The Evolution of Cooperative Breeding in Vertebrates

Abstract

Cooperative breeding – in which some sexually mature individuals forgo independent breeding, join a group as subordinate and help to raise the offspring of others – occurs in at least 3% (mammals) and 9% (birds) of vertebrates. Because helping others is costly, this behaviour contradicts the concept of ‘selfish’ natural selection. The intriguing evolutionary paradox of such seemingly altruistic behaviour has, therefore, been the focus of much study aiming to unravelling the evolutionary drivers underlying cooperative breeding. The benefits of group living, costs of dispersal and constraints of limited available independent breeding positions may persuade individuals to delay independent breeding and remain as subordinates within a group. However, it is the range of subsequent benefits (indirect benefits – such as improving reproduction and survival of related individuals or direct benefits – such as gaining breeding experience, benefits of future cooperation with raised recruits or gaining a share in reproduction) that favour the evolution of helping.

Key Concepts

  • The evolution of cooperative breeding is best understood by considering the benefits for helpers obtained from delayed dispersal and from helping, and the benefits helpers impose on breeders.
  • Subordinate individuals are expected to stay when there are constraints on independent breeding and/or when they obtain benefits in their resident territory.
  • Subordinates individuals can help related individuals and gain indirect (kin selected) fitness benefits, but in many species, helpers can also be unrelated; direct benefits of helping (like parentage, being allowed to stay) may thus be more important than commonly assumed.
  • Breeders can benefit from helpers, either because these improve their reproductive success or because breeders can reduce their own investment in the offspring.
  • The surplus of reproductive capable individuals and the effects of helpers on survival and reproduction can have important implications for population dynamics in cooperatively breeding species.

Keywords: cooperative breeding; helping behaviour; direct fitness benefits; indirect fitness benefits; costs of helping; group stability; population dynamics; relatedness

Figure 1. Four species used in long‐term studies investigating the evolution of cooperative breeding in vertebrates: (a) Lake Tanganyika cichlid (Neolamprologus pulcher). A breeding group defending their territory against a predatory fish. Reproduced with permission from M. Taborsky; (b) superb fairy‐wren (Malurus cyaneus). A dominant male. Reproduced with permission from A. Russell; (c) meerkat (Suricata suricatta). Subordinates help babysit the dominant pairs' offspring. Reproduced with permission from A.J. Young; (d) naked mole rat (Heterocephalus glaber), living in groups that may contain up to hundreds of helpers. Reproduced with permission from Lorna Ellen Faulkes.
Figure 2. Examples of the percentage of group offspring that is sired by male and female subordinates in populations of cooperatively breeding vertebrates. Most of these offspring are sired by a subordinate within the group, but sometimes subordinates, usually males, gain parentage outside the own group. Although in some species, subordinates refrain (almost) completely from direct reproduction, in other species, they produce nearly as many offspring as the dominants in the group [e.g. pukeko (Porphyrio porphyrioi melanotus)]. Furthermore, in some species, subordinates of one sex produce a considerably larger part of group offspring than the other sex (note that in some species,e.g. superb fairy‐wrens and write‐browed scrubwrens, no values were given for females because subordinates in these species are exclusively males). In all cases, parentage was assigned using molecular analyses. The extent to which reproduction is divided between same‐sex individuals within each group is termed ‘reproductive skew’ and the ecological drivers of this variation have been subject to extensive study (not addressed here, but see Trubenová and Hager, for an extensive review). Species and sources: A, dwarf mongoose (Helogale parvula, Keane et al., ); B, wild dog (Lycaon pictus, Girman et al., ); C, meerkat (Suricata suricatta, Griffin et al., ); D, Lake Tanganyika cichlid (Neolamprologus pulcher, Dierkes et al., ); E, Lake Tanganyika cichlid (Julidochromis ornatus, Awata et al., ); F, Seychelles warbler (Acrocephalus sechellensis, Richardson et al., ); G, moorhen (Gallinula chloropus, McRae, ); H, Florida scrub‐jay (Aphelocoma coerulescens, Quinn et al., ); I, white‐browed scrubwren (Sericornis frontalis, Whittingham et al., ); J, Alpine accentor (Prunella collaris, Hartley et al., ); K, pukeko (Lambert et al., ); L, white‐throated magpie‐jay (Calocitta formosa, Berg, ); M, long‐tailed tit (Aegithalos caudatus, Hatchwell et al., ); N, superb fairy‐wren (Malurus cyaneus, Double and Cockburn, ); O, American crow (Corvus brachyrhynchos, Townsend et al., ) and P, ground tit (Parus humilis, Wang and Lu, ). Q, red‐winged fairy‐wren (Malurus elegans, Brouwer et al., ).
close

