Detecting the genomic imprints of extreme sexual selection - Genetic architecture of SSD and male self-sacrificial traits in a sexually cannibalistic widow spider

高通量测序技术的最新进展为以合理的成本解开复杂性状的遗传基础提供了前所未有的机会。在这里，我们建议研究在性别冲突下进化的适应组合的遗传和遗传结构。澳大利亚红背蜘蛛Latrodectus hasselti已经成为自杀交配的教科书范例。求爱的雄鱼表演一个壮观的后空翻，将它们的腹部直接带到雌性海龟身上。这种奇怪的行为会招致同类相食，但也会延长交配时间。奇怪的是，在雌性通过收缩腹部造成的第一次交配中，雄性可以存活下来。雄性通过切断雌性授精管道内的精子转移栓子的末端硬骨来确保父子关系，然后该栓子起到塞子的作用。这一特征集是一夫一妻制交配系统的一部分，在该系统中，雄性被选择来最终投资于交配和确保与单一雌性的父子关系。一夫一妻制与男性偏见的性别比例和男性侏儒症并存。有趣的是，来自新西兰的红背蜘蛛的姐妹物种L.Katipo的交配系统非常不同。雌性L.Katipo既不具攻击性，也不食人，雄性不翻筋斗，可以多次交配。性别大小的二形性也不那么明显。这两个物种直到最近才出现分歧，人们知道它们会杂交并产生可生育的后代。以往的实验表明，在一年内可以饲养3代。因此，这对黑寡妇非常适合解开复杂交配系统进化的遗传结构。我们计划在实验室里对这两个物种进行杂交，以获得将与两个父本物种的雄性进行杂交和回交的F1杂交种。我们将记录F2代中4个相关交配性状的遗传和分离，(I)翻筋斗，(Ii)帮助雄性存活的腹部结构，(Iii)交配插头和(Iv)雄性成年体型。此外，我们将对目标物种的基因组进行测序，并对所研究的交配性状进行群体基因组和QTL定位分析。最后，我们将解剖男性的大脑，并比较自我牺牲行为不同的男性之间的基因表达。该研究项目将揭示无与伦比的洞察力，揭示在性选择下进化迅速且可能一致的特征的遗传结构。我们还将为多种进一步的方法奠定基础，例如结合两性的协同进化，并最终可能允许在一个不寻常的交配系统中重构性对抗的共同进化。

Recent advances in high throughput sequencing technology offer unprecedented opportunities to unravel the genetic basis of complex traits at reasonable costs. Here we propose to study the inheritance and the genetic architecture of a combination of adaptations that evolved under sexual conflict. The Australian redback spider, Latrodectus hasselti, has become a textbook example for suicidal mating. Courting males perform a spectacular backwards somersault that brings their abdomen directly onto the female chelicerae. This peculiar behaviour invites cannibalism but also prolongs copulation. Curiously, the males can survive injuries during a 1st copulation inflicted by the female by constricting their abdomen. Males secure paternity by breaking off a terminal sclerite of the sperm-transferring embolus inside the female insemination duct, which then functions as a plug. This trait set is part of a monogynous mating system in which males are selected to invest terminally in mating and securing paternity with a single female. Monogyny co-occurs with a male biased sex-ratio and male dwarfism. Interestingly, the redback spider’s sister species L. katipo from New Zealand is distinguished by a very different mating system. Females of L. katipo are neither aggressive nor cannibalistic and the males do not somersault and can mate multiple times. Sexual size dimorphism is also less pronounced. The two species diverged only recently and are known to hybridize and produce fertile offspring. Previous experiments have shown that 3 generations can be raised within a single year. This species pair of black widows is thus ideally suited to unravel the genetic architecture of the evolution of complex mating systems. We plan to crossbreed the two species in the lab to achieve F1 hybrids that will be crossed and backcrossed with males from both paternal species. We will document inheritance and segregation of 4 related mating traits, (i) the somersaulting, (ii) the abdominal construction that helps males survive copulation, (iii) the mating plug and (iv) male adult body size, in the F2 generation. Additionally, we will sequence the target species’ genomes and perform population genomic as well as QTL mapping analysis of the studied mating traits. Finally, we will dissect male brains and compare gene-expression between males that vary in self-sacrificial behaviour. The research project will reveal unparalleled insights into the genetic architecture of traits that evolved rapidly and likely in concert under sexual selection. We will also lay the foundation for multiple further approaches that e.g. incorporate concerted evolution in both sexes and may eventually permit a reconstruction of sexually antagonistic co-evolution in an unusual mating system.