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HOME > PAST ISSUE > July-August 2014 > Article Detail

FEATURE ARTICLE

Why Some Animals Forgo Reproduction in Complex Societies

Behaviors of coral reef fishes provide strong support for some major new ideas about the evolution of cooperation.

Peter Buston, Marian Wong

2014-07BustonFp291.jpgClick to Enlarge ImageCharles Darwin’s On the Origin of Species laid the foundations for evolutionary biology and understanding of life on Earth. Even as he was marshalling evidence for the theory of natural selection, Darwin made a point of highlighting observations that seemed to challenge his ideas:

I… will confine myself to one special difficulty, which at first appeared to me insuperable, and actually fatal to my whole theory, I allude to the neuters or sterile females in insect communities: for these neuters often differ widely in instinct and structure from both the male and fertile females, and yet from being sterile they cannot propagate their kind.

In the insect societies that Darwin was alluding to, such as ants or termites, there is a reproductive division of labor: Some individuals forgo their own reproduction and help others reproduce. To express Darwin’s special difficulty in modern terms, these societies are challenging to understand because it’s not immediately apparent how natural selection can preserve the genes that underlie nonbreeding and helping behaviors. Evolutionary biologists have puzzled over such cooperative behaviors ever since Darwin highlighted the challenge that they present to the theory of natural selection.

2014-07BustonFp292top.jpgClick to Enlarge ImageAlthough the social insects present extreme cases of sociality, social birds and mammals exhibit similar, if less extreme, forms of sociality. Indeed, behavioral ecologist Paul W. Sherman of Cornell University and others have suggested that the difference between social insects and social vertebrates is only one of degree, the various forms of sociality lying on a continuum. For example, birds such as white-fronted bee-eaters (Merops bullockoides) and mammals such as naked mole rats (Heterocephalus glaber), also live in complex societies in which some individuals forgo reproduction and help others to reproduce, at least at some point in their lives. Anthropologist Sarah B. Hrdy of University of California, Davis, and others have even argued that such cooperative breeding may have been pivotal in human evolution—essential to support our long and unusual life histories.

Social vertebrates have proven invaluable for developing and testing theories of social evolution—they often exhibit a high level of flexibility in behavior, which enables researchers to manipulate key variables and measure individual responses. In the 1980s, Stephen T. Emlen of Cornell University presented an evolutionary framework for understanding nonbreeding and helping strategies, based on studies of cooperatively breeding birds and mammals (see the sidebar “An Evolutionary Framework for Cooperative Behavior” below). This framework still guides much of today’s research. Emlen emphasized that, to understand cooperative breeding, there are two main questions to answer: First, why do individuals help; second, why don’t individuals disperse to breed elsewhere? The first question focuses on the reproductive payoff that individuals accrue from their current actions, whereas the second focuses on the payoff associated with alternative actions. This framework focused attention on two major reasons that nonbreeding and helping behaviors would evolve: kin selection and ecological constraints.

An Evolutionary Framework for Cooperative Behavior

The evolution of cooperative behavior depends on the costs and benefits of cooperative and alternative actions for the donor and its relatives: Cooperative behavior can be favored because of its beneficial effects on kin (called kin selection), and cooperative behavior can be favored because of the detrimental effects associated with alternative actions (called ecological constraints). The behavior favored by selection can be determined using the equation called Hamilton’s rule. In particular, the cooperative action i will be favored over the alternative action j if

Xi + ri Yi > Xj + rj Yj

where Xi (or Xj) is the number of offspring associated with donor’s ith (or jth) action, Yi (or Yj) is the recipient’s number of offspring, and r is the probability that the two individuals share a copy of a particular gene identical by descent. The r terms capture the effect of kin selection; the j terms capture the effect of ecological constraints. Hamilton’s theory of kin selection showed how altruism might evolve in groups of close kin and provided a solution to Darwin’s problem.








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