Female quality variance explains male selectivity in a non-sex role reversal species

Mathieu Lihoreau & Colette Rivault

UMR 6552, Éthologie Animale et Humaine, CNRS, Université de Rennes 1, Campus Beaulieu, 263 Avenue du Général Leclerc, 35042 Rennes, France

Article soumis à Proceedings of the Royal Society of London B. (soumis le 10/01/2008).

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ABSTRACT

Conventional sex roles imply choosy caring females and indiscriminating competing males. However, growing experimental data as well as theoretical models suggest that male choosiness is more common than expected. While male mate selectivity is clearly linked to high mating investment in sex-role reversal species, with choosy caring males and indiscriminating competing females, the key factors involved in the evolution of male selectivity in non-sex-role reversal species when males invest little in reproduction, are still debated. Here, we investigated factors associated with male selectivity in a non-sex-role reversal species, the cockroach Blattella germanica L., where both sexes exert mutual mate choice to avoid inbreeding. We focused on i) potential reproduction rates of males without constraints due to female availability and inter-male competition; ii) effective reproduction rates of males with these constraints; and iii) female quality variance in relation to their relatedness to males. We demonstrated that males fertilize females successfully during their entire adult life, suggesting a high potential rate of reproduction with low mating investment. However, under constraining conditions due to female availability and inter-male competition, males are restricted to one mating at the most. In accordance with theoretical predictions, our results suggest that the large spectrum of female quality variance due to genetic relatedness is a major cause for the evolution of male selectivity in this non-sex-role reversal species.

Keywords: Blattella germanica; male mate selectivity; inbreeding avoidance; reproduction rate.

INTRODUCTION

Sexual selection arises from differential reproductive success based on intra-sexual competition and mate choice (Andersson 1994). A fundamental question raised by the evolution of mating systems addresses the respective roles of members of each sex while making mating decisions (Kokko & Johnstone 2002). The “classical scenario” concerns species in which one sex is choosy and the other sex invests in competition to gain access to mates. For a long time, female selectivity and male competition have been the paradigm (i.e. conventional sex role), because female investment in gamete production and in parental care is higher than that of males (Darwin 1874; Bateman 1948; Williams 1966; Trivers 1972). This asymmetry in resource allocation between sexes induces lower female potential reproduction rates (i.e. maximum rate of reproduction when not constrained by mate availability) and a male-biased operational sex ratio (i.e. the ratio of males versus females available for mating at a given time) that in turn lead males to compete for access to females (Emlen & Oring 1977;

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Clutton-Brock & Vincent 1991; Clutton-Brock & Parker 1992; Vincent et al. 1992; Parker & Simmons 1996). On the other hand, some reports, although less frequent, highlight the occurrence of reversed sex roles when males are choosy and females compete, in association with high mating investment by males (e.g. costly ejaculates, paternal care) and female-biased operational sex ratios (e.g. Gwynne 1981, 1990; Gwynne & Simmons 1990).

Despite its elegant simplicity, this classical scenario has not stood up well to the challenge of biological complexity. In fact, a wealth of information shows that the true spectrum of sexual selection is much broader and reveals that in many species both sexes compete and are choosy (Cunningham & Birkhead 1998; Kokko & Jennions 2008). These ideas have been elaborated within the complex theoretical framework of mutual mate choice (Parker 1983; Owens & Thompson 1994; Deutsch & Reynolds 1995; Johnstone et al. 1996; Johnstone 1997; Kokko and Monaghan 2001; Kokko & Johnstone 2002; Servedio & Lande 2006) highlighting that at least three parameters must be taken into account to predict the evolution of selectivity: i) mating investment (e.g. parental care); ii) constraints on finding mates and assessing their quality (e.g. operational sex ratio); and iii) variance of quality of potential mates (e.g. mate fecundity). In particular, one of the novelties of these models is that they highlight the importance of mate quality variance and lower the role of biased operational sex ratios in the evolution of selectivity.

Although experimental reports of mutual mate choice are still relatively scarce (Jones & Hunter 1993; Ryan & Altmann 2001; Gowaty et al. 2002; Chenoweth & Blows 2003; Drickamer et al. 2003; Anderson et al. 2007), they provide insightful data to test and validate predictions of sex role theory (Kokko et al. 2006; Kokko & Jennions 2008). Whereas research on the evolution of male selectivity focuses on the small minority of species presenting sex-role reversal, little is known about non-sex-sex-role-reversal species (i.e. conventional sex-sex-role species). In fact, a wealth of information suggests that male selectivity in these species arises in systems where males contribute little more than sperm production to reproduction (Bonduriansky 2001). Male choosiness should then be primarily linked to a large variance in female fecundity, and consequently male mating investment and male-biased operational sex-ratio become less important.

Our aim here was to investigate factors associated with male selectivity in a non-sex-role reversal species when both sexes exert mutual mate choice. We focused on the three key parameters generally taken into account by theoretical models to predict the evolution of mate selectivity: i) male mating investment; ii) constraints on males' mating opportunities; and iii) variance of female quality. The group-living cockroach Blattella germanica (L.) offers

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be selective when choosing a mate (Lihoreau et al. 2008). In this species, individuals live in aggregates with an equilibrated adult sex-ratio (Ross & Mullins 1995). Because of their low dispersion rates (Rivault 1990), group members share high levels of relatedness and members of both sexes exhibit precopulatory mate choice to avoid inbred matings (Lihoreau et al. 2007; Lihoreau & Rivault 2009). Males court preferentially non-sibling females who in turn, choose the most vigorously courting males (Lihoreau et al. 2008). While female mate choice may primarily rely on their high investment in embryonic parental care (bearing oothecae until nymphs hatch) (Roth & Willis 1955; Mullins & Keil 2002), males never provide parental care (Rust et al. 1995). Therefore, the question of why males are selective still remains.

In fact, little information is available about the total mating investment of males, their potential reproduction rates and fitness benefits linked to inbreeding avoidance. Here, we investigated these parameters to understand the causalities of selectivity of B. germanica males. First, we evaluated male mating investment by estimating their potential reproduction rates in a situation without constraints on female availability and without inter-male competition. Then, we estimated the effective reproduction rates of males by testing them in groups with an equilibrated sex-ratio. Finally, we evaluated fitness benefits associated with female quality variance by comparing fecundity of females in inbred matings to that of females in outbred matings.