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Linking population genomic and behavioural data to test fundamental hypotheses of sexually antagonistic coevolution.

Periodic Reporting for period 1 - PopGenSexCon (Linking population genomic and behavioural data to test fundamental hypotheses of sexually antagonistic coevolution.)

Reporting period: 2023-02-01 to 2025-01-31

Sexual conflict and sexually antagonistic coevolution (SAC) are compelling hypotheses to explain some of the extraordinary diversity in morphological and behavioral traits observed in nature. However, the study of the genomic foundations of this conflict and the resulting population genetic dynamics are still in their infancy. This is due to a lack of knowledge about the genetic underpinnings of the most well understood sexual conflict traits. The predictions of SAC, in particular the prediction that relative exaggeration of male and female traits should predict outcomes of mating interactions, remain untested at the genomic level. An exception to the rule are the seminal fluid and female reproductive tract proteins that interact and mediate conflicts over remating rates in the cosmopolitan model species Drosophila melanogaster. However, in this system a population-level perspective to investigate population genomic signals of SAC and the consequences for outcomes of mating interactions within and across populations is lacking. My project will address these remaining questions by taking advantage of a Europe-wide population genetic data-set, as well as an ongoing pan-European collaborative sampling and phenotyping effort of D. melanogaster. My aim is to understand how sexual conflict has shaped co-evolutionary patterns at genetic loci involved in sexually antagonistic traits. In addition, I will investigate the consequences of this genetic coevolution on contemporary male-female interactions. My project has three objectives: i) a population genomic analysis of population genomic data from European D. melanogaster populations, ii) lab-based behavioural experiments to investigate the male-female interactions for inbred lines obtained from populations with extreme patterns of coevolution, iii) and indirect study of the consequences of coevolution on natural behaviour via sampling of wild-caught females and determining mating/re-mating rates. This project will increase our understanding of the role of sexual conflict and sexually antagonistic coevolution in population divergence and set a standard for investigations of the genomic causes and consequences of SAC. I expect this project to produce one or two high-impact manuscripts to be published in top-tier journals as the first test of SAC predictions at the genomic level.
My project had three objectives: i) a population genomic analysis of population genomic data from European D. melanogaster populations, ii) lab-based behavioural experiments to investigate the male-female interactions for inbred lines obtained from populations with extreme patterns of coevolution, iii) and indirect study of the consequences of coevolution on natural behaviour via sampling of wild-caught females and determining mating/re-mating rates. To-date (Feb 2025) I have fully completed parts I) and II), both of which took longer than anticipated.

I) I have completed a comprehensive population genomic analysis of the male- and female- components of the sex-peptide network. In order to complete this I had to develop procedures to use analytical methods not previously used for genetic data. The main results of this work finds that there is strong evidence for a co-evolutionary process shaping patterns of genetic diversity at these loci. Moreover, we can use these genetic patterns to identify populations where males- or females- should show a relative advantage in sexual conflicts.

II) on the basis of results in part I), I identified 2 populations where males should be at an advantage, 2 populations where females should have an advantage, and 2 populations where the sexes should be roughly equally matched. I limited myself to choosing from populations from which isofemale lines had already been established by the DrosEU consortium, which I then used to conduct a large-scale mating and re-mating experiment in the lab. The main achievement of this work is that I can show that to a large extent, observations match the predictions from SAC theory very closely in this system.
My project has achieved two of the three stated goals, and the results for the first time test and confirm predictions of SAC at the genomic level. This work and these findings will set a precedent that SAC theory can be generalised to the molecular level and set a standard for how such links should be established in other systems. I have already presented these findings at conferences and I am preparing manuscripts for publication which I anticipate will have a high-impact.
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