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Animal Behaviour 77 (2009) 1375–1379

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Animal Behaviour 77 (2009) 1375–1379 Animal Behaviour 77 (2009) 1375–1379 Contents lists available at ScienceDirect Animal Behaviour journal homepage: www.elsevier.com/locate/yanbe Sex differences in survival costs of homosexual and heterosexual interactions: evidence from a fly and a beetle Alexei A. Maklakov*, Russell Bonduriansky Evolution & Ecology Research Centre and School of Biological, Earth and Environmental Sciences, University of New South Wales article info Studies on the costs of sexual reproduction have focused primarily on the costs of heterosexual courtship Article history: and mating, whereas the costs of homosexual interactions, such as male–male or female–female displays Received 18 October 2008 and mounting, have been relatively neglected. This may reflect an implicit assumption that heterosexual Initial acceptance 11 December 2008 interactions are more costly in most species, but this assumption has never been verified. We tested this Final acceptance 3 March 2009 assumption experimentally by comparing the effects of hetero- and homosexual interactions on life span Published online 7 May 2009 in two distantly related insects with contrasting mating systems: the seed beetle Callosobruchus mac- MS. number: 08-00672R ulatus, and the sexually dimorphic carrion fly Prochyliza xanthostoma. Despite pronounced behavioural and morphological differences between these species, results were remarkably congruent. Relative to Keywords: individually housed virgin controls, male life span was reduced to a similar degree in males maintained Callosobruchus maculatus with other males and males maintained with females. In contrast, female life span was strongly reduced cost of mating relative to controls when females were kept with males, but was affected very little when females were cost of reproduction courtship maintained with other females. Thus, the costs of homosexual and heterosexual interactions are similar Prochyliza xanthostoma for males, but highly dissimilar for females. Our results suggest that the costs of homosexual interactions sex differences can be considerable, and may have important consequences for the evolution of mating systems. Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. Costs of reproduction are a central tenet of life history theory ‘homosexual interactions’. The costs of homosexual interactions (Stearns 1992; Roff & Fairbairn 2007). Reproduction is costly have been estimated in very few species (especially in females), because it reduces future prospects of survival or reproduction. The despite the paramount importance of such costs for models that costs of reproduction to females result from mating and offspring aim to explain the evolution and maintenance of sexual behaviours. production and care. In contrast, male reproductive costs include The costs of homosexual interactions can be substantial. In material and energetic investment in gamete production, court- many species, males compete with rivals for access to females or ship, combat and scramble competition, and the costs of mating territories through scramble and/or combat interactions, often (Cordts & Partridge 1996; Kotiaho 2001; Martin & Hosken 2004). expending considerable time and energy, and incurring substantial Most research on the costs of sexual behaviours and interactions risk of injury (Thornhill & Alcock 1983; Andersson 1994; Kotiaho has traditionally focused on interactions with members of the 2001). In addition, males often court and mount other males, and opposite sex. However, in many species, males and females may the costs of courtship can be very high (Cordts & Partridge 1996). respond aggressively to same-sex individuals and, indeed, may Homosexual mounting has been reported for a wide variety of taxa, court and attempt to mount them (Aiken 1981; Serrano et al. 1991; including mammals, birds, reptiles and insects (Aiken 1981; Srivastava et al. 1991; Andersson 1994; Vasey 1995; Bagemihl 1999; Thornhill & Alcock 1983; Bagemihl 1999; Harari et al. 2000; Switzer Fang & Clemens 1999; Harari et al. 2000; Sommer & Vasey 2006; et al. 2004; Sommer & Vasey 2006). While homosexual interactions Vasey et al. 2008). Such interactions may function in intrasexual in mammals have received a lion’s share of research attention, competition, but can also result from perception errors (see below), homosexual mounting could be more prevalent in insects, where it and it may often be difficult to distinguish these causes in practice. sometimes amounts to half of all mating attempts observed (Aiken Thus, we refer to all interactions between same-sex individuals as 1981; Serrano et al. 2000). Although most research has focused on male homosexual interactions, females also show homosexual behaviours in many species (Srivastava et al. 1991; Vasey 1995; Fang & Clemens 1999; Harari et al. 2000; Sommer & Vasey 2006; * Correspondence: A. A. Maklakov, Evolution & Ecology Research Centre and Gastal et al. 2007). School of Biological, Earth and Environmental Sciences, University of New South Wales, Sydney, NSW 2052, Australia. Homosexual courtship (or courtship-like) behaviours, and E-mail address: [email protected] (A.A. Maklakov). homosexual mounting, may serve a variety of sexual functions, 0003-3472/$38.00 Ó 2009 The Association for the Study of Animal Behaviour. