The evolution of cooperative breeding in the African cichlid fish, Neolamprologus pulcher

Abstract

The conundrum of why subordinate individuals assist dominants at the expense of their own direct reproduction has received much theoretical and empirical attention over the last 50 years. During this time, birds and mammals have taken centre stage as model vertebrate systems for exploring why helpers help. However, fish have great potential for enhancing our understanding of the generality and adaptiveness of helping behaviour because of the ease with which they can be experimentally manipulated under controlled laboratory and field conditions. In particular, the freshwater African cichlid, Neolamprologus pulcher, has emerged as a promising model species for investigating the evolution of cooperative breeding, with 64 papers published on this species over the past 27 years. Here we clarify current knowledge pertaining to the costs and benefits of helping in N. pulcher by critically assessing the existing empirical evidence. We then provide a comprehensive examination of the evidence pertaining to four key hypotheses for why helpers might help: (1) kin selection; (2) pay-to-stay; (3) signals of prestige; and (4) group augmentation. For each hypothesis, we outline the underlying theory, address the appropriateness of N. pulcher as a model species and describe the key predictions and associated empirical tests. For N. pulcher, we demonstrate that the kin selection and group augmentation hypotheses have received partial support. One of the key predictions of the pay-to-stay hypothesis has failed to receive any support despite numerous laboratory and field studies; thus as it stands, the evidence for this hypothesis is weak. There have been no empirical investigations addressing the key predictions of the signals of prestige hypothesis. By outlining the key predictions of the various hypotheses, and highlighting how many of these remain to be tested explicitly, our review can be regarded as a roadmap in which potential paths for future empirical research into the evolution of cooperative breeding are proposed. Overall, we clarify what is currently known about cooperative breeding in N. pulcher, address discrepancies among studies, caution against incorrect inferences that have been drawn over the years and suggest promising avenues for future research in fishes and other taxonomic groups.

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

“…Large helpers of this species are often unrelated to the dominant breeders 16,42 , which calls for mechanisms other than kin-selection to explain the cooperative effort of subordinates. Individuals prevented from helping by removal were attacked by other helpers upon their return, which might suggest punishment 43 but could also reflect competition for dominance 39 . Helpers prevented from helping to defend the territory against intruders subsequently showed increased levels of cooperative defence, but experienced unchanged aggression levels 44 .…”

“…Some of this previously reported evidence for pay-to-stay might alternatively be explained by direct fitness benefits to helpers without involving coercion by dominants, because territory defence and maintenance might generate immediate shared benefits 17,39 . 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 .…”

“…Other helping behaviours such as predator defence and territory maintenance might also serve immediate direct fitness benefits to subordinates (that is, being 'selfish' 38,39 ), which is not the case with alloparental care. Alternatively or in addition to the operation of a pay-to-stay mechanism, alloparental care could yield direct fitness benefits to helpers by group augmentation.…”

Castration affects reproductive but not aggressive behavior in a cichlid fish

“…cooperative breeding in Neolamprologus pulcher, Desjardins et al, 2007;Fitzpatrick, 2005;Taves et al, 2009;Wong and Balshine, 2011) that allows for comparative studies (e.g. phylogenetic test of the challenge hypothesis in African cichlids with divergent mating systems, Hirschenhauser et al, 2004).…”

First- and second-order sociality determine survival and reproduction in cooperative cichlids

“…Upon capture, we recorded each fish's sex and size (SL to the nearest mm), took a small fin-clip for DNA extraction and marked the fish with an individual subcutaneous elastomer tag (visible implant elastomer; Northwest Marine Technologies). Each individual was classified as dominant male (DM; n ¼ 52), dominant female (DF; n ¼ 94), male helper (subordinate males greater than 1.5 cm SL; SM; n ¼ 59), or female helper (subordinate female greater than 1.5 cm SL; SF; n ¼ 58) [41]. Afterwards, fish were released into their respective home territory, and their continued group membership was checked 24 h later.…”