Emasculation: gloves-off strategy enhances eunuch spider endurance

Abstract

Males of sexually cannibalistic spiders commonly mutilate parts of their paired genitals (palps) during copulation, which may result in complete emasculation or the ‘eunuch phenomenon’. In an orb-web nephilid spider, Nephilengys malabarensis , about 75 per cent of males fall victim to sexual cannibalism, and the surviving males become half-eunuchs (one palp emasculated) or full-eunuchs (both palps emasculated). While it has been shown that surviving eunuchs are better fighters compared with intact males when guarding the females with which they have mated, mechanisms behind eunuchs’ superior fighting abilities are unknown. The previously proposed ‘gloves-off’ hypothesis, attributing eunuchs’ enhanced locomotor endurance to the reduction in total body weight caused by genital mutilation, is plausible but has remained untested. Here, we tested the gloves-off hypothesis in N. malabarensis by comparing the time until exhaustion (i.e. endurance) of intact males with half- and full-eunuchs created experimentally. We found that by reducing body weight up to 4 per cent in half-eunuchs and 9 per cent in full-eunuchs through emasculation, endurance increases significantly in half-eunuchs (32%) and particularly strongly in full-eunuchs (80%). Our results corroborate the gloves-off hypothesis and further point towards the adaptive significance of male emasculation.

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

“…The logical prediction was that due to decreased overall mass after emasculation, palpless males would be more agile and show higher levels of physical endurance compared with intact ones. This prediction received strong support: half‐eunuchs and full eunuchs were 4 and 9% lighter than the intact males, respectively, and their corresponding endurance (time till exhaustion) increased by 32 and 80%, respectively (Lee et al , ). Similarly, in Tidarren sisyphoides , a single palp that is voluntarily amputated by the male represents a 10% mass loss, and his maximum speed correspondingly increased by 44%, his total endurance by 63%, and the total travelled length before exhaustion by a dramatic 300% (Ramos et al , ).…”

“…Therefore, those males that drop one or both palps may be able to achieve higher agility (Ramos et al, 2004;Kuntner et al, 2009a), and the edge in male-male contests. Thus, a proximate explanation for the better fighting abilities is the 'gloves-off' hypothesis (Kuntner et al, 2009c) predicting enhanced physical stamina in emasculated eunuchs (Ramos et al, 2004;Kralj-Fišer et al, 2011;Lee et al, 2012).…”

“…Traits securing paternity or maternity often appear to be self-sacrificial, such as selfless parental care defending offspring against predators (Svagelj, Trivellini & Quintana, 2012), the often risky male defence of females against competing males (Milner, Jennions & Backwell, 2010;Kralj-Fišer et al, 2011), and in some cases pure self-sacrifice such as a mother offering herself as food for her offspring (matriphagy) (Schneider, Salomon & Lubin, 2003), or a male offering himself as food for his mate (male complicity to sexual cannibalism) (Andrade, 1996). Emasculation, where males break off their genitals to become eunuchs (Lee et al, 2012) may be seen as an extreme case of organic sacrifice. From the male standpoint, rendering oneself incapable of future mating incurs obvious and immediate costs that must be offset by some positive trade-off.…”

“…1B) (Kralj-Fišer et al, 2011;Lee et al, 2012;Li et al, 2012). Emasculation in this review thus refers to effective inability to mate in those males without one or both palpal tarsi (Knoflach & van Harten, 2001;Knoflach, 2002;Lee et al, 2012), not to mere breakage/mutilation of the distal palpal sclerite, the embolus (Fromhage & Schneider, 2006;Snow, Abdel-Mesih & Andrade, 2006;. The latter, termed here 'lesser genital damage' (Fig.…”

Sexual Cannibalism as a Manifestation of Sexual Conflict

“…Males of Nephilengys malabarensis copulate by detaching the entire pedipalp, which will continue to transfer sperm into the female independently . Males without pedipalps are better fighters than males with pedipalps (Lee et al 2012), possibly because the pedipalps are somehow in the way or constitute an extra weight. Hence, although sexual cannibalism often co-occurs with a monogynous mating system, it is not tightly linked.…”