The eunuch phenomenon: adaptive evolution of genital emasculation in sexually dimorphic spiders

Abstract

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.

Disentangling the Size and Shape Components of Sexual Dimorphism

“…We scored araneoid spider shape dimorphism from the taxonomic literature as a simple presence/absence character (Table S2), and obtained SSD indices from recent SSD studies (Cheng and Kuntner 2014;Kuntner et al 2015). We followed a recent study of emasculation evolution (Kuntner et al 2015) in devising a genus level phylogeny from Dimitrov et al (Dimitrov et al 2012), but we modified the familial relationships according to the newest phylogenomic topology (Bond et al 2014).…”

The evolution of genital complexity and mating rates in sexually size dimorphic spiders

“…We define polygyny as male mating with more than one female, whereas monogynous males invest into repeated mating with the same female in an attempt to plug both of her copulatory openings. We based the inferred mating rates in nephilids and outgroups (Additional file 1: Table S1) on available experimental studies [13, 39–41, 48–73] and on genital damage data where single versus multiple male mating plugs per female copulatory opening predict monandry and polyandry, respectively [26, 35, 40, 41, 53]. Most Nephila species, and Phonognatha graeffei, are polyandrous [49, 61].…”

“…Relatively small nephilid males of certain species engage in extreme mating strategies, including severing terminal parts of their pedipalps (sperm transferring appendages), which are used to plug female copulatory openings [39, 40]. Experimental studies on selected species found that plugs from males with complex genitals commonly prevent female polyandry, whereas plugs from simple genitals do not [39, 41].…”

Natural breakage of the very long intromittent organ of the seed bug Lygaeus simulans (Heteroptera: Lygaeidae)

“…Alternatively, such breakages could be adaptive if they increase a male's reproductive success. For example, in many spider species a portion of the male copulatory organ frequently breaks off inside the female reproductive tract during mating, and can act as a mating plug, preventing subsequent males from being able to inseminate the female (Snow et al, 2006;Uhl et al, 2010;Kuntner et al, 2015). In some species essentially all matings result in breakage (Uhl et al, 2010).…”

“…In some species essentially all matings result in breakage (Uhl et al, 2010). Though breakage typically renders the copulatory organ nonfunctional, this strategy is likely favoured because males typically encounter few females and so have limited opportunities to mate (Uhl et al, 2010;Kuntner et al, 2015).…”