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Cooperation—The role of past and present
Behavioural Processes 76 (2007) 118–119
Commentary
Cooperation—The role of past and present Jan Ekman ∗ Department of Ecology and Evolution/Population Biology, Evolutionary Biology Centre, Uppsala University, Norbyv¨agen 18 D, 752 36 Uppsala, Sweden Received 22 December 2006; accepted 22 December 2006
Cooperation is with its seemingly inherent instability one of the most galvanizing questions in evolutionary biology. Kinship has been one answer to the evolution of stable cooperation (Foster et al., 2006), but rather than being an essential factor promoting social cohesion kinship appears to be one among several (Clutton-Brock, 2002). The ever-growing number of examples of cooperation among unrelated individuals defies the explanation of cooperation in the form of an “extended self” through the genetic self interest of assisting kin (Clutton-Brock, 2002; Cockburn, 1998). The challenge remains to find what forges stable coherence among unrelated cooperators. Cooperative breeding has been a model system to study social cohesion, and it is not uncommon for unrelated individuals to provide assistance even if they have no share in reproduction (Cockburn, 1998, 2004). Current models explaining the collaboration among unrelated members in cooperatively breeding groups rely on general group living benefits such as group augmentation (Kokko et al., 2001) or the stability of individuals interactions like pay-to-stay (Gaston, 1978), prestige (Zahavi, 1995), and image scoring (Milinski et al., 2001; Nowak and Sigmund, 1998). The “four questions” (Bergm¨uller et al., 2007) take the stance of systematically poising the outcome of behavioural interactions in terms of cost/benefits (investment/repayment) which then can be analyzed as a game. In doing so the approach allows the entire landscape of possible interactions among actors to be explored. A “strategy tree” resulting from the “four questions” lays bare the diversity of mechanisms leading to social coherence and it further exposes why a single unifying explanation appears to be insufficient to account for the diversity of sociality in cooperatively breeding species. The “four questions” derive social coherence from the outcome of interactions among individuals. They focus on how social interactions define sharing and exchanging of commodi-
∗
Tel.: +46 18 471 26 27; fax: +46 18 471 64 24. E-mail address: [email protected].
0376-6357/$ – see front matter © 2007 Published by Elsevier B.V. doi:10.1016/j.beproc.2006.12.017
ties of all kinds among group mates, and by which routes such sharing can give rise to stable cooperation. As such they can serve as a tool to design collection of empirical data and structuring of the outcome of interactions. Basically they provide a template for classifying the effect of social interactions that can account for the maintenance of a stable cooperation. Yet, it is essential to be aware of the limitation that accounting for the maintenance of cooperation is made within the structure of extant group structure and mating systems. Now, cooperative behaviour is shaped not only by the inherent dynamics of interactions. There is a multitude of ways that cooperative groups can be organized, thus, setting the conditions for transactions among group members (Brown, 1987). To understand the outcome of cooperation this diversity needs to be explained, and accounts for the structures of cooperative groups and breeding systems cannot ignore the constraints that are a product of environment and design. Conceivably factors like history, phylogeny and biogeography have shaped large-scale patterns in the diversity of cooperative behaviour (Cockburn, 2003; Ekman and Ericson, 2006). Focusing on cooperative breeding specifically, the behaviour comes in many shapes and is now described within virtually all known forms of mating systems (Cockburn, 2004). We would be able to classify the consequences in fitness terms for members of cooperatively breeding groups according to the scheme in the “four questions”. To what extent interactions defining the “strategy tree” would then be sufficient to account for the diversity of mating systems within cooperatively breeding group remains to be explored. Rather, sexual selection may have shaped a diversity of mating systems that is as yet largely unaccounted for in cooperatively breeding species. Within a social environment with easy access to multiple mates sexual conflict should be rife with ample opportunities for sexual selection. Further cooperative breeding may have shifted some species into an evolutionary path with its own dynamics. In species like the white-winged chough, the brown jay or the apostlebird breeders rely on assistance from extra birds
J. Ekman / Behavioural Processes 76 (2007) 118–119
