Sex Ratio Bias Leads to the Evolution of Sex Role Reversal in Honey Locust Beetles

Abstract

The reversal of conventional sex roles was enigmatic to Darwin, who suggested that it may evolve when sex ratios are female biased [1]. Here we present direct evidence confirming Darwin's hypothesis. We investigated mating system evolution in a sex-role-reversed beetle (Megabruchidius dorsalis) using experimental evolution under manipulated sex ratios and food regimes. In female-biased populations, where reproductive competition among females was intensified, females evolved to be more attractive and the sex roles became more reversed. Interestingly, female-specific mating behavior evolved more rapidly than male-specific mating behavior. We show that sexual selection due to reproductive competition can be strong in females and can target much the same traits as in males of species with conventional mating systems. Our study highlights two central points: the role of ecology in directing sexual selection and the role that females play in mating system evolution. DOI: https://doi.org/10. 1016/j.cub.2016.07.018 Posted at the Zurich Open Repository and Archive, University of Zurich ZORA URL: https://doi.org/10.5167/uzh-134324 Journal Article Accepted Version Originally published at: Fritzsche, Karoline; Booksmythe, Isobel; Arnqvist, Göran (2016). Sex ratio bias leads to the evolution of sex role reversal in honey locust beetles. Current Biology, 26 (18) suggested that it may evolve when sex ratios are female--biased [1]. We present the 24 first direct evidence confirming Darwin's hypothesis. We investigated mating 25 system evolution in a sex--role reversed beetle (Megabruchidius dorsalis) using 26 experimental evolution under manipulated sex ratios and food regimes. In female--27 biased populations, where reproductive competition among females was intensified, 28 females evolved to be more attractive and the sex--roles became more reversed. 29Interestingly, female--specific mating behaviour evolved more rapidly than male--30 specific mating behaviour. We show that sexual selection due to reproductive 31 competition can be strong in females and can target much the same traits as in 32 males of species with conventional mating systems. This highlights the central role 33 that females play in mating system evolution. In the honey locust beetle (Megabruchidius dorsalis), sex--roles in courtship are 54 reversed compared to other seed beetles: females search for males, actively initiate 55 mating and court males vigorously, whereas males often reject female mating 56 attempts [11--13]. Male ejaculates provide females with essential nutrients that 57 increase females' fecundity and longevity [14], and females that secure more 58 4 matings live longer and produce more offspring [8, 11, 15]. In contrast, matings 59 carry substantial direct costs to males [13, 14] and males prefer to mate with 60 females that perform more vigorous courtship displays [11, 13]. 62We allowed replicated honey locust beetle populations to evolve for 19 generations 63 under two adult sex ratios (female--biased, 1:5, or male--biased, ...

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

“…In many instances, low female mating probability on a given day coincides with rarity of males (Calabrese & Fagan, ; Franco et al., ; Calabrese et al., ; Rhainds, ; Fauvergue, ; Faust & Forrest, ; Sciarretta et al., ). These studies support widely held views of female‐biased sex ratios and/or acute shortage of males (‘male vacuum’) as triggers of FMF (Wing, ; Mendel et al., ; Fritzsche et al., ). As expected, the level of female choosiness declines as the sex ratio becomes female biased (Monier et al., ).…”

“…Conversely, aging virgins increase investment in mating activities (signaling or foraging) to counterbalance the ever-increasing risk of lifelong virginity (Lehtonen et al, 2012;de Cock et al, 2014;Simmons, 2015;Umbers et al, 2015). Other adaptations to mitigate FMF include selection of microhabitats most suitable for mate attraction (Rhainds, 2010(Rhainds, , 2015, plasticity in sex role reversal (virgin females becoming the active partner when perceived abundance of males is low) (Lewis & Wang, 1991;Wing, 1991;Gwynne & Lorch, 2013;Westermann et al, 2014;Fritzsche et al, 2016), and agonistic interactions between virgin females for access to males (Rillich et al, 2009;Papadopoulos et al, 2009).…”

Adult sex ratios and reproductive strategies: a critical re-examination of sex differences in human and animal societies

“…Thus, when males are in abundance and surrounded by competitors, they should reduce mating effort [37]. The ASR has since been shown to influence the coevolution of patterns of care and competition through varying sex-specific intensities of sexual selection both across and within species [8,14,[38][39][40]. These findings are in-line with mating market theory from the social sciences that also takes a frequencydependent approach to behaviour [41,42].…”

Mate searching inEnnya maculicornis(Membracidae: Polyglyptini) initiated by females: behavioural and acoustic descriptions

“…The examples in which females initiate mate searching have been related to the energy that she invests in offspring (Magrath & Komdeur, 2003;Campbella et al, 2009), a bias in sex ratio Correspondence: Carlos F. Pinto, Laboratorio de Química Ecológica, Departamento de Ciencias Ecológicas, Facultad de Ciencias, Universidad de Chile, Casilla 653, Santiago, Chile. E-mail: cpintonavia@gmail.com (Liker et al, 2013;Fritzsche et al, 2016) and the occurrence of polyandry or polygyny (Clutton-Brock, 2007). In some instances, information may be exchanged during courtship that takes the form of duets of signals (e.g.…”