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.anbehav.2009.03.005 1376 A.A. Maklakov, R. Bonduriansky / Animal Behaviour 77 (2009) 1375–1379 such as allowing individuals to assert dominance over rivals, or Six experimental treatments were established: virgin males serving as practice for heterosexual encounters (Vasey 1995). alone, virgin females alone, virgin males in groups, virgin females However, such behaviours are often hypothesized to result from in groups, males in mixed-sex groups and females in mixed-sex perception error, or a complete lack of sex recognition (Parker groups. We collected 100 mated females and provided them with 1968; Aiken 1981; Thornhill & Alcock 1983; Serrano et al. 1991; 700 g of mung beans (approximately 8400 beans). This quantity of Harari et al. 2000; Switzer et al. 2004). Thus, a study of homosexual beans per beetle typically results in one egg laid per bean. We then mounting in the flour beetle Tribolium castaneum suggests that sex isolated 4500 infested beans and collected virgin beetles over 24 h recognition is absent in this species, and frequencies of intra- and periods. In all six treatments, beetles were kept in 60 mm petri intersexual mounting correspond to a random null model (Serrano dishes with 10 g of mung beans regardless of density or mating et al. 2000). In many other species, sex recognition occurs but status. Singly kept males and females were placed individually in 10 appears to be poor. In the water bug Palmacorixa nana, males blocks of 10 beetles each (N ¼ 100 per sex). Males and females in preferentially mount individuals that are larger than themselves, same-sex groups were placed in 10 groups of 20 beetles each. In probably because females are larger than males (Aiken 1981). Such each ‘grouped’ petri dish, 10 beetles were marked with white a mounting strategy unsurprisingly results in a very large nontoxic face paint. These marked beetles were considered percentage of errors (Aiken 1980). Several other studies also a ‘background’ against which the death of focal unmarked beetles support the perception error hypothesis (Savalli & Fox 1999; Harari was scored. As marked beetles died they were replaced from the et al. 2000; Serrano et al. 2000; Switzer et al. 2004; Van Gossum surplus of the original 4500 isolated beans. Thus at any time during et al. 2005). the experiment there were 10 marked beetles in each dish and only Thornhill & Alcock (1983) suggested that homosexual mounting the mortality of the unmarked focal ones (N ¼ 100 per sex) was in insects can evolve via selection on males, provided that benefits scored. ‘Mixed-sex groups’ for males and females were established of increased mating success through rapid but indiscriminate and maintained in the same manner, except that instead of marked mating attempts outweigh the costs of discrimination. Since only beetles of the same sex, we had marked beetles of the opposite sex males are likely to gain fitness benefits through increased number (marked females for the ‘male mixed-sex’ group and vice versa). of mountings, an explicit prediction from this hypothesis is that Ten dishes of 10 males and 10 females each were created for each of males will tolerate higher costs of homosexual mounting. Selection the two ‘mixed-sex’ treatments. Only male deaths were scored in is expected to act against the evolution of costly female–female the ‘male mixed-sex’ treatment (N ¼ 100) while dead females were interactions because females are less likely to benefit from such replaced from the stock. For the ‘female mixed-sex’ treatment this interactions (but see Harari et al. 2000). order was reversed. Deaths were scored twice a day for each We carried out two experimental studies aimed at comparing treatment. the cost of homosexual interactions relative to heterosexual inter- actions in two very different insects: the carrion fly Prochyliza Prochyliza xanthostoma xanthostoma and the seed beetle Callosobruchus maculatus. These species have markedly different mating systems. Callosobruchus Thirty gravid females of P. xanthostoma (Walker) were collected maculatus males mount but do not fight other males. Males chase from chunks of moose, Alces alces, carcasses at
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