German cockroach males maximize their inclusive fitness by avoiding mating with kin

International audienceKeywords: Blattella germanica German cockroach inbreeding avoidance kin selection male mate choice sex role Conventional sex roles imply choosy females and nondiscriminating males. However, growing evidence suggests that male choosiness is more common than expected. While male mate choice is clearly linked to high mating investment in sex role-reversed species, factors promoting male mate choice in conventional sex role species are still debated. We addressed this fundamental issue in the German cockroach, Blattella germanica (L.), a group-living species where members of both sexes exercise mutual mate choice to avoid inbreeding. We focused on (1) male potential reproductive rate, (2) male effective reproductive rate, and (3) male reproductive success in relation to female quality. Males tested in situations with unrestrained female availability were able to mate throughout their life, thus revealing a high potential reproductive rate. However, their effective reproductive rate was much more limited under ecologically realistic conditions with restrained female availability. In contradiction with general predictions of sex role theory, mate choice by B. germanica males occurs despite an apparent low mating investment and a male-biased operational sex ratio. The finding that inbred matings were less fertile than outbred matings reveals that kinship is the key factor promoting male choice in this particular case. In the light of inbreeding avoidance theory, we propose that by being choosy cockroach males avoid imposing inbreeding costs on their sisters, thus maximizing their own inclusive fitness via kin selection. A fundamental question raised by the study of sexual selection and mating systems addresses the respective roles of members of each sex in making mating decisions. The 'classical scenario' assumes that individuals of one sex are choosy while individuals of the opposite sex compete to gain access to mates. Conventional sex roles traditionally imply female mate choice and male competition. This dichotomy has been the paradigm for a long time because female investment in gamete production and parental care is higher than that of males in the great majority of species (Darwin 1874; Bateman 1948; Williams 1966; Trivers 1972; Andersson 1994). Such asymmetry in resource allocation between males and females leads to lower female potential reproductive 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 to females available for mating at a given time), which in turn lead males to compete for access to females, and allow females to choose among males (Emlen & Oring 1977; Clutton-Brock & Vincent 1991; Clutton-Brock & Parker 1992; Vincent et al. 1992; Parker & Simmons 1996). Some reports, although less frequent, also provide evidence for the occurrence of male mate choice and female competition. These cases of reversed sex roles are generally associated with high mating investments by males (e.g. costly ejaculates, paternal care) and female-biased operational sex ratios (e.g. Gwynne 1981; Gwynne & Simmons 1990; Berglund & Rosenqvist 2003). However, despite its elegant simplicity, this classical scenario does not encompass the breadth of complexity observed. A wealth of information shows that the true spectrum of sexual selection is much broader and that in many species both sexes can compete and be choosy at the same time (e