How males respond to rivals: an integrated study of molecular mechanisms and fitness consequences

许多不同的哺乳动物、鸟类和无脊椎动物的雄性对它们的社会和性环境做出反应。这些反应对它们的繁殖成功有着深远的影响。例如，许多物种的雄性在交配过程中会将更多的精子转移给雌性，以增加自己的父权份额。然而，从发现来自对手雄性的线索，到对雄性射精成分的影响，再到最终的繁殖成功，整个过程尚不清楚。我们也不知道对竞争对手的反应对男性衰老的影响。发现竞争对手和父权之间的途径代表了理解雄性交配成功进化的下一个关键阶段。在这个提案中，我们的目标是提供第一个案例研究，使用果蝇。果蝇提供了一个独特的机会，它的基因组已经被测序，有许多不同的基因试剂可以用来操纵雄性对竞争对手数量的感知。我们还产生了大量相关和新颖的背景数据。例如，雄性在交配前对竞争对手的存在做出反应，随后当它们遇到雌性时，交配时间更长。更重要的是，在更长时间的交配中，它们传递了更多的关键射精成分，这增加了后代的总数。雄性似乎通过闻到一种特殊的雄性信息素来探测对手。对纯研究的重要性：这项工作解决了一些至关重要的问题：男性如何应对竞争对手，以及这样做对健康的影响是什么。当射精量有限时（例如，当雄性交配几次就筋疲力尽时），雄性根据存在的竞争雄性的数量，将射精分配给不同的交配对象和不同的雌性。然而，尽管大量的研究表明男性会这样做，关键问题仍然存在：(i)男性发出信号和感知竞争对手的分子机制是什么？（ii）对于那些对竞争对手的存在做出反应的男性来说，总体后果是什么，尤其是对衰老的影响。这些都是我们要回答的问题。应用研究的重要性：同样重要的是，我们的工作将提供改进害虫控制的技术。害虫是世界上最严重的农业（和健康）问题的根源。研究的重点是以生物防治为基本原理的方法。然而，为控制而繁殖的雄性往往交配成功率很低。我们的目标是提供方法来改善这一点（例如，简单的饲养规则，以增加暴露于竞争对手或信息素）使用果蝇，这是唯一的物种，相关的背景数据和遗传试剂可用。我们计划将来将我们的发现应用于害虫。方法：我们将控制雄性的数量和与竞争对手接触的时间，以及我们的工作强调的重要的嗅觉通路。我们可以测试在交配过程中转移给雌性的射精蛋白的数量，使用的方法是由我们的项目伙伴，康奈尔大学的Mariana Wolfner开发的。我们可以通过染色和计数转移的精子来检测精子转移。为了测试对竞争对手的反应对雄性衰老的影响，我们将比较在与竞争对手接触或不接触后交配的雄性的寿命和繁殖成功率。及时性和原创性：我们的提议将首次对雄性对竞争对手做出反应的完整途径进行调查。鉴于最近嗅觉受体的阐明，我们最近发现在竞争对手存在时射精成分的变化，以及最近在遗传虫害控制方面的发展激增，这项工作是及时的。

Males of many different mammal, bird and invertebrate species respond to their social and sexual environment. These responses have profound effects on their reproductive success. For example, males of many species that perceive rivals transfer more sperm to females during mating, to increase their share of paternity. However, the complete pathway from the detection of cues from rival males, to effects on the composition of the male ejaculate through to ultimate reproductive success is not known. Nor do we know the effects on ageing for males of responding to rivals. The discovery of the pathway between rival detection and paternity represents the next key stage in understanding the evolution of male mating success. In this proposal we aim to provide the first case study, using the fruitfly. The fruitfly offers a unique opportunity, its genome has been sequenced and there are many different genetic reagents available with which to manipulate a male's perception of the number of rivals present. We have also generated a substantial amount of relevant and novel background data. For example, males respond to the presence of rivals before mating, and subsequently mate for longer when they do meet a female. More importantly, during those longer matings they transfer more of key ejaculate components, which increase the overall number of offspring fathered. Males appear to detect rivals by smelling a particular male pheromone. Importance for pure research: The work tackles questions of fundamental importance: how do males respond to rivals and what are the fitness consequences of doing so. When ejaculates are limiting (e.g. when males that mate just a few times become exhausted), males partition their ejaculates among different matings and different females, according to how many rival males are present. However, despite the wealth of studies showing that males do this, key questions remain: (i) what are molecular mechanisms by which males signal and perceive rivals? and (ii) what are the overall consequences, particularly the impact on ageing, for males that respond to the presence of rivals. These are the questions we will answer. Importance for applied research: Of equal importance, our work will provide techniques to improve insect pest control. Insect pests are the source of the world's most serious agricultural (and health) problems. Research is focusing on methods whose basic principles lie in biological control. However, males produced for control often have poor mating success. We aim to provide methods to improve this (e.g. simple husbandry rules to increase exposure to rivals or pheromones) using the fruitfly, which is the only species in which the relevant background data and genetic reagents are available. We plan to apply our findings to pests in the future. Methodology: We will manipulate male numbers and length of exposure to rivals, and the smell pathways that our work has highlighted as important. We can test the amount of ejaculate proteins transferred to females during mating using a method developed by our project partner, Mariana Wolfner from Cornell University. We can test for sperm transfer by staining and counting the sperm transferred. To test for the effects of responding to rivals on male ageing, we will compare the lifespan and reproductive success of males that mate following exposure, or not, to rivals. Timeliness and originality: Our proposal will provide the first investigation of the complete pathway by which males respond to rivals. The work is timely given the recent elucidation of smell receptors, our recent discoveries of changes to ejaculate composition in the presence of rivals and the recent surge of developments in genetic insect pest control.