Thermal phenotypic plasticity of pre- and post-copulatory male harm buffers sexual conflict in wildDrosophila melanogaster

Abstract

Strong sexual selection frequently leads to sexual conflict and ensuing male harm, whereby males increase their reproductive success at the expense of harming females. Male harm is a widespread evolutionary phenomenon with a strong bearing on population viability. Thus, understanding how it unfolds in the wild is a current priority. Here, we sampled a wild Drosophila melanogaster population and studied male harm across the normal range of temperatures under which it reproduces optimally in nature by comparing female lifetime reproductive success and underlying male harm mechanisms under monogamy (i.e., low male competition/harm) vs. polyandry (i.e., high male competition/harm). While females had equal lifetime reproductive success across temperatures under monogamy, polygamy resulted in a maximum decrease of female fitness at 24 degrees C (relative harm; H = 0.36), reducing its impact at both 20 degrees C (H = 0.22), and 28 degrees C (H = 0.10). Furthermore, female fitness components and pre- (i.e., harassment) and post-copulatory (i.e., ejaculate toxicity) mechanisms of male harm were asymmetrically affected by temperature. At 20 degrees C, male harassment of females was reduced, and high male competition accelerated female actuarial senescence. In contrast, at 28 degrees C male ejaculate effects on female reproduction were modulated, and high male competition mostly resulted in accelerated reproductive ageing. We thus show that, across a natural thermal range, sexual conflict processes and their effects on female fitness components are plastic and complex. As a result, the net effect of male harm on overall population viability is likely to be lower than previously surmised. We discuss how such plasticity may affect selection, adaptation and, ultimately, evolutionary rescue under a warming climate.

Environmental complexity mitigates the demographic impact of sexual selection

“…We predicted that this negative demographic impact can be mitigated by environmental complexity and increased opportunities for individuals to modulate behaviour in response to the intensity of mating interactions and that this effect would become more apparent and of greater importance during rapid environmental change and population decline (Londoño‐Nieto et al., 2022; Martínez‐Ruiz & Knell, 2017; Svensson & Connallon, 2019). We found evidence for this prediction, with N + S populations derived from sexually selected experimental evolution lines maintaining higher census sizes (Figure 2) and more stable growth rates (Figure 3) when reared in complex environments under the heatwave, compared to N population derived from monogamous lines.…”

“…Recent theoretical studies have shown that this type of sexual conflict could lead to increased extinction risk in already maladapted populations (Flintham et al., 2023; Gómez‐Llano et al., 2023; Martínez‐Ruiz & Knell, 2017). Moreover, as males of high genetic quality are likely to impose more harm to their female mates compared to males of low quality (Baur et al., 2022; Londoño‐Nieto et al., 2022; Yun et al., 2017), this effect could cancel out or even outweigh any potential population benefits of purifying sexual selection on male genetic quality (Chenoweth et al., 2015; Flintham et al., 2023).…”