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Is the initiation of selfing linked to a hermaphrodite’s female or male reproductive function?
Behavioral Ecology and Sociobiology ( IF 2.3 ) Pub Date : 2020-03-17 , DOI: 10.1007/s00265-020-2816-3
Philipp Kaufmann 1, 2 , Lukas Schärer 1
Affiliation  

There is an ongoing debate about whether simultaneous hermaphrodites capable of selfing should prefer selfing over outcrossing or vice versa. While many theoretical models predict a transmission advantage for alleles that favour selfing, empirical studies often reveal low selfing rates. Despite these considerations, the underlying mechanisms that determine reproductive strategies in simultaneously hermaphroditic animals are poorly understood. In our study on the facultatively selfing free-living flatworm, Macrostomum hystrix, we ask whether the initiation of selfing, as inferred from the differential spatial distribution of received sperm, is linked to an individual’s female or male reproductive function. Specifically, the initiation of selfing could (i) be linked to the male function, when an individual is unable to donate sperm to others and hence donates sperm to self, or it could (ii) be linked to the female function, when an individual fails to receive sperm from others—and hence is unable to fertilize its eggs via outcrossing—thus inducing it to self-fertilize. We experimentally created a social environment that allowed focals to outcross via sperm donation, but simultaneously prevented them from receiving sperm—by pairing them with a partner lacking the male copulatory organ—so that fertilization of the focal’s eggs was restricted to selfing. Our results suggest that such focals generally do not initiate selfing, while we readily observe selfing in isolated worms. This suggests that in isolated M. hystrix, it is the male function that is linked to the initiation of selfing, likely due to a lack of opportunities for sperm donation. A variety of simultaneously hermaphroditic animals are capable of reproducing via both selfing and outcrossing. While the reproductive choices of such animals can be modelled by the joint action of genetic (e.g. inbreeding depression) and ecological factors (e.g. partner availability), experimental evaluation of theoretical results is often lacking. By manipulating the social environment of focal individuals, we here provide evidence that explores the respective role that the co-occurring male and female sex functions have on the initiation of selfing in a simultaneously hermaphroditic flatworm species. Specifically, our results suggest that the initiation of selfing is linked to the worm’s male function. Insights about which function is linked to the initiation of selfing may ultimately help to better understand reproductive decisions in simultaneous hermaphrodites.

中文翻译:

自交的开始是否与雌雄同体的雌性或雄性生殖功能有关?

关于能够自交的同时雌雄同体是否应该更喜欢自交而不是异交,或者反之亦然,一直存在争论。虽然许多理论模型预测了有利于自交的等位基因的传播优势,但实证研究往往揭示了低自交率。尽管有这些考虑,但对同时决定雌雄同体动物生殖策略的潜在机制知之甚少。在我们对兼性自交的自由生活扁虫 Macrostomum hystrix 的研究中,我们询问从接收的精子的不同空间分布推断自交的开始是否与个体的雌性或雄性生殖功能有关。具体来说,自交的开始可能(i)与男性功能有关,当一个人无法向他人捐赠精子并因此向自己捐赠精子时,或者它可能(ii)与女性功能有关,当一个人无法从他人那里接收精子时 - 因此无法通过异交使其卵子受精——从而诱导它自我受精。我们实验性地创造了一个社会环境,允许焦点通过精子捐赠进行异交,但同时阻止它们接收精子——通过将它们与缺乏雄性交配器官的伴侣配对——因此焦点卵子的受精仅限于自交。我们的研究结果表明,这些焦点通常不会引发自交,而我们很容易观察到孤立蠕虫的自交。这表明在孤立的 M. hystrix 中,雄性功能与自交的开始有关,可能是由于缺乏精子捐赠的机会。多种同时雌雄同体的动物能够通过自交和异交进行繁殖。虽然这些动物的生殖选择可以通过遗传(例如近亲繁殖衰退)和生态因素(例如伴侣可用性)的联合作用来模拟,但通常缺乏对理论结果的实验​​评估。通过操纵焦点个体的社会环境,我们在此提供证据来探索同时发生的男性和女性性功能对同时雌雄同体扁虫物种自交的开始所起的各自作用。具体来说,我们的研究结果表明,自交的开始与蠕虫的雄性功能有关。
更新日期:2020-03-17
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