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Mate choice in the brain: Species differ in how male traits ‘turn on’ gene expression in female brains

ABSTRACT: Mate choice plays a fundamental role in speciation, yet we know little about the molecular mechanisms that underpin this crucial decision-making process. Stickleback fish differentially adapted to limnetic and benthic habitats are reproductively isolated and females of each species use different male traits to evaluate prospective partners and reject heterospecific males. Here, we integrate behavioral data from a mate choice experiment with gene expression profiles from the brains of females actively deciding whether to mate. We find substantial gene expression variation between limnetic and benthic females, regardless of behavioral context, suggesting general divergence in constitutive gene expression patterns, corresponding to their genetic differentiation. Intriguingly, female gene co-expression modules covary with male display traits but in opposing directions for sympatric populations of the two species, suggesting male displays elicit a dynamic neurogenomic response that reflects known differences in female preferences. Furthermore, we confirm the role of numerous candidate genes previously implicated in female mate choice in other species, suggesting that evolutionary tinkering with these conserved molecular processes underlies divergent mate preferences and sexual isolation. Taken together, our study adds important new insights to our understanding of the molecular processes underlying female decision-making critical for generating sexual isolation and speciation.

ORGANISM(S): Gasterosteus aculeatus

PROVIDER: GSE263554 | GEO | 2024/05/07

REPOSITORIES: GEO

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Female Drosophila melanogaster gene expression and mate choice: candidate genes underlying sexual isolation

Project description:Background The evolution of female choice mechanisms favouring males of their own kind is considered as crucial step during the early stages of speciation. However, although the genomics of mate choice may influence both the likelihood and speed of speciation, the identity and location of genes underlying assortative mating remain largely unknown. Methods and Findings We used mate choice experiments and gene expression analysis of female D. melanogaster to examine three key components influencing speciation. We show that the 1,498 genes in Zimbabwean female Drosophila melanogaster whose expression levels differ when mating with more (Zimbabwean) versus less (Cosmopolitan strain) preferred males include many with high expression in the central nervous system and ovaries, are disproportionately X-linked and form a number of clusters with low recombination distance. Significant involvement of the brain and ovaries is consistent with the action of a combination of pre- and postcopulatory female choice mechanisms, while sex linkage and clustering of genes lead to high potential evolutionary rate and sheltering against the homogenizing effects of gene exchange between populations. Conclusion Taken together our results imply favourable genomic conditions for the evolution of reproductive isolation through mate choice in Zimbabwean D. melanogaster and suggest that mate choice may, in general, act as an even more important engine of speciation than previously realized.

2011-02-05 | GSE27076 | GEO

Kin recognition: neurogenomic response to sib mating avoidance in a parasitic wasp

Project description:Sib mating increase homozygosity and can lead to inbreeding depression. Selective pressures have favored the evolution of kin recognition and sib avoidance in mate choice. Such avoidance behavior has been recorded in the parasitoid wasp Venturia canescens where the sex determining system (single-locus complementary sex determination, sl-csd) introduces an extra short-term cost to inbreeding; females preferentially mate with unrelated males. The genetics underlying mate choice of females and kin recognition remains largely unexplored. Here we analyzed the head transcriptomic changes after exposure to distinct stimulus: courtship by unrelated male or courtship by brother, while transcriptome of females alone was used as control. Our results demonstrate that male courtship provokes a major transcriptome reprogramming in females heads. The transcriptomic response is highly dependent on the compatibility of the courting male. We subdivided the socially responsive genes using an integrative gene network analysis, we highlighted genes regulated by courtship, whatever the relatedness of the courting male. We also showed that the regulation of some peculiar group of genes is very specific of compatible male courtship, while others are regulated only by incompatible male courtship. We suggest that those different transcriptomic responses lead to mating decision or sib mating avoidance behavior observed in this species.

2018-12-20 | GSE124129 | GEO

Female Drosophila melanogaster gene expression and mate choice: candidate genes underlying sexual isolation

Project description:The evolution of female choice mechanisms favouring males of their own kind is considered as crucial step during the early stages of speciation. However, although the genomics of mate choice may influence both the likelihood and speed of speciation, the identity and location of genes underlying assortative mating remain largely unknown. We used mate choice experiments and gene expression analysis of female D. melanogaster to examine three key components influencing speciation. We show that the 1,498 genes in Zimbabwean female Drosophila melanogaster whose expression levels differ when mating with more (Zimbabwean) versus less (Cosmopolitan strain) preferred males include many with high expression in the central nervous system and ovaries, are disproportionately X-linked and form a number of clusters with low recombination distance. Significant involvement of the brain and ovaries is consistent with the action of a combination of pre- and post-copulatory female choice mechanisms, while sex linkage and clustering of genes lead to high potential evolutionary rate and sheltering against the homogenizing effects of gene exchange between populations. Taken together our results imply favourable genomic conditions for the evolution of reproductive isolation through mate choice in Zimbabwean D. melanogaster and suggest that mate choice may, in general, act as an even more important engine of speciation than previously realized. We measured gene expression of adult female Drosophila melanogaster from a composite Zimbabwe (Z) strain population named SZ, produced by mixing the genomes of six Z strain isofemale lines, shortly after mating them with either SZ strain or cosmopolitan (M strain) males. Data from four replicates of each of the two treatments (SZ mated with SZ; SZ mated with M) are presented, giving a total of eight arrays.