References

Awata S, Munehara H and Kohda M (2005) Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses. Behavioral Ecology and Sociobiology 58: 506–516.

Baglione V, Canestrari D, Marcos JM, and Ekman J (2006) Experimentally increased food resources in the natal territory promote offspring philopatry and helping in cooperatively breeding carrion crows. Proceedings of the Royal Society of London B 273: 1529–1535.

Bell MBV, Cant MA, Borgeaud C, et al. (2014) Suppressing subordinate reproduction provides benefits to dominants in cooperative societies of meerkats. Nature Communications 5: 4499.

Berg EC (2005) Parentage and reproductive success in the white‐ throated magpie‐jay, Calocitta formosa, a cooperative breeder with female helpers. Animal Behaviour 70: 375–385.

Bergmüller R, Johnstone RA, Russell AF and Bshary R (2007) Integrating cooperative breeding into theoretical concepts. Behavioural Processes 76: 61–72.

Brouwer L, Tinbergen JM, Both C, et al. (2009) Experimental evidence for density‐dependent reproduction in a cooperatively breeding passerine. Ecology 90: 729–741.

Brouwer L, van de Pol M, Atema E and Cockburn A (2011) Strategic promiscuity helps avoid inbreeding at multiple levels in a cooperative breeder where both sexes are philopatric. Molecular Ecology 20: 4796–4807.

Buston P (2003) Social hierarchies: size and growth modification in clownfish. Nature 424: 145–146.

Canestrari D, Marcos JM and Baglione V (2009) Cooperative breeding in carrion crows reduces the rate of brood parasitism by great spotted cuckoos. Animal Behaviour 77: 1337–1344.

Cant MA (2012) Suppression of social conflict and evolutionary transitions to cooperation. American Naturalist 179: 293–301.

Clobert J, Danchin E, Dhondt AA and Nichols JD (eds) (2001) Dispersal. Oxford, UK: Oxford University Press.

Clutton‐Brock TH (2009) Cooperation between non‐kin in animal societies. Nature 462: 51–57.

Clutton‐Brock TH, Brotherton PNM, Smith R, et al. (1998) Infanticide and expulsion of females in a cooperative mammal. Proceedings of the Royal Society of London Series B‐Biological Sciences 265: 2291–2295.

Clutton‐Brock TH, Brotherton PNM, Russell AF, et al. (2001) Cooperation, control, and concession in meerkat groups. Science 291: 478–481.

Clutton‐Brock TH, Hodge S and Flower T (2008) Group size and the suppression of subordinate reproduction in Kalahari meerkats. Animal Behaviour 76: 689–700.

Cockburn A (2004) Mating systems and sexual conflict. In: Koenig WD and Dickinson J (eds) Cooperative Breeding in Birds: Recent Research and New Theory, pp. 81–101. Cambridge, MA: Cambridge University Press.

Cockburn A (2006) Prevalence of different modes of parental care in birds. Proceedings of the Royal Society of London B 273: 1375–1383.

Cockburn A (2010) Evolutionary biology: Oh sibling, who art thou? Nature 466: 930–931.

Cockburn A, Osmond HL, Mulder RA, et al. (2003) Divorce, dispersal and incest avoidance in the cooperatively breeding superb fairy‐wren Malurus cyaneus. Journal of Animal Ecology 72: 189–202.

Cornwallis CK, West SA and Griffin AS (2009) Routes to indirect fitness in cooperatively breeding vertebrates: kin discrimination and limited dispersal. Journal of Evolutionary Biology 22: 2445–2457.

Cornwallis CK, West SA, Davis KE and Griffin AS (2010) Promiscuity and the evolutionary transition to complex societies. Nature 466: 969–972.

