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

许多不同哺乳动物、鸟类和无脊椎动物的雄性会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，以增加它们的父子份额。然而，从发现竞争对手雄性的线索，到影响雄性射精的成分，再到最终繁殖成功的完整途径尚不清楚。我们也不知道回应竞争对手对男性衰老的影响。竞争对手检测和亲子鉴定之间路径的发现，代表着理解雄性交配成功进化的下一个关键阶段。在这项提案中，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，有许多不同的遗传试剂可以用来操纵雄性对在场竞争对手数量的感知。我们还生成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，交配时间会更长。更重要的是，在这些较长的交配过程中，它们转移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定的雄性信息素来发现竞争对手。对于纯研究的重要性：这项工作解决了根本重要的问题：男性如何应对竞争对手，这样做会带来什么健康后果。当射精是有限的(例如，当只交配几次的雄性变得筋疲力尽时)，雄性根据有多少竞争对手的存在，将它们的射精分配给不同的交配和不同的雌性。然而，尽管有大量研究表明男性会这样做，但关键的问题仍然存在：(I)男性发出信号和感知竞争对手的分子机制是什么？以及(Ii)对男性在竞争对手的存在做出反应的总体后果是什么，特别是对衰老的影响。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虫害控制的技术。虫害是世界上最严重的农业(和健康)问题的根源。研究的重点是其基本原理在于生物防治的方法。然而，为控制而生产的雄性通常交配成功率很低。我们的目标是利用果蝇提供改进这一点的方法(例如，增加对竞争对手或信息素的暴露的简单饲养规则)，这是唯一可以获得相关背景数据和遗传试剂的物种。我们计划在未来将我们的发现应用于害虫。方法：我们将操纵男性数量和与竞争对手接触的时间，以及我们的工作强调的气味途径。我们可以使用我们的项目合作伙伴康奈尔大学的玛丽安娜·沃尔夫纳开发的一种方法来测试交配过程中转移给雌性的射精蛋白质的数量。我们可以通过对转移的精子进行染色和计数来测试精子转移。为了测试对竞争对手的反应对男性衰老的影响，我们将比较接触或不接触后交配的雄性与竞争对手的寿命和生殖成功。及时性和原创性：我们的建议将首次对男性对竞争对手做出反应的完整途径进行调查。考虑到最近对嗅觉受体的阐明，我们最近发现在竞争对手存在的情况下射精成分发生了变化，以及最近基因害虫控制的发展激增，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.