Female-limited X chromosome evolution reveals that lifespan is mainly modulated by interlocus rather than intralocus sexual conflict

Abstract

Abstract: Sexual dimorphism in somatic investment may be shaped by two distinct forms of sexual conflict; under intralocus sexual conflict (IASC), males and females have different optimal levels of somatic investment but are constrained from reaching their respective optima by their shared genome, while under interlocus sexual conflict (IRSC), males and females have different optimal sexual strategies, which could have direct or indirect effects on levels of somatic investment. We investigated effects of IASC and IRSC on two aspects of somatic investment, immune defence strategies and longevity, using previously established female-limited experimental evolution lines in Drosophila melanogaster. We found little evidence for any effect of either type of sexual conflict on investment in the immune defence resistance or tolerance. Nor did we find convincing evidence that longevity is subject to IASC in this species. However, we did find evidence that increased female control over mating rate had important and opposite effects on longevity between the sexes. Specifically, females that had adapted to high levels of female control over mating had a longer lifespan when kept in mixed-sex groups, while males had shorter longevity, perhaps due to increased investment in post-copulatory sexual selection. These novel results show that female control over mating rates may have important and unexpected effects on patterns of somatic investment.

Significance statement: Sexual conflict occurs between the two sexes over numerous life history traits, and it is complex to disentangle how these traits interact and affect each other. Here we use a long-term evolution experiment to investigate sexual dimorphism in somatic maintenance. We found no effect of feminising the X chromosome on female immune defence. However, we did find that increased female control over mating rate resulted in longer female lifespan, but reduced male lifespan, and that these effects were dependent on social context (isolated or in mixed-sex groups). Unlike previous studies on the effect of sexual conflict on longevity, our experiment did not manipulate environmental conditions nor the adult sex ratio, which is likely to reduce both pre- and post-copulatory sexual selection.

Supplementary information: The online version contains supplementary material available at 10.1007/s00265-022-03231-4.

Keywords: Drosophila melanogaster; Experimental evolution; Longevity; Resistance; Sexual antagonism; Tolerance.

Fig. 1

Lifespan for the different selection regimes in both sexes either isolated or in mixed-sex groups. Light grey line: FLX regime, dark grey line: CFM regime, and black line Cwt regime. a Female lifespan when isolated. We did not find any significant difference in lifespan between the three regimes when kept isolated. b Female lifespan in mixed-sex groups. We did find a significant difference in lifespan between the three regimes when the females were continuously exposed to males (p = 0.030). c Male lifespan when isolated. We found a significant difference in lifespan between the three regimes when the males were kept isolated (p = 6.765e⁻⁰⁵). d Male lifespan in mixed-sex groups. There were no significant different in lifespan between the three regimes, when the males could continuously mate with females