Creel S, Creel NM, Mills MGL, and Monfort SL (1997) Rank and reproduction in cooperatively breeding African wild dogs: behavioral and endocrine correlates. Behavioral Ecology 8: 298–306.

Crick HQ (1992) Load‐lightening in cooperatively breeding birds and the cost of reproduction. Ibis 134: 56–61.

Darwin C (1859) On the Origin of Species. London, UK: Murray.

Dierkes P, Taborsky M and Kohler U (1999) Reproductive parasitism of broodcare helpers in a cooperatively breeding fish. Behavioral Ecology 10: 510–515.

Dillard JR and Westneat DF (2016) Disentangling the correlated evolution of monogamy and cooperation. Trends in Ecology and Evolution 31: 503–513.

Double CM and Cockburn A (2003) Subordinate superb fairy‐ wrens (Malurus cyaneus) parasitize the reproductive success of attractive dominant males. Proceedings of the Royal Society of London Series B 270: 379–384.

Ekman J, Baglione V, Eggers S and Griesser M (2001) Delayed dispersal: living under the reign of nepotistic parents. The Auk 118: 1–10.

Eikenaar C, Richardson DS, Brouwer L and Komdeur J (2007) Parent presence, delayed dispersal, and territory acquisition in the Seychelles warbler. Behavioural Ecology 18: 874–879.

Feeney WE, Medina I, Somveille M, et al. (2013) Brood parasitism and the evolution of cooperative breeding in birds. Science 342: 1506–1508.

Fuller TK, Kat PW, Bulger JB, et al. (1992) Population dynamics of African wild dogs. In: McCullough DR and Barret RH (eds) Wildlife 2001: Populations, pp. 1125–1139. London, UK: Elsevier Applied Sciences.

Gardner A and West SA (2004) Spite and the scale of competition. Journal of Evolutionary Biology 17: 1195–1203.

Girman DJ, Mills MGL, Geffen E and Wayne RK (1997) A molecular genetic analysis of social structure, dispersal, and interpack relationships of the African wild dog (Lycaon pictus). Behavioral Ecology and Sociobiology 40: 187–198.

Greenwood PJ (1980) Mating systems, philopatry and dispersal in birds and mammals. Animal Behaviour 28: 1140–1162.

Griesser M and Ekman J (2004) Nepotistic alarm calling in the Siberian jay. Perisoreus infaustus Animal Behaviour 67: 933–939.

Griffin AS and West S (2003) Kin discrimination and the benefit of helping in cooperatively breeding vertebrates. Science 302: 634–636.

Griffin AS, Pemberton JM, Brotherton PNM, et al. (2003) A genetic analysis of breeding success in the cooperative meerkat (Suricata suricatta). Behavioural Ecology 14: 472–480.

Hamilton WD (1964) The genetical evolution of social behaviour. Journal of Theoretical Biology 7: 1–52.

Hammers M, Kingma SA, Bebbington K, et al. (2015) Senescence in the wild: insights from a long‐term study on Seychelles warblers. Experimental Gerontology 71: 69–79.

Hannon SJ, Mumme RL, Koenig WD, and Pitelka FA (1985) Replacement of breeders and within-group conflict in the cooperatively breeding acorn woodpecker. Behavioral Ecology and Sociobiology 17: 303–312.

Hartley IR, Davies NB, Hatchwell BJ, et al. (1995) The polygynandrous mating system of the alpine accentor, Prunella collaris, II. Multiple paternity and parental effort. Animal Behaviour 49: 789–803.

Hatchwell BJ (1999) Investment strategies of breeders in avian cooperative breeding systems. American Naturalist 154: 205–219.

Hatchwell BJ and Komdeur J (2000) Ecological constraints, life history traits and the evolution of cooperative breeding. Animal Behaviour 59: 1079–1086.

Hatchwell BJ, Ross DJ, Chaline N, et al. (2002) Parentage in the cooperative breeding system of long‐tailed tits, Aegithalos caudatus. Animal Behaviour 64: 55–63.

Heg D, Bachar Z, Brouwer L and Taborsky M (2004) Predation risk is an ecological constraint for helper dispersal in a cooperatively breeding cichlid. Proceedings of the Royal Society of London Series B‐Biological Sciences 271: 2367–2374.

