Quantifying fitness benefits of polyandry in Atlantic salmon

量化大西洋鲑鱼一妻多夫的健康益处

• 批准号: NE/I015523/1
• 负责人: Matthew Gage
• 金额: $ 6.75万
• 依托单位: University of East Anglia
• 依托单位国家: 英国
• 项目类别: Research Grant
• 财政年份: 2011
• 资助国家: 英国
• 起止时间: 2011 至 无数据
• 项目状态: 已结题
• 来源: https://gtr.ukri.org/projects?ref=NE%2FI015523%2F1
• 关键词: Quantifying; fitness; benefits; polyandry; Atlantic

Why do females of so many species mate with multiple males, when they gain nothing from this 'polyandry' apart from spermatozoa, and mating with only one male is sufficient to ensure full fertility? This remains an enduring question in evolutionary biology, because significant costs have been measured for females when they multiply mate. We now know that the mechanisms operating at the gamete level between mating and fertilization are much more complex than previously supposed. Under polyandry, with bigger and more diverse populations of spermatozoa competing for fertilization, there is even more selective opportunity for adaptations that promote sperm competitive ability, and / or cryptic female choice. Recent experimental research suggests that polyandry allows females to 'capture' genetic benefits at the gamete level for their resulting offspring. Such benefits may arise because of links between sperm quality and general fitness, or because females have evolved mechanisms that allow selection of sperm that carry intrinsically superior genes or undamaged DNA, or there may be cryptic choice for sperm that carry genes that are more compatibile to the female/egg genotype. We propose to quantify benefits of polyandry in a system using carefully controlled in vitro fertilizations to create offspring batches from the same female that only differ according to whether they were fertilized by five separate males singly, or by the same five males but in simultaneous sperm competition. Our experimental model will be the Atlantic salmon, in which females naturally mate with up to 16 males at once, and where external fertilization allows us to conduct in vitro fertilizations that control or eliminate a number of important confounding effects on offspring fitness, such as biased or variable maternal investment in egg quality. Our previous work on salmon in vitro fertilization dynamics will allow us to ensure that fertility is not a limiting factor for each egg batch. For each female, we will create 5 egg batches which were fertilized by sperm from 5 different, single males (=monandrous condition), and 5 egg batches that were fertilized by homogenised mixes of sperm from the same 5 males (= polyandry condition). These paired comparisons will be repeated 25 times, using 25 females and 125 males. The design will control for adult identity and egg effects, and generate offspring batches that only differ according to fertilization in the presence or absence of sperm competition and/or egg choice. After fertilization, the offspring batches will be measured for survival and growth across key stages of embryo development, egg hatch, alevin development, fry emergence, and parr survival, success and growth. These fitness measures will all be conducted in experimental stream sections that allow environmentally-relevant selection to operate. Use of the Ims salmon field station in Norway will provide access to facilities that enable experimental control, while rearing eggs and fry in semi-natural conditions with selection from many of the normal forces that operate on salmon eggs, embryos, fry and parr. It is essential that we measure egg and offspring perfomance under conditions that present some selection from the natural environment, because this is where fitness benefits will be most important. At the conclusion of the project, we will have measured what fitness benefits can be gained under polyandry, and what life stages these gains occur in salmon. The results will be of central importance to a pure understanding of the genetic benefits of polyandry. Importantly, our work will have applied relevance for salmon hatchery breeding strategies. To conserve genetic diversity, hatchery protocols now use enforced monogamy to maximize the number of male breeders involved in reproduction. However, there may be important polyandry benefits that are excluded by these protocols, and our project will measure how important these benefits might be.

