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The Evolution of Cooperative Breeding in the African Cichlid Fish, Neolamprologus Pulcher

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The Evolution of Cooperative Breeding in the African Cichlid Fish, Neolamprologus Pulcher Biol. Rev. (2011), 86, pp. 511–530. 511 doi: 10.1111/j.1469-185X.2010.00158.x The evolution of cooperative breeding in the African cichlid fish, Neolamprologus pulcher Marian Wong∗ and Sigal Balshine Department of Psychology, Neuroscience & Behaviour, McMaster University, Hamilton, Ontario, L8S 4L8, Canada (Received 14 December 2009; revised 5 August 2010; accepted 16 August 2010) 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 researchinfishesandothertaxonomicgroups. Key words: cooperative breeding, Neolamprologus pulcher, altruism, helping, alloparental care, kin selection, pay to stay, signals of prestige, group augmentation. CONTENTS I. Introduction ................................................................................................ 512 II. Study species ............................................................................................... 513 III. Do helpers really help? ..................................................................................... 515 (1) Immediate reproduction by helpers .................................................................... 515 (2) Benefits of helping to breeders ......................................................................... 516 IV. Is helping costly to helpers? ................................................................................. 517 V. Why do helpers help? ...................................................................................... 518 (1) Kin selection ........................................................................................... 518 (a) Theoretical background ............................................................................ 518 * Address for correspondence: (Tel: +1 905 921 3858; E-mail: [email protected] or [email protected]) Biological Reviews 86 (2011) 511–530 © 2010 The Authors. Biological Reviews © 2010 Cambridge Philosophical Society 512 Marian Wong and Sigal Balshine (b) Key predictions and tests ........................................................................... 518 (c) Summary ........................................................................................... 519 (2) Pay-to-stay ............................................................................................. 519 (a) Theoretical background ............................................................................ 519 (b) Key predictions and tests ........................................................................... 519 (c) Summary ........................................................................................... 521 (3) Signals of prestige ...................................................................................... 521 (a) Theoretical background ............................................................................ 521 (b) Key predictions and tests ........................................................................... 521 (c) Summary ........................................................................................... 522 (4) Group augmentation hypothesis ....................................................................... 522 (a) Theoretical background ............................................................................ 522 (b) Key predictions and tests ........................................................................... 522 (c) Group augmentation and the trait group selection perspective ..................................... 523 (d) Summary ........................................................................................... 523 VI. Future directions ........................................................................................... 524 (1) Long-term studies of marked individuals ............................................................... 524 (2) Distinguishing the fitness effects of helping from helper presence ...................................... 524 (3) Tests of the key predictions of the adaptive explanations for helping ................................... 524 (4) Assessing the relative contributions of the adaptive explanations for helping ........................... 524 (5) Variation in helping effort ............................................................................. 525 (6) Altruism versus mutualism? ............................................................................. 525 (7) New technologies ...................................................................................... 527 VII. Conclusions ................................................................................................ 527 VIII. Acknowledgements ......................................................................................... 528 IX. References .................................................................................................. 528 I. INTRODUCTION (Reeve & Keller, 2001; Magrath, Johnstone & Heinsohn, 2004; Hager & Jones, 2009). In cooperatively breeding species, subordinate individuals The third question of why non-breeders should help dom- typically forego their own reproductive efforts and help to inant breeders presents a significant evolutionary challenge. raise the offspring of dominant breeders. Understanding the This is because helping is costly to helpers owing to missed evolution of this behaviour has proven to be an enduring reproductive opportunities elsewhere (Brown, 1987) and the research challenge for evolutionary biologists (Hamilton, act of helping itself (Russell et al., 2003), while the recipients 1964a,b; Brown, 1987; Emlen, 1991; Russell, 2004; Clutton- of help benefit in the form of enhanced reproductive output Brock, 2002, 2009). Attempts to address the evolution (Emlen, 1991; Dickinson & Hatchwell, 2004; Russell, 2004). This problem of apparent altruism has inspired a number of helping usually break the problem down into three of theoretical ideas that explain the factors compensating for questions (Brown, 1987): (1) why do subordinates stay rather such costs and thus why such cooperative breeding could than disperse to breed independently elsewhere; (2) why have evolved and be maintained in many species (Hamilton, do subordinates forego breeding within the group; and 1964a,b; Gaston, 1978; Emlen & Wrege, 1989; Zahavi, 1995; (3) why do subordinates help rear the offspring of breeders? Pen & Weissing, 2000; Kokko, Johnstone & Clutton-Brock, The first question of why non-breeding subordinates should 2001; Kokko, Johnstone & Wright, 2002). Once again, the stay focuses on identifying the benefits and constraints that primary model species used to address these theoretical promote delayed dispersal and hence group formation. The developments have been birds, mammals and social insects majority of such investigations have been conducted on birds, (Solomon & French, 1997; Koenig & Dickinson, 2004; Cock- mammals and social insects, with much debate continuing burn, 1998; Bourke & Franks, 1995; Queller & Strassman, to surround the relative importance of life history versus 1998; Field & Foster, 1999). ecology, as well as the type of ecological factors promoting While the questions of why to delay dispersal, why to delayed dispersal in such taxa (Arnold & Owens, 1998; Field forego breeding and why to help have received relatively et al., 1998; Hatchwell & Komdeur, 2000; Cockburn, 2003; little attention
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