Within-group male relatedness reduces harm to females in Drosophila

Abstract

Resolving the mechanisms that switch competition to cooperation is key to understand biological organization1. This is particularly relevant for intrasexual competition, which often leads to males harming females2. Recent theory proposes that kin selection may modulate female harm by relaxing competition among relatives3-5. We experimentally manipulated the relatedness of groups of male Drosophila melanogaster competing over females to demonstrate that, as expected, within group relatedness inhibits male competition and female harm. Females exposed to three brothers unrelated to the female had higher lifetime reproductive success and slower reproductive ageing compared to females exposed to triplets of males unrelated to each other. Triplets of brothers also fought less with each other, courted females less intensively and lived longer than triplets of unrelated males. However, associations among brothers may be vulnerable to invasion by minorities of unrelated males: when two brothers were matched with an unrelated male, the latter sired on average twice as many offspring as either brother. These results demonstrate that relatedness can profoundly affect fitness through its modulation of intrasexual competition, as flies plastically adjust sexual behaviour in a way consistent with kin selection theory.We first tested the effect of relatedness of males within a group on female fitness, by quantifying different aspects of fitness and life-history (experiment 1) in females exposed to male triplets. Males were unrelated to the female and either full-sib brothers of each other (AAA) or unrelated to each other (ABC), and were replaced weekly until female death. Consistent with expectations3-5, we found that females exposed to AAA-males had significantly higher lifetime reproductive success than females exposed to ABC-males (Fig. 1a). This was due to the fact that while total female lifespan did not differ on average between treatments (F 1, 119 = 1.66, P = 0.2), females exposed to AAA-males had significantly longer reproductive lifespan (from eclosion to last egg-laying day6, Fig. 1b), and female reproductive lifespan was positively correlated with female lifetime reproductive success (F 1, 117 = 484.59, P < 0.001). Two non-mutually exclusive mechanisms might cause this. First, high-fecundity females might die faster when exposed to ABC-males, leading to an average higher productivity of AAA-replicates ('selective death'). Second, individual Author contributions. Expt.1 was designed by P.C., S.W. and T.P., conducted by P.C. and F.A. and analysed by P.C. Expt. 2 was designed by P.C., C.K.W.T., S.W. and T.P., and conducted/analysed by P.C. Expt. 3 was designed and conducted by S.W. and P.C. and analysed by P.C. Expt. 4 was designed by C.K.W.T., T.P. and S.W., and conducted/analysed by C.K.W.T. The article was conceived and written by T.P. with input from P.C., C.K.W.T. and S.W. Europe PMC Funders Author Manuscripts females might suffer a steeper rate of age-dependent decline in reproductive output when exposed...

Male tolerance and male–male bonds in a multilevel primate society

“…Apparently, reduced competition between related males also reduced aggression against females who might be bearing the offspring of related males. Notably, reduced aggression also was observed in situations where not all males were related (36), indicating that the presence of related males may benefit both unrelated males and females across species as diverse as fruit flies and baboons.…”

“…Indirect fitness benefits also may play a role, however. A study of fruit flies (Drosophila melanogaster) showed that females which were kept with males that were related to each other experienced less aggression than females kept with unrelated males (36). Apparently, reduced competition between related males also reduced aggression against females who might be bearing the offspring of related males.…”

Are flies kind to kin? The role of intra- and inter-sexual relatedness in mediating reproductive conflict

“…In other words, males acted equally as antagonistically towards their sisters as they did towards unrelated females. In their study, Carazo et al [11] had suggested that males modulate aggression when housed with kin to reduce the magnitude of harm done to brothers and to shared mates, thereby increasing indirect fitness gains. However, our study, like that of Chippindale et al [31], reveals no such fitness benefit.…”

“…Hollis et al [29] argued that by failing to properly control for developmental and social familiarity between relatives, the results of Carazo et al [11] cannot be clearly interpreted as arising due to kin selection alone. Specifically, Hollis et al [29] argued that increased male-male aggression in the unrelated males treatment could be an artefact of the pre-trial developmental conditions.…”

“…In order to more fully understand the role of inter-and intra-sexual relatedness on reproductive behaviour and fitness, we conducted a series of experiments designed to replicate and elaborate upon the first Carazo et al [11] study. Using D. melanogaster, we examined variation in behaviour and fitness under a number of possible mating and social settings that differed in the potential for male-male competition, the degree of relatedness between males and the relatedness of male(s) to a target female.…”