Estación Biológica de Doñana - CSIC, Seville, 41092, Spain.
School of Biological Sciences, Monash University, Clayton, 3800, VIC, Australia.
Heredity (Edinb). 2018 Sep;121(3):282-291. doi: 10.1038/s41437-018-0093-y. Epub 2018 May 25.
Mating often bears large costs to females, especially in species with high levels of sexual conflict over mating rates. Given the direct costs to females associated with multiple mating, which include reductions in lifespan and lifetime reproductive success, past research focused on identifying potential indirect benefits (through increases in offspring fitness) that females may accrue. Far less attention has, however, been devoted to understanding how costs of sexual interactions to females may extend across generations. Hence, little is known about the transgenerational implications of variation in mating rates, or the net consequences of maternal sexual activities across generations. Using the seed beetle, Callosobruchus maculatus, a model system for the study of sexual conflict, we investigate the effects of mating with multiple males versus a single male, and tease apart effects due to sexual harassment and those due to mating per se, over three generations. A multigenerational analysis indicated that females that were exposed to ongoing sexual harassment and who also were permitted to mate with multiple males showed no difference in net fitness compared to females that mated just once without ongoing harassment. Intriguingly, however, females that were continually harassed, but permitted to mate just once, suffered a severe decline in net fitness compared to females that were singly (not harassed) or multiply mated (harassed, but potentially gaining benefits via mating with multiple males). Overall, the enhanced fitness in multiply mated compared to harassed females may indicate that multiple mating confers transgenerational benefits. These benefits may counteract, but do not exceed (i.e., we found no difference between singly and multiply mated females), the large transgenerational costs of harassment. Our study highlights the importance of examining transgenerational effects from an inclusive (looking at both indirect benefits but also costs) perspective, and the need to investigate transgenerational effects across several generations if we are to fully understand the consequences of sexual interactions, sexual conflict evolution, and the interplay of sexual conflict and multi-generational costs and benefits.
交配通常会给雌性带来巨大的代价，尤其是在那些交配率存在高度性冲突的物种中。考虑到雌性多次交配所带来的直接代价，包括寿命和终生繁殖成功率的降低，过去的研究主要集中在确定雌性可能获得的潜在间接利益（通过增加后代的适应性）上。然而，对于雌性的性相互作用成本如何在代际间延伸，人们的关注要少得多。因此，人们对交配率的变化对代际的影响，或者母性行为在代际间的净后果知之甚少。我们利用斑皮豆象（Callosobruchus maculatus）作为性冲突研究的模型系统，研究了与多个雄性交配与与单个雄性交配的影响，并在三代中分离了由于性骚扰和交配本身所带来的影响。多代分析表明，与那些只交配一次且没有持续骚扰的雌性相比，那些持续受到性骚扰且被允许与多个雄性交配的雌性在净适应度上没有差异。然而，有趣的是，与那些只受到一次骚扰（未受到骚扰）或多次交配（受到骚扰，但通过与多个雄性交配可能获得利益）的雌性相比，那些持续受到骚扰但只允许交配一次的雌性的净适应度严重下降。总的来说，与受骚扰的雌性相比，多次交配的雌性适应性增强，这可能表明多次交配带来了跨代利益。这些利益可能抵消了（但没有超过，即我们没有发现单次交配和多次交配的雌性之间有差异）骚扰的巨大跨代代价。我们的研究强调了从包容性的角度（同时考虑间接利益和成本）来研究跨代效应的重要性，以及如果我们要充分理解性相互作用、性冲突进化以及性冲突和多代成本和利益之间相互作用的后果，就需要在几代中研究跨代效应。
