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

雄性和雌性之间在繁殖上的相互作用最终会导致生殖行为、形态和生理上惊人多样性的进化。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（一妻多夫制）时，以及当雌性体内存在长期受精和精子储存时，这种相互作用特别强烈。这是因为，即使在交配之后，雄性之间也会为交配和受精而进行频繁、激烈和持续的竞争。 在过去的几十年里，人们已经意识到，女性和男性之间的互动往往是对立的，而不是合作的。这种“性冲突”的发生是因为每一种性别都能以一种可能导致另一种性别付出代价的方式来提高生殖成功率。例如，通常情况下，雄性而不是雌性通过增加交配频率来增加繁殖成功率。当这种情况发生时，一种性别的变化会导致另一种性别的反变化，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”，是推动进化变化的广泛而强大的力量。因为它的影响集中在生殖基因的变化上，它可能导致生殖不相容。这可能会导致新物种的产生。 因此，性冲突是重要的，因为它代表了一个强大的和永恒的燃料，通过增加基因的变化，并最终物种的数量产生生物多样性。 当交配频率等现象的相对微小差异对雄性与雌性相比的生殖成功产生巨大影响时，性冲突应该特别强烈。这将是特别激烈的典型情况下，其中一个以上的男性参与生殖回合与一个单一的女性（'永恒的三角形'，其中一个女性交配与两个或两个以上的男性在系列）。因此，经常会有三种（或更多）关于生殖决定的“分歧”，例如多久交配一次，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，第一个交配的雄性将受益。 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了解。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）在两性中操纵“性肽（SP）”途径（我们知道它介导性冲突）的果蝇中的分歧程度。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的影响。 我们的支持背景工作表明，原则上这是一个有效和有希望的方式。我们的工作提供了以下原则的证据：（a）在永恒三角形内，正常男性和女性的生殖成功率存在差异;（B）女性性肽受体（SPR）的失活显著改变了所观察到的模式，主要是通过改变不同男性精子的储存和用于受精的方式。后者可能会增加男性生殖失败的机会。因此，我们的第二个目标是测试永恒三角中的性冲突如何通过打破精子之间的竞争而导致生殖隔离。 总体而言，研究工作将显示进化分歧的程度，基础和意义，男性和女性的生殖决策，可以推动进化的变化，以及它们对生殖隔离和生物多样性的产生的潜在贡献。

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.