Heinsohn RG (2004) Parental care, load‐lightening, and costs. In: Koenig WD and Dickinson J (eds) Cooperative Breeding in Birds: Recent Research and New Theory, pp. 67–80. Cambridge, MA: Cambridge University Press.

Heinsohn R and Legge S (1999) The cost of helping. Trends in Ecology and Evolution 14: 53–57.

Hidalgo‐Aranzamendi N, Hall ML, Kingma SA, et al. (2016) Incest avoidance, extrapair paternity, and territory quality drive divorce in a year‐round territorial bird. Behavioral Ecology. DOI: 10.1093/beheco/arw10.

Huchard E, English S, Bell MBV, et al. (2016) Competitive growth in a cooperative mammal. Nature 533: 532–534.

Jetz W and Rubenstein DR (2011) Environmental uncertainty and the global biogeography of cooperative breeding in birds. Current Biology 21: 72–78.

Keane B, Waser PM, Creel SR, et al. (1994) Subordinate reproduction in dwarf mongooses. Animal Behaviour 47: 65–75.

Kingma SA, Hall ML and Peters A (2011) Multiple benefits drive helping behavior: an integrated analysis. American Naturalist 177: 486–495.

Kingma SA, Hall ML and Peters A (2013) Breeding synchronization facilitates extrapair mating for inbreeding avoidance. Behavioral Ecology 24: 1390–1397.

Kingma SA, Santema P, Taborsky M and Komdeur J (2014) Group augmentation and the evolution of cooperation. Trends in Ecology and Evolution 29: 476–484.

Kingma SA, Komdeur J, Hammers M and Richardson DS (2016a) The cost of prospecting for dispersal opportunities in a social bird. Biological Letters 12: 20160316.

Kingma SA, Bebbington K, Hammers M, et al. (2016b) Delayed dispersal and the costs and benefits of different routes to independent breeding in a cooperatively breeding bird. Evolution. DOI: 10.1111/evo.13071.

Kokko H, Johnstone RA and Clutton‐Brock TH (2001) The evolution of cooperative breeding through group augmentation. Proceedings of the Royal Society of London Series B‐Biological Sciences 268: 187–196.

Komdeur J (1992) Importance of habitat saturation and territory quality for the evolution of cooperative breeding in the Seychelles warbler. Nature 358: 493–495.

Komdeur J (1996) Influence of helping and breeding experience on reproductive performance in the Seychelles warbler: a translocation experiment. Behavioural Ecology 7: 326–333.

Komdeur J, Richardson DS and Hatchwell B (2008) Kin‐recognition mechanisms in cooperative breeding systems: ecological causes and behavioral consequences of variation. In: Heinze J and Korb J (eds) Ecology of Social Evolution, pp. 175–193. Berlin, Germany: Springer‐Verlag.

Komdeur J, Huffstadt A, Prast W, et al. (1995) Transfer experiments of Seychelles warblers to new islands: changes in dispersal and helping behaviour. Animal Behaviour 49: 695–708.

Krause J and Ruxton GD (2002) Living in Groups. Oxford, UK: Oxford University Press.

Lambert DM, Millar CD, Jack K, et al. (1994) Single‐locus and multilocus DNA fingerprinting of communally breeding pukeko – do copulations or dominance en‐ sure reproductive success? Proceedings of the National Academy of Sciences of the U S A 91: 9641–9645.

Lehmann L and Keller L (2006) The evolution of cooperation and altruism ‐ a general framework and a classification of models. Journal of Evolutionary Biology 19: 1365–1376.

Ligon JD and Ligon SH (1978) The communal social system of the green woodhoopoe in Kenya. Living Bird 17: 159–197.

Ligon JD, Ligon SH and Ford HA (1991) An experimental study of the basis of male philopatry in the cooperatively breeding superb fairy‐wren Malurus cyaneus. Ethology 87: 134–148.

Lukas D and Clutton‐Brock TH (2011) Group structure, kinship, inbreeding risk and habitual female dispersal in plural‐breeding mammals. Journal of Evolutionary Biology 24: 2624–2630.

