Institute of Biology, Scientific Research Centre, Slovenian Academy of Sciences and Arts, Novi Trg 2, 1000, Ljubljana, Slovenia; Centre for Behavioural Ecology & Evolution, College of Life Sciences, Hubei University, 368 Youyi Road, 430062, Wuhan, China; National Museum of Natural History, Smithsonian Institution, PO Box 37012, Washington, DC, 20013-7012, U.S.A.
Biol Rev Camb Philos Soc. 2015 Feb;90(1):279-96. doi: 10.1111/brv.12109. Epub 2014 May 8.
Under natural and sexual selection traits often evolve that secure paternity or maternity through self-sacrifice to predators, rivals, offspring, or partners. Emasculation-males removing their genitals-is an unusual example of such behaviours. Known only in insects and spiders, the phenomenon's adaptiveness is difficult to explain, yet its repeated origins and association with sexual size dimorphism (SSD) and sexual cannibalism suggest an adaptive significance. In spiders, emasculation of paired male sperm-transferring organs - secondary genitals - (hereafter, palps), results in 'eunuchs'. This behaviour has been hypothesized to be adaptive because (i) males plug female genitals with their severed palps (plugging hypothesis), (ii) males remove their palps to become better fighters in male-male contests (better-fighter hypothesis), perhaps reaching higher agility due to reduced total body mass (gloves-off hypothesis), and (iii) males achieve prolonged sperm transfer through severed genitals (remote-copulation hypothesis). Prior research has provided evidence in support of these hypotheses in some orb-weaving spiders but these explanations are far from general. Seeking broad macroevolutionary patterns of spider emasculation, we review the known occurrences, weigh the evidence in support of the hypotheses in each known case, and redefine more precisely the particular cases of emasculation depending on its timing in relation to maturation and mating: 'pre-maturation', 'mating', and 'post-mating'. We use a genus-level spider phylogeny to explore emasculation evolution and to investigate potential evolutionary linkage between emasculation, SSD, lesser genital damage (embolic breakage), and sexual cannibalism (females consuming their mates). We find a complex pattern of spider emasculation evolution, all cases confined to Araneoidea: emasculation evolved at least five and up to 11 times, was lost at least four times, and became further modified at least once. We also find emasculation, as well as lesser genital damage and sexual cannibalism, to be significantly associated with SSD. These behavioural and morphological traits thus likely co-evolve in spiders. Emasculation can be seen as an extreme form of genital mutilation, or even a terminal investment strategy linked to the evolution of monogyny. However, as different emasculation cases in araneoid spiders are neither homologous nor biologically identical, and may or may not serve as paternity protection, the direct link to monogyny is not clear cut. Understanding better the phylogenetic patterns of emasculation and its constituent morphologies and behaviours, a clearer picture of the intricate interplay of natural and sexual selection may arise. With the here improved evolutionary resolution of spider eunuch behaviour, we can more specifically tie the evidence from adaptive hypotheses to independent cases, and propose promising avenues for further research of spider eunuchs, and of the evolution of monogyny.
在自然选择和性选择下，生物通常会进化出一些特征，通过自我牺牲来保护自身或后代免受捕食者、竞争对手、后代或配偶的侵害。去势——雄性动物切除自己的生殖器官——就是这种行为的一个不寻常例子。这种现象仅在昆虫和蜘蛛中被发现，其适应性很难解释，但它的反复出现以及与性二态性（SSD）和性食同类（sexual cannibalism）的关联表明了其具有适应性意义。在蜘蛛中，雄性的用于传输精子的成对器官——第二性器官——（以下简称触肢）被切除，导致“太监”现象。这种行为被假设是适应性的，因为（i）雄性用切断的触肢堵塞雌性生殖器（堵塞假说），（ii）雄性切除触肢以在雄性之间的竞争中成为更好的斗士，由于总体重减轻，可能会变得更加敏捷（脱手套假说），以及（iii）雄性通过切断的生殖器实现更长时间的精子转移（远程交配假说）。之前的研究在一些圆网蜘蛛中为这些假设提供了证据，但这些解释远非普遍适用。为了寻找蜘蛛去势的广泛宏观进化模式，我们回顾了已知的发生情况，权衡了每个已知案例中支持这些假设的证据，并根据其与成熟和交配的关系，更精确地定义了去势的具体情况：“成熟前”、“交配时”和“交配后”。我们使用蜘蛛属水平的系统发育树来探索去势的进化，并调查去势、SSD、生殖器损伤较小（栓塞破裂）和性食同类（雌性吃掉雄性）之间潜在的进化联系。我们发现了一个复杂的蜘蛛去势进化模式，所有案例都局限于 Araneoidea：去势至少进化了五次，最多进化了十一次，至少失去了四次，并且至少又进化了一次。我们还发现，去势以及生殖器损伤较小和性食同类与 SSD 显著相关。因此，这些行为和形态特征很可能在蜘蛛中共同进化。去势可以被视为生殖器畸形的一种极端形式，甚至是与单配制进化相关的终极投资策略。然而，由于不同的蜘蛛去势案例既不是同源的，也不是生物学上相同的，并且可能也不一定能起到保护父权的作用，因此与单配制的直接联系并不明确。更好地了解去势的系统发育模式及其组成形态和行为，可能会更清楚地了解自然选择和性选择之间错综复杂的相互作用。随着蜘蛛太监行为的进化分辨率的提高，我们可以更具体地将适应性假说的证据与独立案例联系起来，并为进一步研究蜘蛛太监以及单配制的进化提出有希望的途径。
