EDWARD WILSON has given us a characteristically fascinating account of the evolution of social insects (see 鈥淜inship doesn鈥檛 matter 鈥 how insects are altruistic鈥 and BioScience, vol 58, p 17). But his 鈥済roup selection鈥 terminology is misleading, and his distinction between 鈥渒in selection鈥 and 鈥渋ndividual direct selection鈥 is empty.
What matters is gene selection. All we need ask of a purportedly adaptive trait is, 鈥淲hat makes a gene for that trait increase in frequency?鈥 Wilson wrongly implies that explanations should resort to kin selection only when 鈥渄irect鈥 selection fails. Here he falls for the first of my 鈥溾; that is, he thinks it is a special, complex kind of natural selection, which it is not.
鈥淓dward Wilson thinks kin selection is a special, complex kind of natural selection, which it is not鈥
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In the true sense of kin selection, offspring are 鈥渒in鈥 just as siblings are. Parental care and sibling care both evolve because copies of genes for caring are present in beneficiaries. Genes promoting feeding of larvae by sterile workers are passed on by those larvae 鈥 sisters, nephews, and so on 鈥 destined to become reproductives. That鈥檚 kin selection, and it maintains sterile worker castes in insect colonies. Wilson could not dispute that.
What he does dispute 鈥 perhaps correctly 鈥 is that eusociality originated through related females clubbing together because of kinship. It could also originate through unrelated females nesting together. But to call this 鈥済roup selection鈥 is massively confusing. A better approach is John Maynard Smith鈥檚 concept of evolutionarily stable strategies (ESS). 鈥淪table鈥 means that when most individuals follow the strategy, no alternative does better. If 鈥渂reed cooperatively鈥 were a stable strategy for unrelated females, this would furnish a good preadaptation for the evolution of eusociality.
Jane Brockmann, now at the University of Florida, Gainesville, and I explored this with an ESS model developed with Alan Grafen of the University of Oxford, using Brockmann鈥檚 fieldwork on solitary digger wasps, Sphex ichneumoneus. When following the 鈥渄ig鈥 strategy, a female digs a burrow, provisions it with prey on which she lays a single egg, seals the burrow and departs. But burrows may be abandoned and this opens the way for an alternative strategy: 鈥渆nter鈥 an existing burrow and take it over, saving the time and effort of digging. The disadvantage is that the original owner may not have abandoned the burrow, and you run the risk of a dangerous fight. So the decision whether to enter or dig is a gamble.
With too much entering in the population, not enough new burrows get dug and chances rise that a given burrow will be occupied. Selection would therefore favour digging. With too much digging, many abandoned burrows go begging, and individuals should enter instead. Grafen鈥檚 ESS model predicted an equilibrium frequency of digging versus entering with equal benefits to each. Brockmann鈥檚 field measurements were rich enough to test this prediction, and it was, with reservations, fulfilled.
Brockmann and I then postulated an ecological 鈥渓andscape鈥 over which the parameters governing Grafen鈥檚 model might vary. A change in ecological conditions might move digger wasps from an 鈥渁ggressive space鈥 strategy, as used by S. ichneumoneus, to 鈥渢olerant space鈥 鈥 where diggers benefit from being joined by an enterer. From here there is a smooth gradient to 鈥渃ooperative space鈥, where both parties benefit from sharing. Our review of the literature uncovered wasp species that apparently take such intermediate positions. From here, the evolutionary journey to full eusociality is easy.
Revealingly, Wilson鈥檚 great book Sociobiology allots only four sentences 鈥 in the chapter on group selection 鈥 to ESS theory. Kin selection is also here, as a form of group selection! Evidently Wilson鈥檚 weird infatuation with 鈥済roup selection鈥 goes way back: unfortunate in a biologist who is so justly influential.
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