2011-02-05 | E-GEOD-27076 | biostudies-arrayexpress

Individual variation in preference behavior in sailfin fish refines the neurotranscriptomic pathway for mate preference

Project description:Social interactions can drive distinct gene expression profiles which may vary by social context. Here we use female sailfin molly fish (Poecilia latipinna) to identify genomic profiles associated with preference behavior in distinct social contexts: male-interactions (mate choice) versus female-interactions (shoaling partner preference). We measured behavior of 15 females interacting in a non-contact environment with either two males or two females for 30 minutes followed by whole brain transcriptomic profiling by RNA sequencing. We profiled females that exhibited high levels of social affiliation and great variation in preference behavior to identify an order of magnitude more differentially expressed genes associated with behavioral variation than by differences in social context. Using linear modeling (limma), we took advantage of the individual variation in preference behavior to identify unique gene sets that exhibited distinct correlational patterns of expression with preference behavior in each social context. By combining limma and weighted gene co-expression network analyses (WGCNA) approaches we identify a refined set of 401 genes robustly associated with mate preference that is independent of shoaling partner preference or general social affiliation. While our refined gene set confirmed neural plasticity pathways involved in moderating female preference behavior, we also identified a significant proportion of discovered that our preference-associated genes were enriched for ‘immune system’ gene ontology categories. We hypothesize that the association between mate preference and transcriptomic immune function is driven by the less well-known role of these genes in neural plasticity which is likely involved in higher-order learning and processing during mate choice decisions.

2023-07-01 | GSE233523 | GEO

Quantitative proteomics reveals rapid divergence in the postmating response of female reproductive tracts among sibling species

Project description:Fertility depends, in part, on interactions between male and female reproductive proteins inside the female reproductive tract (FRT) that mediate postmating changes in female behavior, morphology, and physiology. Coevolution between interacting proteins within species may drive reproductive incompatibilities between species, yet the mechanisms underlying postmating-prezygotic isolating barriers remain poorly resolved. Here, we used quantitative proteomics in sibling Drosophila species to investigate the molecular composition of the FRT environment and its role in mediating species-specific postmating responses. We found that (1) FRT proteomes in D. simulans and D. mauritiana virgin females express unique combinations of secreted proteins and are enriched for distinct functional categories, (2) mating induces substantial changes to the FRT proteome in D. mauritiana but not in D. simulans, and (3) the D. simulans FRT proteome exhibits limited postmating changes irrespective of whether females mate with conspecific or heterospecific males, suggesting an active female role in mediating reproductive interactions. Our study suggests that divergence in the FRT extracellular environment and postmating response contribute to previously described patterns of postmating-prezygotic isolation and the maintenance of species boundaries.

2020-06-25 | PXD017708 | Pride

Opioid withdrawal produces sex-specific effects on fentanyl-vs.-food choice and mesolimbic transcription

Project description:Background: Opioid withdrawal is a key driver of opioid addiction and an obstacle to recovery. However, withdrawal effects on opioid reinforcement and mesolimbic neuroadaptation are understudied and the role of sex is largely unknown. Methods: Male (n=13) and female (n=12) rats responded under a fentanyl-vs.-food “choice” procedure during daily 2h sessions. In addition to the daily choice sessions, rats were provided extended access to fentanyl during 12h self-administration sessions. After two weeks of this selfadministration regimen, the nucleus accumbens (NAc) and ventral tegmental area (VTA) of a subset of rats were subjected to RNA sequencing. In the remaining rats, a third week of this self-administration regimen was conducted, during which methadone effects on fentanyl-vs.-food choice were determined. Results: Prior to opioid dependence, male and female rats similarly allocated responding between fentanyl and food. Abstinence from extended fentanyl access elicited similar increases in somatic withdrawal signs in both sexes. Despite similar withdrawal signs and extended access fentanyl intake, opioid withdrawal was accompanied by a maladaptive increase in fentanyl choice in males, but not females. Behavioral sex differences corresponded with a greater number of differentially expressed genes in the NAc and VTA of opioidwithdrawn females relative to males. Methadone blocked withdrawal-associated increases in fentanyl choice in males, but failed to further decrease fentanyl choice in females. Conclusions: These results provide foundational evidence of sex-specific neuroadaptations to opioid withdrawal, which may be relevant to the female-specific resilience to withdrawal-associated increases in opioid choice and aid in the identification of novel therapeutic targets.

2021-05-06 | GSE173959 | GEO

Evolutionary quantitative proteomics of reproductive interactions in Drosophila

Project description:We present data using a novel method to simultaneously identify and quantify transferred male seminal proteins and the female reproductive proteome using multiplexed Tandem-Mass-Tag (TMT) isobaric labelling of the lower female reproductive tracts dissected from virgin- or recently mated- females of three species of the virilis group. We identified over 200 putative male ejaculate proteins many of which show differential abundance between species. We also identified over 2000 proteins providing the first description of the Drosophila female reproductive tract proteome outside of the melanogaster group which also shows significant divergence between species. We then assessed the utility of species-specific compared to single species query databases for protein identification and quantification.

2023-10-24 | PXD031638 | Pride

Project description:Drosophila simulans and D. sechellia male mate choice QTL mapping

| PRJNA558426 | ENA

Julidochromis species male vs. female 20100721

Project description:Whole brain gene expression profiling for Julidochromis transcriptus male vs. female and Julidochromis marlieri male vs female to identify sex-role biased and sex biased gene expression in these species that exhibit conventional and reversed sex-biased behavior respectively. 5 J. transcriptus male vs. female and 5 J. transcriptus female vs. male hybridizations compare 4 males and 4 females in a balanced loop design with dye-swaps that is independent of the 5 J. marlieri male vs. female and 5 J. marlieri female vs. male hybridizations compare 4 males and 4 females also in a balanced loop design with dye swaps.

2010-07-24 | E-GEOD-23094 | biostudies-arrayexpress

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

Project description:Female Nasonia 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 fertilise 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.

2018-01-11 | GSE105796 | GEO

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