The evolution of sperm storage organs in Diptera: mating responsiveness, molecular diversity andgene regulation

双翅目精子储存器官的进化：交配反应、分子多样性和基因调控

• 批准号: 531256570
• 负责人: Dr. Claudia Fricke
• 金额: --
• 依托单位: Lehrstuhl für Evolutionsbiologie
• 依托单位国家: 德国
• 项目类别: Research Grants
• 资助国家: 德国
• 项目状态: 未结题
• 来源: https://gepris.dfg.de/gepris/projekt/531256570?language=en
• 关键词: evolution; sperm; storage; organs; Diptera

The majority of females with internal fertilisation have dedicated organs to store sperm. Thereby, females can disentangle mating activity from fertilisation and egg deposition which is important when both activities happen at different locations or are separated in time. Particularly insect females have evolved highly specialized sperm storage organs. In most insect species, females possess one or several spermathecae, but some Dipteran species have an additional sperm storage organ called a seminal receptacle. While on the surface both organs serve the same function, molecular work showed that they possess distinct expression profiles and thus have taken on different specializations. Further, while in the genus Drosophila most species use both kinds of organs, some species only use one or the other type to store sperm while the remaining type seems to have lost this function and it is unclear if it evolved new functions. While the morphological variation of these organs is well described, the details of reproductive processes leading to fertilization and particularly the molecules involved, their regulation and the possible variation across species are largely unknown. Intriguingly, the specific transcription factor doublesex (dsx), long known for its developmental function in sex differentiation, was found to be expressed in adult Drosophila melanogaster spermathecae. However, its specific role in adults, particularly its possible interplay with both transcriptional regulation of sperm storage organ function and with other gene regulatory mechanisms remains elusive. Here, we propose a collaborative project to study the evolution of sperm storage organs across Diptera to address these open questions. First, we aim to investigate the molecular characteristics of female sperm storage organs by studying the possible conservation of dsx expression in female storage organs, its mating responsiveness and possible function while assessing molecular diversity in reproductive tract secretomes across Drosophila species. We hypothesize that while dsx expression is conserved across the Diptera, the downstream reproductive molecules produced in the respective sperm storage organs are not. Second, we aim to understand the gene regulatory mechanisms underlying the evolution of female reproductive organs in Diptera. We hypothesize that species that use the ancestral spermathecae as main sperm storage organs do not express the same transcription factors or do not have the same accessible chromatin regions compared to species using solely or predominantly the subsequently evolved seminal receptacle after mating. We use a comparative genomics, transcriptomics and epigenomics approach in combination with DNA-protein binding assays and machine learning to establish a framework that can be used for functional and regulatory studies to better understand the complex evolution and interplay of gene regulatory networks before and after mating in Diptera.

大多数接受内部受精的女性都有专门的器官来储存精子。因此，雌性可以将交配活动从受精和产卵中分离出来，当这两种活动发生在不同的位置或在时间上分开时，这是很重要的。特别是雌性昆虫进化出高度专业化的精子储存器官。在大多数昆虫物种中，雌性昆虫拥有一个或多个受精囊，但一些双翅目物种有一个额外的精子储存器官，称为精液容器。虽然表面上这两个器官具有相同的功能，但分子研究表明，它们具有不同的表达谱，因此呈现出不同的特化。此外，虽然在果蝇属中，大多数物种使用这两种器官，但一些物种只使用其中一种类型来存储精子，而剩下的类型似乎已经失去了这一功能，目前还不清楚它是否进化出了新的功能。虽然这些器官的形态变异已经被很好地描述，但导致受精的生殖过程的细节，特别是涉及的分子，它们的调节和可能的物种变异在很大程度上是未知的。有趣的是，长期以来一直被认为在性别分化中具有发育功能的特异转录因子Doublesex(Dsx)，被发现在成年果蝇受精囊中表达。然而，它在成人中的具体作用，特别是它与精子储存器官功能的转录调控以及与其他基因调控机制的可能相互作用，仍然难以捉摸。在这里，我们提出了一个合作项目，研究双翅目精子储存器官的进化，以解决这些悬而未决的问题。首先，我们的目的是通过研究Dsx在雌性储存器官中表达的可能保守性、交配反应和可能的功能来研究雌性精子储存器官的分子特征，同时评估不同物种生殖道分泌物的分子多样性。我们假设，虽然DSX的表达在双翅目中是保守的，但在各自的精子储存器官中产生的下游生殖分子却不是。其次，我们的目标是了解双翅目雌性生殖器官进化背后的基因调控机制。我们假设，与仅使用或主要使用交配后进化的精囊的物种相比，使用祖先精囊作为主要精子储存器官的物种表达不同的转录因子，或者不具有相同的可获得的染色质区域。我们使用比较基因组学、转录组学和表观基因组学方法，结合DNA-蛋白质结合分析和机器学习，建立了一个可用于功能和调控研究的框架，以更好地了解双翅目昆虫交配前后基因调控网络的复杂进化和相互作用。