to raise offspring. Conceivably, the cooperative behaviour can have allowed these species or their ancestors to enter niches that would not have been accessible as an unassisted pair breeder. The “four questions” are based on the assumption that an adaptive peak is accessible. For cooperative breeding, this is a leap of faith. The ontogenetic route to become an extra bird in cooperatively breeding units is a sequential process, where stability of coherent non-breeding groups can be a prerequisite to cooperative breeding. Such an intermediate is obvious in kin groups where the offspring first have to survive together before they can become alloparenting extra birds, but it applies also to a situation where the non-breeding season is spent in the role as an unrelated group member. Thus, cooperative breeding may be absent under conditions where it would otherwise be favourable because conditions during the non-breeding season preclude family/group coherence. It would be perfectly possible that the breeding system of two species would differ under similar breeding conditions simply because they differ in ecology during the non-breeding season, preventing the origin of cooperative breeding in one of them. The adaptive peak could not be accessible simply because of absence of conditions forging the group coherence that would provide the social environment promoting selection for cooperative breeding. The sequential process in becoming an extra bird makes it crucial to be clear over the question asked. It is possible to ask (1) under which conditions coherent groups form providing the social environment allowing group members to eventually become extra birds, (2) under which conditions alloparental care (helping-at-the-nest) will be maintained within coherent social groups. Measuring the fitness outcome of alloparental care will only give an answer to the second question why alloparental care is maintained. This entails the frustrating conclusion that with the ontogeny towards becoming an alloparenting extra bird being a sequential process with stable non-breeding groups as a permissive precursor it may not be possible to generalize from results identifying factors promoting cooperative breeding from current utility, which may be one contributing factor to the seemingly bewildering diversity of cooperatively breeding system. A sweeping conclusion that fitness effects of alloparental care provides an adequate explanation for the maintenance of cooperative breeding in the wider sense including stable non-breeding groups would, thus, not be justified. Within a broader perspective of accounting for the diversity of cooperative breeding the question why coherent groups are formed in the first place must be accounted for. The “four questions” focus on the role of individual interactions in the maintenance of stable social units. This approach has
119
the potential to unify research traditions. Mammal studies have focused on social interactions while resorting to ecological constraints has prevailed as an explanation for cooperative breeding in birds (Russell, 2004). Yet, constraints are ubiquitous (Kokko and Ekman, 2002) and the limitations of ecological constraints as an explanation for joining cooperatively breeding groups are by now well established. Individuals that forego reproduction do not necessarily join cooperative or any other group, while equally subordinate group members do not necessarily forego reproduction. The fundament of the “four questions” is that the nature of social interactions is pivotal whether non-breeding individuals will eventually join groups. While not excluding the role of environmental quality this more inclusive approach assigning a role to social interactions forms the basis for a wider research program that could provide a deeper understanding of the diversity of cooperative groups. References Bergm¨uller, R., Johnstone, R., Russell, A., Bshary, R., 2007. Integrating cooperative breeding into theoretical concepts of cooperation. Behav. Process. Brown, J.L., 1987. Helping and Communal Breeding in Birds. Princeton University Press, Princeton, p. 354. Clutton-Brock, T., 2002. Behavioral ecology—breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69–72. Cockburn, A., 1998. Evolution of helping behavior in cooperatively breeding birds. Ann. Rev. Ecol. Syst. 29, 141–177. Cockburn, A., 2003. Cooperative breeding in oscine passerines: does sociality inhibit speciation? Proc. R. Soc. Lond. B 270, 2207–2214. Cockburn, A., 2004. Mating systems and sexual conflict. In: Koenig, W.D., Dickinson, J.L. (Eds.), Ecology and Evolution of Cooperative Breeding in Birds. Cambridge University Press, Cambridge, pp. 81–101. Ekman, J., Ericson, P.G.P., 2006. Out of Gondwanaland; the evolutionary history of cooperative breeding and social behaviour among crows, magpies, jays and allies. Proc. R. Soc. Lond. B 273, 1117–1125. Foster, K.R., Wenseleers, T., Ratnieks, F.L.W., 2006. Kin selection is the key to altruism. Trends Ecol. Evol. 21, 57–60. Gaston, A.J., 1978. The evolution of group territorial behaviour and cooperative breeding. Am. Nat. 112, 1091–1100. Kokko, H., Ekman, J., 2002. Delayed dispersal as a route to breeding: territorial inheritance, safe havens, and ecological constraints. Am. Nat. 160, 468–484. Kokko, H., Johnstone, R.A., Clutton-Brock, T.H., 2001. The evolution of cooperative breeding through group augmentation. Proc. R. Soc. Lond. B 268, 187–196. Milinski, M., Semmann, D., Bakker, T.C.M., Krambeck, H.J., 2001. Cooperation through indirect reciprocity: image scoring or standing strategy? Proc. R. Soc. Lond. B 268, 2495–2501. Nowak, M.A., Sigmund, K., 1998. Evolution of indirect reciprocity by image scoring. Nature 393, 573–577. Russell, A.J., 2004. Mammals: comparisons and contrasts. In: W.D. Koenig, J.L. Dickinson, (Eds.), Ecology and Evolution of Cooperative Breeding in Birds, pp. 210–227. Zahavi, A., 1995. Altruism as a Handicap: the limitations of kin selection and reciprocity. J. Avian Biol. 26, 1–3.
