Paternity of Subordinates Raises Cooperative Effort in Cichlids

Abstract

BackgroundIn cooperative breeders, subordinates generally help a dominant breeding pair to raise offspring. Parentage studies have shown that in several species subordinates can participate in reproduction. This suggests an important role of direct fitness benefits for cooperation, particularly where groups contain unrelated subordinates. In this situation parentage should influence levels of cooperation. Here we combine parentage analyses and detailed behavioural observations in the field to study whether in the highly social cichlid Neolamprologus pulcher subordinates participate in reproduction and if so, whether and how this affects their cooperative care, controlling for the effect of kinship.Methodology/Principal FindingsWe show that: (i) male subordinates gained paternity in 27.8% of all clutches and (ii) if they participated in reproduction, they sired on average 11.8% of young. Subordinate males sharing in reproduction showed more defence against experimentally presented egg predators compared to subordinates not participating in reproduction, and they tended to stay closer to the breeding shelter. No effects of relatedness between subordinates and dominants (to mid-parent, dominant female or dominant male) were detected on parentage and on helping behaviour.Conclusions/SignificanceThis is the first evidence in a cooperatively breeding fish species that the helping effort of male subordinates may depend on obtained paternity, which stresses the need to consider direct fitness benefits in evolutionary studies of helping behaviour.

Kinship reduces alloparental care in cooperative cichlids where helpers pay-to-stay

“…Therefore, the cooperative behaviour experimentally elicited in this study is of crucial importance for a test of the pay-to-stay hypothesis, as alloparental egg-care does not provide immediate fitness benefits to unrelated helpers, whereas it involves clear costs 36,37 . As this helping effort is hence altruistic, it can be selected for only if helpers receive other fitness benefits in return, which result from the tolerance in a safe territory that provides them with access to vital resources such as shelter and protection 19,29,48 , and opportunities to share in reproduction 49,50 .…”

“…cleaning and fanning) could not be measured and potential effects of subordinate reproduction were not considered, which can strongly affect subordinate helping effort 35,49 . Potential effects of relatedness on alloparental brood care have generally received much attention 4 .…”

“…Kin recognition has been demonstrated 55 and both related and unrelated subordinates participate in brood care of dominants' broods by cleaning and fanning the eggs 19 , in territory defence against predators, space competitors and conspecific intruders 19,29,53,54 , and in territory maintenance (for example, digging out shelters 47,53 ). The social conditions in this species seem to predispose it to the operation of some sort of trading help against resource access, such as assumed in evolutionary pay-to-stay models [26][27][28] : overall relatedness is low 16,42 and subordinates impose costs on the dominants by reducing the growth of the dominant female 40 and by occasional participation in reproduction 40,49 . Furthermore, predation risk is the major environmental factor constraining …”

The Right Tools for the Job: Cooperative Breeding Theory and an Evaluation of the Methodological Approaches to Understanding the Evolution and Maintenance of Sociality

“…For example, Nam et al (2010) examined the investment of helpers of the cooperatively breeding long-tailed tit, Aegithalos caudatus, using group history pedigrees and microsatellite genotypes from a 14 year field study to show that investment by helpers increased with relatedness. Likewise, Bruintjes et al (2011) found that subordinate cichlids, Neolamprologus pulcher, raised their levels of helping behavior when they had bred successfully and their offspring were present in the clutch. In another observational study, Canestrari et al (2005) found that among a cooperative breeding population of carrion crows, Corvus corone corone, genetic parents fed chicks at greater rates than helpers with no parentage.…”

Eco-evolutionary dynamics of social dilemmas

“…Additional members can dilute the risk of predation and/or actively take part in territory defence. Costs due to enhanced brood parasitism, cannibalism and growth reduction [90,91], however, reduce the benefit leading to active eviction of immigrants [92][93][94]. In addition, the cichlid example emphasizes an important ecological factor: variable risks.…”