Help from earlier offspring in rearing a subsequent brood should evolve more easily when the mother is strictly monogamous. A comparative study of birds provides evidence in support of this view.
Cooperative breeding, in which more than two individuals combine to rear a single brood of young, has evolved repeatedly in animals, and most commonly in insects and birds. This situation poses an evolutionary paradox: because individuals have only two parents, some of the carers in these cooperative societies are helping to raise young that are not their own. The evolutionary biologist W. D. Hamilton famously solved part of the puzzle by pointing out that helping to rear siblings can be completely analogous to rearing your own offspring, as both actions facilitate the propagation of your own genes in subsequent generations.
However, many females are so promiscuous that young will be uncertain whether they share paternal genes with other young produced by their mother. This argument has been used to suggest that the evolutionary transition to and from cooperative care will depend on the extent to which the mother mates monogamously1,2. On page 969 of this issue, Cornwallis and colleagues3 exploit the great variation in the mating systems of cooperatively breeding birds to provide support for this hypothesis (Fig. 1).
The authors' approach involved use of the phylogenetic comparative method, which relates changes in the trait of interest on different branches of the tree of life to changes in potential explanatory factors. This approach is well known and frequently used, but Cornwallis et al. estimate the correlation by applying a novel and very general Bayesian statistical technique4. The response variable they initially investigated was whether birds bred cooperatively, an activity that they conclude declines strongly with an index of female infidelity — the proportion of broods in which some young are sired by extra-group (or extra-pair) males. The effect works in both directions: transition to cooperative breeding occurs more commonly in monogamous species, and transitions from cooperation to non-cooperation increase with infidelity.
The evolution of mechanisms to detect relatedness would allow potential helpers to overcome the uncertainty that flows from infidelity. However, the strength of evolutionary selection for sophisticated means of recognizing kinship will vary. It is sufficient to have a rule-of-thumb that presumes kinship if the female is always faithful; assuming limited relatedness also works if the female is highly promiscuous. Somewhere in the middle of these extremes, it would pay to know whether you are related or not and to adjust your care accordingly. Consistent with this view, Cornwallis et al. found that the ability of birds to vary their investment in offspring according to kinship was most pronounced at intermediate levels of infidelity.
The phylogenetic comparative method can be extremely powerful, but has some limitations. First, particularly with transitions to complex behavioural states, defining whether the transition has occurred is not always straightforward. Cooperative breeding in birds can be confined to family groups, can occur among completely unrelated individuals, or can be a bewildering mixture of the two5. Cornwallis et al. use a restrictive definition, and define cooperative breeding as applying only to family groups, which is reasonable, as their index of infidelity is defined as mating outside such groups. However, using this definition excludes a lot of the complexity that makes cooperative breeding most interesting, and potentially underemphasizes direct benefits to the provider of help relative to those derived indirectly through kinship.
The second universal problem of using correlations in evolutionary biology is that the direction of causation is often uncertain. For example, in Australian fairy wrens (Malurus species), which, despite ubiquitous cooperative breeding, are the least faithful of all birds6, females exploit the availability of helpers as an alternative source of care for their young, allowing them to increase the extent to which they cuckold their mates7. This indicates that cooperative behaviour can drive the incidence of fidelity rather than vice versa, and that the coevolution of fidelity and cooperation could be much more complex than is assumed in Cornwallis and colleagues' analysis. Nonetheless, their study provides a welcome and exciting direction for empiricists, who have failed miserably to produce models that predict the incidence of cooperative breeding.
We are most likely to learn about the forces that lead to cooperation by studying pairs of species sitting close to the point of evolutionary transition. To take a different case, the study of primitively social wasps might tell us more about the conditions that produce sociality in insects than does research on army ants in which the single queen could be attended by a million workers. Likewise, investigations of closely related birds that either lack or exhibit a low level of cooperative breeding might allow the most illuminating direct tests of the monogamy hypothesis. Although such primitively social birds lack the charisma of the most highly developed avian cooperative societies, there is new impetus for adding them to the already impressive array of birds in which molecular tools have been used to dissect patterns of parentage.
Boomsma, J. J. Curr. Biol. 17, R673–R683 (2007).
Boomsma, J. J. Phil. Trans. R. Soc. B 364, 3191–3207 (2009).
Cornwallis, C. K., West, S. A., Davis, K. E. & Griffin, A. S. Nature 466, 969–972 (2010).
Hadfield, J. D. J. Stat. Software 33(2), 1–22 (2010).
Cockburn, A. Annu. Rev. Ecol. Syst. 29, 141–177 (1998).
Griffith, S. C., Owens, I. P. F. & Thuman, K. A. Mol. Ecol. 11, 2195–2212 (2002).
Mulder, R. A., Dunn, P. O., Cockburn, A., Lazenby-Cohen, K. A. & Howell, M. J. Proc. R. Soc. Lond. B 255, 223–229 (1994).
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The importance of the altricial – precocial spectrum for social complexity in mammals and birds – a review
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