Commentary
Cooperation—The role of past and present Jan Ekman ∗ Department of Ecology and Evolution/Population Biology, Evolutionary Biology Centre, Uppsala University, Norbyv¨agen 18 D, 752 36 Uppsala, Sweden Received 22 December 2006; accepted 22 December 2006
Cooperation is with its seemingly inherent instability one of the most galvanizing questions in evolutionary biology. Kinship has been one answer to the evolution of stable cooperation (Foster et al., 2006), but rather than being an essential factor promoting social cohesion kinship appears to be one among several (Clutton-Brock, 2002). The ever-growing number of examples of cooperation among unrelated individuals defies the explanation of cooperation in the form of an “extended self” through the genetic self interest of assisting kin (Clutton-Brock, 2002; Cockburn, 1998). The challenge remains to find what forges stable coherence among unrelated cooperators. Cooperative breeding has been a model system to study social cohesion, and it is not uncommon for unrelated individuals to provide assistance even if they have no share in reproduction (Cockburn, 1998, 2004). Current models explaining the collaboration among unrelated members in cooperatively breeding groups rely on general group living benefits such as group augmentation (Kokko et al., 2001) or the stability of individuals interactions like pay-to-stay (Gaston, 1978), prestige (Zahavi, 1995), and image scoring (Milinski et al., 2001; Nowak and Sigmund, 1998). The “four questions” (Bergm¨uller et al., 2007) take the stance of systematically poising the outcome of behavioural interactions in terms of cost/benefits (investment/repayment) which then can be analyzed as a game. In doing so the approach allows the entire landscape of possible interactions among actors to be explored. A “strategy tree” resulting from the “four questions” lays bare the diversity of mechanisms leading to social coherence and it further exposes why a single unifying explanation appears to be insufficient to account for the diversity of sociality in cooperatively breeding species. The “four questions” derive social coherence from the outcome of interactions among individuals. They focus on how social interactions define sharing and exchanging of commodi-
∗
Tel.: +46 18 471 26 27; fax: +46 18 471 64 24. E-mail address: [email protected].
0376-6357/$ – see front matter © 2007 Published by Elsevier B.V. doi:10.1016/j.beproc.2006.12.017
ties of all kinds among group mates, and by which routes such sharing can give rise to stable cooperation. As such they can serve as a tool to design collection of empirical data and structuring of the outcome of interactions. Basically they provide a template for classifying the effect of social interactions that can account for the maintenance of a stable cooperation. Yet, it is essential to be aware of the limitation that accounting for the maintenance of cooperation is made within the structure of extant group structure and mating systems. Now, cooperative behaviour is shaped not only by the inherent dynamics of interactions. There is a multitude of ways that cooperative groups can be organized, thus, setting the conditions for transactions among group members (Brown, 1987). To understand the outcome of cooperation this diversity needs to be explained, and accounts for the structures of cooperative groups and breeding systems cannot ignore the constraints that are a product of environment and design. Conceivably factors like history, phylogeny and biogeography have shaped large-scale patterns in the diversity of cooperative behaviour (Cockburn, 2003; Ekman and Ericson, 2006). Focusing on cooperative breeding specifically, the behaviour comes in many shapes and is now described within virtually all known forms of mating systems (Cockburn, 2004). We would be able to classify the consequences in fitness terms for members of cooperatively breeding groups according to the scheme in the “four questions”. To what extent interactions defining the “strategy tree” would then be sufficient to account for the diversity of mating systems within cooperatively breeding group remains to be explored. Rather, sexual selection may have shaped a diversity of mating systems that is as yet largely unaccounted for in cooperatively breeding species. Within a social environment with easy access to multiple mates sexual conflict should be rife with ample opportunities for sexual selection. Further cooperative breeding may have shifted some species into an evolutionary path with its own dynamics. In species like the white-winged chough, the brown jay or the apostlebird breeders rely on assistance from extra birds
J. Ekman / Behavioural Processes 76 (2007) 118–119