Lukas D and Clutton‐Brock TH (2012) Cooperative breeding and monogamy in mammalian societies. Proceedings of the Royal Society of London Series B‐Biological Sciences 279: 2151–2156.

Macedo RH and Bianchi CA (1997) Communal breeding in tropical Guira Cuckoos Guira guira: sociality in the absence of a saturated habitat. Journal of Avian Biology 28: 207–215.

MacLeod KJ, Nielsen JF and Clutton‐Brock TH (2013) Factors predicting the frequency, likelihood and duration of allonursing in the cooperatively breeding meerkat. Animal Behaviour 86: 1059–1067.

Maynard Smith J (1964) Group selection and kin selection. Nature 201: 1145–1147.

McRae SB (1996) Family values: costs and benefits of communal nesting in the moorhen. Animal Behaviour 52: 225–245.

Mulder RA and Langmore NE (1993) Dominant males punish helpers for temporary defection in superb fairy‐wrens. Animal Behaviour 45: 830–833.

Nichols HJ, Amos W, Bell MBV, et al. (2012) Food availability shapes patterns of helping effort in a cooperative mongoose. Animal Behaviour 83: 1377–1385.

Trubenová B and Hager R (2012) Reproductive skew theory. Encyclopedia of Life Sciences. DOI: 10.1002/9780470015902.a0023661.

Platt TG and Bever JD (2009) Kin competition and the evolution of cooperation. Trends in Ecology and Evolution 24: 370–377.

Pruett‐Jones SG and Lewis MJ (1990) Sex‐ratio and habitat limitation promote delayed dispersal in superb fairy‐wrens. Nature 348: 541–542.

Quilichini A, Debussche M and Thompson JDE (2001) Evidence for local outbreeding depression in the Mediterranean island endemic Anchusa crispa Viv. (Boraginaceae). Heredity 87: 190–197.

Quinn JS, Woolfenden GE, Fitzpatrick JW and White BN (1999) Multi‐locus DNA fingerprinting supports genetic monogamy in Florida scrub‐jays. Behavioral Ecology and Sociobiology 45: 1–10.

Richardson DS, Jury FL, Blaakmeer K, (2001) Parentage assignment and extra-group paternity in a cooperative breeder: The Seychelles warbler (Acrocephalus sechellensis). Molecular Ecology 10: 2263–2273.

Richardson DS, Komdeur J and Burke T (2004) Inbreeding in the Seychelles warbler: environment‐dependent maternal effects. Evolution 58: 2037–2048.

Ridley J, Komdeur J and Sutherland WJ (2003) Population regulation in group‐living birds: predictive models of the Seychelles warbler. Journal of Animal Ecology 72: 588–598.

Riehl C (2013) Evolutionary routes to non‐kin cooperative breeding in birds. Proceedings of the Royal Society B‐Biological Sciences 280: 20132245.

Russell AF and Hatchwell BJ (2001) Experimental evidence for kin‐biased helping in a cooperatively breeding vertebrate. Proceedings of the Royal Society of London Series B‐Biological Sciences 268: 2169–2174.

Russell AF, Sharpe LL, Brotherton PNM and Clutton‐Brock TH (2003) Cost minimization by helpers in cooperative vertebrates. Proceedings of the National Academy of Sciences of the United States of America 100: 3333–3338.

Russell AF, Langmore NE, Cockburn A, et al. (2007) Reduced egg investment can conceal helper effects in cooperatively breeding birds. Science 317: 941–944.

Selander RK (1964) Speciation in wrens of the genus Campylorynchus. University of California Publications in Zoology 74: 1–305.

Sharp SP, McGowan A, Wood MJ and Hatchwell BJ (2005) Learned kin recognition cues in a social bird. Nature 434: 1127–1130.

Smith JE (2014) Hamilton's legacy: kinship, cooperation and social tolerance in mammalian groups. Animal Behaviour 92: 291–304.

Sorato E, Gullett PR, Griffith SC and Russell AF (2012) Effects of predation risk on foraging behaviour and group size: adaptations in a social cooperative species. Animal Behaviour 84: 823–834.

