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Mating failure shapes the patterns of sperm precedence in an insect
Behavioral Ecology and Sociobiology ( IF 1.9 ) Pub Date : 2020-01-27 , DOI: 10.1007/s00265-020-2801-x
Vicki L. Balfour , Daniella Black , David M. Shuker

Abstract Estimates of last male sperm precedence ( P 2 ) are often used to infer mechanisms of sperm competition, a form of post-copulatory sexual selection. However, high levels of mating failure (i.e. copulations resulting in no offspring) in a population can lead to misinterpretations of sperm competition mechanisms. Through simulations, García-González ( 2004 ) illustrated how mating failure could cause bimodal distributions of paternity with peaks at P 2 = 0 and 1, under a random sperm mixing mechanism. Here, we demonstrate this effect empirically with the seed bug Lygaeus simulans , a species known to exhibit high levels of mating failure (40–60%), using a morphological marker to estimate paternity. Contrary to previous findings in a sister species, we did not find strong evidence for last male sperm precedence. There was a tendency towards last male precedence ( P 2 = 0.58) but within the expected range for random sperm mixing. Instead, P 2 was highly variable, with a bimodal distribution, as predicted by García-González ( 2004 ). After taking mating failure into account, the strongest driver of paternity outcome was copulation duration. Furthermore, we found evidence that mating failure could partly be a female-associated trait. Some doubly-mated females were more likely to produce no offspring or produce offspring from two different sires than expected by chance. Therefore, some females are more prone to experience mating failure than others, a result that mirrors an earlier result in male L. simulans . Our results confirm that mating failure needs to be considered when interrogating mechanisms of post-copulatory sexual selection. Significance statement Mating failure arises when animals fail to produce offspring across their lifetime. This may be due to a failure to find a mate or a failure to produce offspring after one or more apparently successful matings. Sperm competition is when ejaculates of rival males compete to fertilize a female’s eggs. Estimates of second male paternity ( P 2 ) are often used to infer mechanisms of sperm competition (i.e. which male “wins” and how). However, García-González ( 2004 ) suggested that high levels of mating failure can skew paternity (i.e. give spuriously high/low levels of P 2 ) and lead to misinterpretations of these mechanisms. We carried out sperm competition experiments on Lygaeus simulans seed bugs using a morphological marker to estimate paternity. We show empirically that mating failure does skew patterns of paternity, causing a bimodal distribution of P 2 . Therefore, by disrupting patterns of sperm competition, mating failure influences both the action of post-copulatory sexual selection and also our understanding of the mechanisms of sperm competition.

中文翻译:

交配失败塑造了昆虫精子优先的模式

摘要 对最后一个男性精子优先级 (P 2 ) 的估计通常用于推断精子竞争的机制,这是一种交配后的性选择形式。然而,群体中大量的交配失败(即交配导致没有后代)会导致对精子竞争机制的误解。通过模拟,García-González (2004) 说明了在随机精子混合机制下,交配失败如何导致在 P 2 = 0 和 1 处出现峰值的双峰分布。在这里,我们用种子虫 Lygaeus simulans 凭经验证明了这种效果,这是一种已知表现出高水平交配失败(40-60%)的物种,使用形态学标记来估计亲子关系。与之前在姊妹物种中的发现相反,我们没有找到最后雄性精子优先的有力证据。有最后男性优先的趋势(P 2 = 0.58),但在随机精子混合的预期范围内。相反,正如 García-González (2004) 所预测的,P 2 是高度可变的,具有双峰分布。考虑到交配失败后,亲子关系结果的最强驱动因素是交配持续时间。此外,我们发现有证据表明交配失败可能部分是与女性相关的特征。一些双交雌性更有可能不产生后代或产生来自两个不同公牛的后代,而不是偶然的。因此,一些雌性比其他雌性更容易出现交配失败,这一结果反映了雄性 L. simulans 的早期结果。我们的结果证实,在询问交配后性选择的机制时,需要考虑交配失败。意义说明 当动物一生都无法生育后代时,就会出现交配失败。这可能是由于在一次或多次明显成功的交配后未能找到配偶或未能产生后代。精子竞争是指雄性雄性的射精竞争使雌性的卵子受精。对第二个男性亲子关系 (P2) 的估计通常用于推断精子竞争的机制(即哪个男性“获胜”以及如何“获胜”)。然而,García-González (2004) 认为,高水平的交配失败会扭曲亲子关系(即给出虚假的高/低水平的 P 2 )并导致对这些机制的误解。我们使用形态标记来估计亲子关系,对类似 Lygaeus simulans 种子臭虫进行了精子竞争实验。我们凭经验表明,交配失败确实会扭曲父系模式,导致 P 2 的双峰分布。因此,通过破坏精子竞争的模式,交配失败会影响交配后性选择的作用以及我们对精子竞争机制的理解。
更新日期:2020-01-27
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