to raise offspring. Conceivably, the cooperative behaviour can have allowed these species or their ancestors to enter niches that would not have been accessible as an unassisted pair breeder. The “four questions” are based on the assumption that an adaptive peak is accessible. For cooperative breeding, this is a leap of faith. The ontogenetic route to become an extra bird in cooperatively breeding units is a sequential process, where stability of coherent non-breeding groups can be a prerequisite to cooperative breeding. Such an intermediate is obvious in kin groups where the offspring first have to survive together before they can become alloparenting extra birds, but it applies also to a situation where the non-breeding season is spent in the role as an unrelated group member. Thus, cooperative breeding may be absent under conditions where it would otherwise be favourable because conditions during the non-breeding season preclude family/group coherence. It would be perfectly possible that the breeding system of two species would differ under similar breeding conditions simply because they differ in ecology during the non-breeding season, preventing the origin of cooperative breeding in one of them. The adaptive peak could not be accessible simply because of absence of conditions forging the group coherence that would provide the social environment promoting selection for cooperative breeding. The sequential process in becoming an extra bird makes it crucial to be clear over the question asked. It is possible to ask (1) under which conditions coherent groups form providing the social environment allowing group members to eventually become extra birds, (2) under which conditions alloparental care (helping-at-the-nest) will be maintained within coherent social groups. Measuring the fitness outcome of alloparental care will only give an answer to the second question why alloparental care is maintained. This entails the frustrating conclusion that with the ontogeny towards becoming an alloparenting extra bird being a sequential process with stable non-breeding groups as a permissive precursor it may not be possible to generalize from results identifying factors promoting cooperative breeding from current utility, which may be one contributing factor to the seemingly bewildering diversity of cooperatively breeding system. A sweeping conclusion that fitness effects of alloparental care provides an adequate explanation for the maintenance of cooperative breeding in the wider sense including stable non-breeding groups would, thus, not be justified. Within a broader perspective of accounting for the diversity of cooperative breeding the question why coherent groups are formed in the first place must be accounted for. The “four questions” focus on the role of individual interactions in the maintenance of stable social units. This approach has
119
the potential to unify research traditions. Mammal studies have focused on social interactions while resorting to ecological constraints has prevailed as an explanation for cooperative breeding in birds (Russell, 2004). Yet, constraints are ubiquitous (Kokko and Ekman, 2002) and the limitations of ecological constraints as an explanation for joining cooperatively breeding groups are by now well established. Individuals that forego reproduction do not necessarily join cooperative or any other group, while equally subordinate group members do not necessarily forego reproduction. The fundament of the “four questions” is that the nature of social interactions is pivotal whether non-breeding individuals will eventually join groups. While not excluding the role of environmental quality this more inclusive approach assigning a role to social interactions forms the basis for a wider research program that could provide a deeper understanding of the diversity of cooperative groups. References Bergm¨uller, R., Johnstone, R., Russell, A., Bshary, R., 2007. Integrating cooperative breeding into theoretical concepts of cooperation. Behav. Process. Brown, J.L., 1987. Helping and Communal Breeding in Birds. Princeton University Press, Princeton, p. 354. Clutton-Brock, T., 2002. Behavioral ecology—breeding together: kin selection and mutualism in cooperative vertebrates. Science 296, 69–72. Cockburn, A., 1998. Evolution of helping behavior in cooperatively breeding birds. Ann. Rev. Ecol. Syst. 29, 141–177. Cockburn, A., 2003. Cooperative breeding in oscine passerines: does sociality inhibit speciation? Proc. R. Soc. Lond. B 270, 2207–2214. Cockburn, A., 2004. Mating systems and sexual conflict. In: Koenig, W.D., Dickinson, J.L. (Eds.), Ecology and Evolution of Cooperative Breeding in Birds. Cambridge University Press, Cambridge, pp. 81–101. Ekman, J., Ericson, P.G.P., 2006. Out of Gondwanaland; the evolutionary history of cooperative breeding and social behaviour among crows, magpies, jays and allies. Proc. R. Soc. Lond. B 273, 1117–1125. Foster, K.R., Wenseleers, T., Ratnieks, F.L.W., 2006. Kin selection is the key to altruism. Trends Ecol. Evol. 21, 57–60. Gaston, A.J., 1978. The evolution of group territorial behaviour and cooperative breeding. Am. Nat. 112, 1091–1100. Kokko, H., Ekman, J., 2002. Delayed dispersal as a route to breeding: territorial inheritance, safe havens, and ecological constraints. Am. Nat. 160, 468–484. Kokko, H., Johnstone, R.A., Clutton-Brock, T.H., 2001. The evolution of cooperative breeding through group augmentation. Proc. R. Soc. Lond. B 268, 187–196. Milinski, M., Semmann, D., Bakker, T.C.M., Krambeck, H.J., 2001. Cooperation through indirect reciprocity: image scoring or standing strategy? Proc. R. Soc. Lond. B 268, 2495–2501. Nowak, M.A., Sigmund, K., 1998. Evolution of indirect reciprocity by image scoring. Nature 393, 573–577. Russell, A.J., 2004. Mammals: comparisons and contrasts. In: W.D. Koenig, J.L. Dickinson, (Eds.), Ecology and Evolution of Cooperative Breeding in Birds, pp. 210–227. Zahavi, A., 1995. Altruism as a Handicap: the limitations of kin selection and reciprocity. J. Avian Biol. 26, 1–3.