Evolution in eternal triangles: a dynamic landscape for driving rapid changes in reproduction

雄性和雌性在繁殖方面的相互作用最终会导致生殖行为、形态和生理上惊人的多样性进化。这可以从令人惊叹的孔雀尾巴到精致而奇异的阴茎形态。当雌性与多个雄性交配时（一妻多夫制），当雌性体内存在内部受精和精子长期储存时，这种相互作用尤其强烈。这是因为即使在交配发生后，雄性之间也会频繁、激烈和持续地竞争交配和受精。在过去的几十年里，人们已经意识到，雌性和雄性之间的互动往往是敌对的，而不是合作的。这种“性冲突”之所以发生，是因为两性都可以通过一种方式来提高自己的繁殖成功率，从而导致另一方付出代价。例如，通常情况下，雄性而不是雌性通过增加交配频率来提高繁殖成功率。当这种情况发生时，一种性别的变化会导致另一种性别的变化，就像军备竞赛一样。这种雄性和雌性之间的持续往复，也被称为“对抗性共同进化”，是推动进化变化的一种广泛而有力的力量。因为它的影响集中在生殖基因的改变上，它可能导致生殖不相容。这就会导致新物种的产生。因此，性冲突很重要，因为它代表了通过增加基因变异和最终物种数量来产生生物多样性的一种强大而永恒的燃料。当诸如交配频率等现象的相对微小差异对雄性与雌性的繁殖成功率产生巨大影响时，性冲突应该特别强烈。在典型的情况下，当一个以上的雄性与一个雌性进行繁殖时，这种情况会特别强烈（“永恒的三角”，一个雌性与两个或两个以上的雄性进行交配）。因此，在繁殖决策上经常会有三种（或更多）方式的“分歧”，比如交配的频率，因为两个雄性的利益是由非常不同的结果服务的。例如，如果雌性不再交配，第一个交配的雄性就会受益。虽然我们目前有预测，但我们缺乏对这些进化分歧程度的实际测量，我们也缺乏对潜在机制的任何理解。因此，这是一个需要填补的重要空白。因此，我们的第一个目标是与果蝇一起工作，并首次测量(i)正常果蝇和（ii）“性肽（SP）”途径（我们知道它调解性冲突）在两性中被操纵的果蝇之间的差异程度。我们将使用自然和工程版本的SP途径基因，以充分确定其因果关系。我们的支持背景工作表明，原则上这是一种有效和有希望的进行方式。我们的工作提供了以下原则的证明：(a)在永恒三角形中，正常雄性和雌性的生殖成功率存在差异；(b)雌性性肽受体（SPR）的失活显著改变了所见的模式，其中包括不同雄性精子的储存和受精方式的变化。后者可能会增加男性生殖失败的几率。因此，我们的第二个目标是测试永恒三角中的性冲突是如何通过精子之间竞争的中断而导致生殖隔离的。总的来说，这项研究工作将揭示在雄性和雌性生殖决策方面的进化分歧的程度、基础和意义，这些分歧可以推动进化变化，以及它们对生殖隔离和生物多样性产生的潜在贡献。

The interplay between males and females over reproduction can ultimately lead to the evolution of spectacular diversity in reproductive behaviour, morphology and physiology. This can range from the stunning peacock's tail to elaborate and bizzare penis morphology. The interactions are particularly strong when females mate with multiple males (polyandry) and when there is internal fertilization and sperm storage for long periods within females. This is because there are then frequent, intense and continuing competitions between males for matings and for fertilizations even after matings have occurred. In the last few decades it has been realized that interactions between females and males can often be antagonistic rather than co-operative. This 'sexual conflict' occurs because each sex can increase their reproductive success in a way that can result in the expression of costs in the other sex. It is often the case, for example, that males but not females increase their reproductive success through increasing their mating frequency. When this happens, changes in one sex lead to counter changes in the other, as in an arms race. This continual back and forth between males and females, otherwise known as 'antagonistic coevolution', is a widespread and potent force for driving evolutionary change. Because its effects are focussed on changes to reproductive genes it can lead to reproductive incompatibilities. This can then lead to the creation of new species. Therefore, sexual conflict is important because it represents a potent and eternal fuel for generating biodiversity through increasing variation in genes and ultimately the number of species. Sexual conflict should be particularly strong when relatively minor differences in phenomena such as how often to mate result in large effects on the reproductive success of males in comparison to females. This will be particularly intense in the typical situation in which more than one male is involved in a reproductive bout with a single female (the 'eternal triangle' where one females mates with two or more males in series). Hence there can often be three- (or more) way 'disagreements' about reproductive decisions such as how often to mate, since the interests of the two males are served by very different outcomes. For example, the first male to mate would benefit if females never mated again. Although we currently have predictions, we lack actual measurements of the extent of these evolutionary disagreements and we also lack any understanding of the underlying mechanisms. This is therefore an important gap to fill. Our first aim is therefore to work with the fruitfly and measure for the first time the magnitude of disagreements in (i) normal flies and (ii) in those in which the 'sex peptide (SP)' pathway - which we know mediates sexual conflict - has been manipulated in both sexes. We will use natural and engineered versions of SP pathway genes, to fully pin down their causal effects. Our supporting background work shows that in principle this is a valid and promising way to proceed. Our work provides proof of principle (a) that there are differences in reproductive success for normal males and females within eternal triangles, and (b) that inactivation of sex peptide receptor (SPR) in females significantly alters the patterns seen, party through changes in how the sperm of different males are stored and used for fertilisation. The latter could increase the chance of reproductive failure for males. Our second aim is therefore to test how sexual conflict within the eternal triangle could lead to reproductive isolation via a break down in competitions between sperm. Overall, the research work will show the extent, basis and significance of evolutionary disagreements over reproductive decisions in males and females that can drive evolutionary change, and their potential contribution to reproductive isolation and the generation of biodiversity.