Males prefer virgin females, even if parasitized, in the terrestrial isopod Armadillidium vulgare

Abstract

In many species, males increase their reproductive success by choosing high‐quality females. In natural populations, they interact with both virgin and mated females, which can store sperm in their spermatheca. Therefore, males elaborate strategies to avoid sperm competition. In the terrestrial isopod Armadillidium vulgare, females can store sperm and produce several clutches. Moreover, this species can be parasitized by Wolbachia, which feminizes genetic males, transforming them into functional females. Our study compared attractiveness and mate choice when a male is exposed to both virgin and experienced females (i.e., females who have produced offspring and rested for 6 months), with or without Wolbachia. Our results revealed that males are more attracted to virgin females than experienced females, even if these virgin females are parasitized. Moreover, the chemical analysis highlighted different odors in females according to their reproductive and infection (Wolbachia‐free or vertically Wolbachia‐infected) status. Males attempted copulation more frequently and for longer with virgin females, even if Wolbachia‐infected, while experienced females refused further copulation. The evolutionary consequences of both male choice and female resistance on their fitness are discussed in this study.

The effect of the endosymbiont Wolbachia on the behavior of insect hosts

“…Recently, Schneider et al (2019) have shown that Wolbachiaknockdown D. paulistorum males express altered sexual pheromone profiles, with decrease between 9-and 23-fold in several male-specific compounds when compared to wild-type levels. This is in accord with the finding in A. vulgare, where females presented variations in the relative proportion of chemical compounds according to the presence or the absence of Wolbachia (Richard, 2017;Fortin et al, 2018). In many insects, sexual pheromones play an important role in recognition cues for mate choice between and within species.…”

“…This indicates that it is Wolbachia that are able to affect host mating behavior and thus can trigger pre-and post-mating isolation. Furthermore, Fortin et al (2018) showed that A. vulgare males spent more time near the Wolbachia-free females than the Wolbachia-infected females, when both females were virgin. This finding supported the result reported by Moreau et al (2001) that A. vulgare males performed more insemination events with uninfected females.…”

Ecology of female mating failure/lifelong virginity: a review of causal mechanisms in insects and arachnids

“…In particular, males exhibit near universal preference for virgin over mated females in insects and arachnids (Thomas, 2011;Kelly, 2018). In extreme cases, males may be deterred by mated females (Xu et al, 2014) or prefer parasitized virgins over old (otherwise healthy) mated females (Fortin et al, 2018). Preference of males for virgin females is beneficial as it minimizes sperm competition and enhances reproductive output as residual fecundity of virgin females is usually higher than that of previously mated females.…”

How do familiarity and relatedness influence mate choice in Armadillidium vulgare?

“…Male mate choice occurs in this species, as males can discriminate between females from short distances based on chemical cues associated with their molting status [24]. A recent study showed that the female reproductive experience is also a factor affecting choice by males in this species, with virgin females being preferred over females that have had a previous reproductive experience [27]. However, whether discrimination based on kin recognition occurs remains unknown.…”

“…vulgare females’ learning and memory capacities [37], survival [38], and attractiveness for mating [27, 39] and is probably linked to lower copulation investment [40]. Moreover, recent data indicate that males are able to discriminate Wolbachia- free females from Wolbachia- infected females from short distances and prefer the former type [27, 41]. Although infection can impact mate choice and the performance of infected individuals, little is known about its effect within the context of individual recognition used to assess kinship and familiarity.…”