Department of Evolution, Ecology and Behaviour, University of Liverpool, Crown Street, Liverpool, L69 7RB, U.K.
Division of Ecology & Evolution, Research School of Biology, The Australian National University, 46 Sullivans Creek Road, Canberra, ACT, 2600, Australia.
Biol Rev Camb Philos Soc. 2022 Aug;97(4):1365-1388. doi: 10.1111/brv.12846. Epub 2022 Feb 28.
In many animal species, males may exhibit one of several discrete, alternative ways of obtaining fertilisations, known as alternative reproductive tactics (ARTs). Males exhibiting ARTs typically differ in the extent to which they invest in traits that improve their mating success, or the extent to which they face sperm competition. This has led to the widespread prediction that males exhibiting ARTs associated with a high sperm competition risk, or lower investment into traits that improve their competitiveness before mating, should invest more heavily into traits that improve their competitiveness after mating, such as large ejaculates and high-quality sperm. However, despite many studies investigating this question since the 1990s, evidence for differences in sperm and ejaculate investment between male ARTs is mixed, and there has been no quantitative summary of this field. Following a systematic review of the literature, we performed a meta-analysis examining how testes size, sperm number and sperm traits differ between males exhibiting ARTs that face either a high or low sperm competition risk, or high or low investment in traits that increase mating success. We obtained data from 92 studies and 67 species from across the animal kingdom. Our analyses showed that male fish exhibiting ARTs facing a high sperm competition risk had significantly larger testes (after controlling for body size) than those exhibiting tactics facing a low sperm competition risk. However, this effect appears to be due to the inappropriate use of the gonadosomatic index as a body-size corrected measure of testes investment, which overestimates the difference in testes investment between male tactics in most cases. We found no significant difference in sperm number between males exhibiting different ARTs, regardless of whether sperm were measured from the male sperm stores or following ejaculation. We also found no significant difference in sperm traits between males exhibiting different ARTs, with the exception of sperm adenosine triphosphate (ATP) content in fish. Finally, the difference in post-mating investment between male ARTs was not influenced by the extent to which tactics were flexible, or by the frequency of sneakers in the population. Overall, our results suggest that, despite clear theoretical predictions, there is little evidence that male ARTs differ substantially in investment into sperm and ejaculates across species. The incongruence between theoretical and empirical results could be explained if (i) theoretical models fail to account for differences in overall resource levels between males exhibiting different ARTs or fundamental trade-offs between investment into different ejaculate and sperm traits, and (ii) studies often use sperm or ejaculate traits that do not reflect overall post-mating investment accurately or affect fertilisation success.
在许多动物物种中,雄性可能表现出几种不同的、可替代的获取受精的方式,这些方式被称为替代生殖策略(ARTs)。表现出 ART 的雄性通常在以下两个方面存在差异:一是在提高交配成功率的特征上投入的程度,二是在面临精子竞争时的投入程度。这导致了广泛的预测,即与高精子竞争风险相关的表现出 ART 的雄性,或者在交配前对提高竞争力的特征投入较低的雄性,应该在交配后投入更多的资源来提高竞争力,例如大的精液量和高质量的精子。然而,尽管自 20 世纪 90 年代以来,许多研究都在调查这个问题,但关于雄性 ART 之间在精子和精液投入上的差异的证据是混杂的,而且这个领域也没有定量的总结。在对文献进行系统回顾后,我们进行了一项荟萃分析,研究了在面临高或低精子竞争风险、或在提高交配成功率的特征上投入高或低的雄性 ART 之间,睾丸大小、精子数量和精子特征如何不同。我们从动物王国的 92 项研究和 67 个物种中获得了数据。我们的分析表明,面临高精子竞争风险的表现出 ART 的雄性鱼类的睾丸(在控制了身体大小后)明显大于面临低精子竞争风险的雄性鱼类。然而,这种影响似乎是由于性腺体指数被不恰当地用作睾丸投资的身体大小校正测量,这在大多数情况下高估了雄性策略之间睾丸投资的差异。我们发现,无论精子是从雄性精子库中测量还是射精后测量,表现出不同 ART 的雄性之间的精子数量没有显著差异。我们也没有发现表现出不同 ART 的雄性之间的精子特征有显著差异,除了鱼类精子中的三磷酸腺苷(ATP)含量。最后,雄性 ART 之间的交配后投资差异不受策略灵活性的程度或群体中 Sneaker 的频率的影响。总的来说,我们的研究结果表明,尽管有明确的理论预测,但在物种间雄性 ART 在精子和精液的投入上并没有明显的差异。理论和实证结果之间的不一致可能是由于(i)理论模型未能解释表现出不同 ART 的雄性之间总体资源水平的差异,或者投资于不同精液和精子特征之间的基本权衡,以及(ii)研究中经常使用的精子或精液特征不能准确反映整体交配后投资,或者影响受精成功。