为什么这么多物种的雌性会与多个雄性交配，除了精子之外，它们从这种“一妻多夫制”中得不到任何好处，而且只与一个雄性交配就足以确保完全的生育能力？这在进化生物学中仍然是一个持久的问题，因为雌性繁殖配偶的成本很高。我们现在知道，在配子水平上，在交配和受精之间运作的机制比以前想象的要复杂得多。在一妻多夫制下，有更大、更多样化的精子群体竞争受精，有更多的选择机会来促进精子的竞争能力，和/或隐藏的雌性选择。最近的实验研究表明，一妻多夫制允许雌性在配子水平上为其后代“捕获”遗传利益。这些好处可能是因为精子质量和总体适应性之间的联系，或者因为女性已经进化出允许选择携带内在优越基因或未受损DNA的精子的机制，或者可能存在对携带与女性/卵子基因型更相容的基因的精子的隐性选择。我们建议量化一妻多夫制在一个系统中的好处，该系统使用精心控制的体外受精来从同一雌性中产生后代批次，这些后代批次仅根据它们是由五个单独的雄性单独受精，还是由相同的五个雄性同时竞争精子而受精而不同。我们的实验模型将是大西洋鲑鱼，雌性鲑鱼一次自然地与多达16只雄性鲑鱼交配，外部受精允许我们进行体外受精，控制或消除一些对后代适应性的重要混杂影响，例如对卵子质量的偏差或可变的母体投资。我们之前对鲑鱼体外受精动态的研究将使我们能够确保生育能力不是每批卵的限制因素。对于每个雌性，我们将创造5个卵子批次，这些卵子批次由来自5个不同的单一雄性的精子受精（=单雄条件），以及5个卵子批次由来自相同5个雄性的均匀混合精子受精（=多雄条件）。这些配对比较将重复25次，使用25名女性和125名男性。该设计将控制成人身份和卵子的影响，并产生仅根据受精在精子竞争和/或卵子选择是否存在而不同的后代批次。受精后，将测量后代批次的存活和生长情况，包括胚胎发育、卵孵化、卵泡发育、鱼苗羽化以及伴侣存活、成功和生长的关键阶段。这些适应性措施都将在实验河段进行，以便进行与环境相关的选择。利用挪威的伊姆斯鲑鱼野外站，将提供能够进行实验控制的设施，同时在半自然条件下饲养鸡蛋和鱼苗，从许多对鲑鱼卵、胚胎、鱼苗和幼崽起作用的正常力量中进行选择。我们必须在自然环境中进行一些选择的条件下测量卵子和后代的表现，因为这是健康效益最重要的地方。在项目结束时，我们将测量在一妻多夫制下可以获得的健康益处，以及这些益处发生在鲑鱼的哪个生命阶段。这些结果对于纯粹理解一妻多夫制的遗传益处至关重要。重要的是，我们的工作将适用于鲑鱼孵化场育种策略。为了保护遗传多样性，现在的孵化场协议使用强制的一夫一妻制，以最大限度地增加参与繁殖的雄性育种者的数量。然而，可能有重要的一妻多夫制的好处被排除在这些协议之外，我们的项目将测量这些好处的重要性。

项目成果

Assessing risks of invasion through gamete performance: farm Atlantic salmon sperm and eggs show equivalence in function, fertility, compatibility and competitiveness to wild Atlantic salmon.

• DOI: 10.1111/eva.12148
• 发表时间: 2014-04
• 期刊: Evolutionary applications
• 影响因子: 4.1
• 作者: Yeates SE;Einum S;Fleming IA;Holt WV;Gage MJ
• 通讯作者: Gage MJ

Cryptic choice of conspecific sperm controlled by the impact of ovarian fluid on sperm swimming behavior.

• DOI: 10.1111/evo.12208
• 发表时间: 2013-12
• 期刊: Evolution; international journal of organic evolution
• 作者: Yeates SE;Diamond SE;Einum S;Emerson BC;Holt WV;Gage MJ
• 通讯作者: Gage MJ

Post-copulatory opportunities for sperm competition and cryptic female choice provide no offspring fitness benefits in externally fertilizing salmon.

• DOI: 10.1098/rsos.150709
• 发表时间: 2016-03
• 期刊: Royal Society open science
• 影响因子: 3.5
• 作者: Lumley AJ;Diamond SE;Einum S;Yeates SE;Peruffo D;Emerson BC;Gage MJ
• 通讯作者: Gage MJ