differences, which have attracted much attention. C_LIO_LIOur findings support recent calls for a nuanced approach to understanding immune adaptations and extended longevity in bats, informed by individual and species-level differences in ecology, resource allocation, and selection. These widely overlooked factors offer valuable insights into sources of immune variation and connections to other traits, such as differences in mortality and age-related deterioration. C_LI

evolutionary biology↗

Genomic signatures of local adaptation across parasitised cricket populations

Novel species interactions provide an opportunity to assess the earliest stages of genetic adaptation in wild populations. We explored the genomic and geographic landscape of adaptation in small, fragmented Hawaiian cricket populations, which are parasitised by larvae of an introduced fly that targets singing males. Multiple protective male-silencing cricket morphs have recently spread despite songs role in mate attraction. Combining population genomics and field selection experiments, we found sharp declines in the crickets effective population size after the flys introduction. Nevertheless, geographical variation in selection influences the distribution of male-silencing alleles, consistent with local adaptation. Populations showing the strongest evidence of recovery retain large numbers of singing-capable males, suggesting that initially adaptive responses to the fly created an evolutionary trap via loss of sexual signalling.

evolutionary biology↗

Sex differences in DNA methylation in bats

Sex-biased longevity is observed across a wide range of animal taxa, including bats, for reasons not well understood. Patterns of cytosine methylation vary predictably with age in many organisms, offering a valuable means to investigate differences in patterns of aging at the molecular level. We tested sex differences in cytosine methylation across 14 bat species and compared patterns of age-associated variation. Sex differences were overrepresented on the X chromosome, showing a strong pattern of female hypermethylation within promoter regions. Sex and age-associated differences in methylation were non-randomly distributed with respect to proximity to putative sex hormone receptor binding sites, with sites hypermethylated in males and females tending to be underrepresented near androgen and estrogen receptor binding sites, respectively. Across species, we observed the relative steepness of male versus female slopes of age-associated variation was associated with the strength of precopulatory sexual selection, with especially strong trends towards male-biased age-associated slopes in two harem-polygynous species that exhibit female-biased longevity. Our results offer insights into how patterns of methylation differ across sexes and ages, and raise intriguing questions for future research, such as whether sex differences in molecular aging reflect sex-biased longevity, for which records in bats are sparse.

evolutionary biology↗

Competing adaptations maintain non-adaptive variation in a wild cricket population

How emerging adaptive variants interact is an important factor in the evolution of wild populations. However, the opportunity to empirically study this interaction is rare. We recently documented the emergence of an adaptive phenotype curly-wing in Hawaiian populations of field crickets (Teleogryllus oceanicus). Curly-wing inhibits males ability to sing, protecting them from eavesdropping parasitoid flies (Ormia ochracea). Surprisingly, curly-wing co-occurs with similarly protective silent flatwing phenotypes in multiple populations, in which neither phenotype has spread to fixation. These two phenotypes are frequently co-expressed, but since either phenotype sufficiently reduces song amplitude to evade the fly, co-expression confers no additional fitness benefit. Numerous negative fitness consequences are known to accompany flatwing, and we find that curly-wing, too, incurs fitness costs via reduced male courtship success and reduced female longevity. We show through crosses, genomic and mRNA sequencing that curly-wing expression is associated with variation on a single autosome. In parallel analyses of flatwing, our results reinforce previous findings of X-linked single-locus inheritance, with the phenotype likely arising through down-regulation of doublesex. By combining insights about the genetic architecture of these alternative phenotypes with simulations and field observations, we show that the co-occurrence of these two adaptations impedes either from fixing, despite extreme fitness benefits. Interestingly, both flatwing and curly-wing are statistically associated with nearby inversions, which are also retained as polymorphisms. This co-occurrence of similar adaptive forms in the same populations might be more common than generally considered, and could be an important force inhibiting adaptive evolution in wild populations.

evolutionary biology↗

Silent crickets reveal the genomic footprint of recent adaptive trait loss

Secondary trait loss is widespread and has profound consequences, from generating diversity to driving adaptation. Sexual trait loss is particularly common1. Its genomic impact is challenging to reconstruct because most reversals occurred in the distant evolutionary past and must be inferred indirectly2, and questions remain about the extent of disruption caused by pleiotropy, altered gene expression and loss of homeostasis3. We tested the genomic signature of recent sexual signal loss in Hawaiian field crickets, Teleogryllus oceanicus. Song loss is controlled by a sex-linked Mendelian locus, flatwing, which feminises male wings by erasing sound-producing veins. This variant spread rapidly under pressure from an eavesdropping parasitoid fly. We sequenced, assembled and annotated the T. oceanicus genome, produced a high-density linkage map, and localised flatwing on the X chromosome. We characterised pleiotropic effects of flatwing, including changes in embryonic gene expression and alteration of another sexual signal, chemical pheromones. Song loss is associated with pleiotropy, hitchhiking and genome-wide regulatory disruption which feminises flatwing male pheromones. The footprint of recent adaptive trait loss illustrates R. A. Fishers influential prediction that variants with large mutational effect sizes can invade genomes during the earliest stages of adaptation to extreme pressures, despite having severely disruptive genomic consequences.

evolutionary biology↗