Joseph M. Long Marine Laboratory, University of California-Santa Cruz, Santa Cruz, CA 95060, USA.
Integr Comp Biol. 2013 Oct;53(4):671-88. doi: 10.1093/icb/ict088. Epub 2013 Aug 22.
As George Williams pointed out in 1975, although evolutionary explanations, based on selection acting on individuals, have been developed for the advantages of simultaneous hermaphroditism, sequential hermaphroditism and gonochorism, none of these evolutionary explanations adequately explains the current distribution of these sexual systems within the Metazoa (Williams' Paradox). As Williams further pointed out, the current distribution of sexual systems is explained largely by phylogeny. Since 1975, we have made a great deal of empirical and theoretical progress in understanding sexual systems. However, we still lack a theory that explains the current distribution of sexual systems in animals and we do not understand the evolutionary transitions between hermaphroditism and gonochorism. Empirical data, collected over the past 40 years, demonstrate that gender may have more phenotypic plasticity than was previously realized. We know that not only sequential hermaphrodites, but also simultaneous hermaphrodites have phenotypic plasticity that alters sex allocation in response to social and environmental conditions. A focus on phenotypic plasticity suggests that one sees a continuum in animals between genetically determined gonochorism on the one hand and simultaneous hermaphroditism on the other, with various types of sequential hermaphroditism and environmental sex determination as points along the spectrum. Here I suggest that perhaps the reason we have been unable to resolve Williams' Paradox is because the problem was not correctly framed. First, because, for example, simultaneous hermaphroditism provides reproductive assurance or dioecy ensures outcrossing does not mean that there are no other evolutionary paths that can provide adaptive responses to those selective pressures. Second, perhaps the question we need to ask is: What selective forces favor increased versus reduced phenotypic plasticity in gender expression? It is time to begin to look at the question of sexual system as one of understanding the timing and degree of phenotypic plasticity in gender expression in the life history in terms of selection acting on a continuum, rather than on a set of discrete sexual systems.
正如乔治·威廉姆斯（George Williams）在 1975 年指出的那样，尽管已经针对个体选择作用提出了用于解释雌雄同体、雌雄异体和两性异形生殖等优势的进化解释，但这些进化解释都无法充分解释后生动物门中这些性系统的当前分布情况（威廉姆斯悖论）。正如威廉姆斯进一步指出的那样，性系统的当前分布主要由系统发育决定。自 1975 年以来，我们在理解性系统方面取得了大量的经验和理论进展。然而，我们仍然缺乏一个能够解释动物性系统当前分布的理论，也不了解雌雄同体和雌雄异体之间的进化转变。过去 40 年来收集的经验数据表明，性别可能比以前认识到的具有更多的表型可塑性。我们知道，不仅是雌雄同体动物，而且是雌雄异体动物都具有表型可塑性，这种可塑性会根据社会和环境条件改变性别分配。对表型可塑性的关注表明，在动物中，一方面是由遗传决定的雌雄异体，另一方面是雌雄同体，各种类型的雌雄同体和环境性别决定作为这个连续体上的点。在这里，我认为，也许我们一直无法解决威廉姆斯悖论的原因是问题没有被正确地框定。首先，因为例如，雌雄同体提供生殖保障，或者雌雄异体确保异交并不意味着没有其他进化途径可以对这些选择压力提供适应性反应。其次，也许我们需要问的问题是：什么选择压力有利于增加还是减少性别表达的表型可塑性？现在是时候开始将性系统的问题视为理解生命史中性别表达的表型可塑性的时机和程度的问题，而不是作为一系列离散的性系统来考虑。
