Sex peptide receptor-regulated polyandry modulates the balance of pre- and post-copulatory sexual selection in Drosophila

Juliano Morimoto,Tracey Chapman,Jennifer C Perry,Tommaso Pizzari,Emelia Smith,Damian T Smith,Stuart Wigby,Grant C Mcdonald

doi:10.1038/s41467-018-08113-w

Juliano Morimoto, Tracey Chapman + Show 6 more

Open Access

https://doi.org/10.1038/s41467-018-08113-w

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Abstract

Polyandry prolongs sexual selection on males by forcing ejaculates to compete for fertilisation. Recent theory predicts that increasing polyandry may weaken pre-copulatory sexual selection on males and increase the relative importance of post-copulatory sexual selection, but experimental tests of this prediction are lacking. Here, we manipulate the polyandry levels in groups of Drosophila melanogaster by deletion of the female sex peptide receptor. We show that groups in which the sex-peptide-receptor is absent in females (SPR-) have higher polyandry, and – as a result – weaker pre-copulatory sexual selection on male mating success, compared to controls. Post-copulatory selection on male paternity share is relatively more important in SPR- groups, where males gain additional paternity by mating repeatedly with the same females. These results provide experimental evidence that elevated polyandry weakens pre-copulatory sexual selection on males, shifts selection to post-copulatory events, and that the sex peptide pathway can play a key role in modulating this process in Drosophila.

Highlights

Polyandry prolongs sexual selection on males by forcing ejaculates to compete for fertilisation
We found that polyandry levels were significantly elevated in SP receptor (SPR)− groups relative to controlSPR groups (Supplementary Figure 2A)
The single focal male in each group accounted for approximately one-third of the matings observed, while his three rivals accounted for the remaining two-thirds (F test: Focal vs. Rivals: F1,112 = 20.050, p < 0.001), with no statistically significant differences between the patterns observed in SPR− and controlSPR treatments (F test: Focal vs. Rivals × Treatment: F1,110 = 1.220, p value = 0.272; Supplementary Table 1)

Summary

Introduction

Polyandry prolongs sexual selection on males by forcing ejaculates to compete for fertilisation. We tested the hypothesis that elevated polyandry in groups where females lack SPR (i.e. SPR−) will weaken pre-copulatory selection on male mating success (the Bateman gradient40), and increase the relative contribution of post-copulatory selection (i.e., the proportion of the variance in male reproductive success explained by variance in paternity share), thereby altering the overall opportunity for sexual selection on males. We tested whether increasing levels of polyandry modulated the operation of sexual selection by influencing the relationship between the polygyny of males and the polyandry of their female mates, and the covariance between male pre- and post-copulatory performance (i.e. mating success and paternity share, respectively)

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