Stacey PB and Ligon JD (1987) Territory quality and dispersal options in the acorn woodpecker, and a challenge to the habitat saturation model of cooperative breeding. The American Naturalist 130: 654–676.

Stacey PB, and Koenig WD (1990) Cooperative breeding in birds: long‐term studies of ecology and behaviour. Cambridge, UK: Cambridge University Press.

Solomon NG and French JA (eds) (1997) Cooperative Breeding in Mammals. Cambridge, MA: Cambridge University Press.

Taborsky M (1994) Sneakers, satellites and helpers: parasitic and cooperative behavior in fish reproduction. Advances in the Study of Behavior 23: 1–100.

Townsend AK, Clark AB, McGowan KJ and Lovette IJ (2009) Reproductive partitioning and the assumptions of reproductive skew models in the cooperatively breeding American crow. Animal Behaviour 77: 503–512.

Van de Crommenacker J, Komdeur J and Richardson DS (2011) Assessing the cost of helping: the roles of body condition and oxidative balance in the Seychelles warbler (Acrocephalus sechellensis). PLoS One 6: e26423.

Trubenová B, and Hager R (2012) Reproductive skew theory. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023661]

Vehrencamp SL (2000) Evolutionary routes to joint-female nesting in birds. Behavioral Ecology 11: 334–344.

Wang C and Lu X (2011) Female ground tits prefer relatives as extra‐pair partners: driven by kin selection? Molecular Ecology 20: 2851–2863.

Whittingham LA, Dunn PO and Magrath RD (1997) Related‐ ness, polyandry and extra‐group paternity in the cooperatively breeding white‐browed scrubwren (Sericornis frontalis). Behavioral Ecology and Sociobiology 40: 261–270.

Young AJ, Carlson AA, Monfort SL, et al. (2006) Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proceedings of the National Academy of Science 103: 12005–12010.

Zahavi A (1990) Arabian babblers: the quest for social status in a cooperative breeder. In: Stacey B and Koenig WD (eds) Cooperative Breeding in Birds, pp. 105–130. Cambridge, MA: Cambridge University Press.

Further Reading

Brown JL (1987) Helping and Communal Breeding in Birds. Princeton, NJ: Princeton University Press.

Clutton‐Brock TH (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296: 69–72.

Cockburn A (1998) Evolution of helping behavior in cooperatively breeding birds. Annual Review of Ecology and Systematics 29: 141–177.

Emlen ST (1982) The evolution of helping. 1. An ecological constraints model. 2. The role of behavioral conflict. The American Naturalist 119: 29–39.

Green JP, Freckleton RP and Hatchwell BJ (2016) Variation in helper effort among cooperatively breeding bird species is consistent with Hamilton's Rule. Nature Communications 7: 12663.

Hatchwell BJ (2009) The evolution of cooperative breeding in birds: kinship, dispersal and life history. Philosophical Transactions of the Royal Society B‐Biological Sciences 364: 3217–3227.

Kingma SA, Hall ML, Arriero E and Peters A (2010) Multiple benefits of cooperative breeding in purple‐crowned fairy‐wrens: a consequence of fidelity? Journal of Animal Ecology 79: 757–768.

Koenig WD and Dickinson JL (eds) (2004) Ecology and Evolution of Cooperative Breeding in Birds. Cambridge, MA: Cambridge University Press.

Koenig WD and Dickinson JL (eds) (2016) Cooperative Breeding in Vertebrates: Studies of Ecology, Evolution,and Behavior. Cambridge, MA: Cambridge University Press.

Stacey PP and Ligon JD (1991) The benefits‐of‐philopatry hypothesis for the evolution of cooperative breeding: variation in territory quality and group size effects. The American Naturalist 137: 831–846.

Walters JR, Copeyon CK and Carter JH (1992) Test of the ecological basis of cooperative breeding in red‐cockaded woodpeckers. The Auk 109: 90–97.

West SA, Griffin AS and Gardner A (2007) Evolutionary explanations for cooperation. Current Biology 17: 661–672.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Komdeur, Jan, Richardson, David S, Hammers, Martijn, Eikenaar, Cas, Brouwer, Lyanne, and Kingma, Sjouke A(Apr 2017) The Evolution of Cooperative Breeding in Vertebrates. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0021218.pub2]