A new paper in Nature on bird reproduction ends with this provocative quote from E. O. Wilson’s Sociobiology: “sex is an antisocial force in evolution.” What does that mean? In the case of cooperatively breeding birds, the subject of the report by Charlie Cornwallis et al., it means that the cooperation between parents and their offspring is endangered if the parents have too much sex.
Cooperative breeding is the phenomenon whereby offspring help their parents have more offspring. In birds, the young will hang around at the nest and, rather than reproduce themselves, help their parents raise the next brood. The classic example is the Florida scrub jay (Aphelocoma coerulescens), but it’s estimated to occur in about 10% of all bird species.
It would seem to defy evolutionary sense to sacrifice your own reproduction to help your parents, but it may not. After all, a young bird is related by exactly as much to its own offspring as to the brothers and sisters that it could help its parents to raise: in both cases there is sharing of 50% of one’s genes. Any gene, then that promotes this behavior—do not reproduce yourself but help your parents raise more brothers and sisters—won’t necessarily be at a disadvantage. Indeed, if there’s a problem with you being able to reproduce personally, such as your having to first learn the ropes about how to tend broods, or your inability to gain a breeding territory since the area is full of other birds, the evolutionary balance may be tipped in favor of your deferring reproduction while you stay at home for a while, but still passing on your genes by helping mom and dad.
Cooperative breeding is a case of kin selection: animals exercising “altruism” (deferral or absence of reproduction) towards close relatives as a way of passing on their own genes. Kin selection is also the classic explanation for another very famous case of cooperative breeding: the sterile workers in social insects like ants and bees. In this case, because males are haploid, if the queen mates only once it may be genetically advantageous for a worker to produce more sisters, with whom she shares three-quarters of her genes, than to produce her own offspring, with whom she shares only half of her genes. This genetic explanation for sterile workers is controversial, but I won’t go into that now.
Now the kin-selection explanation for cooperative breeding in birds (and social insects) breaks down if the female parent is “promiscuous”, that is, mates more than once. If, after producing you, your mother then mates with a male who is not your own father, then your relatedness to her offspring drops from 50% to 25%. In that case you’d share more genes with your own offspring than with your potential brothers and sisters, and so it’s not such a good idea, evolutionarily speaking, to defer your own reproduction and help mom and dad. The evolution of cooperative breeding, then, is hindered if females are promiscuous, and you’d expect to see that phenomenon less often in promiscuous than in monogamous species.
That leads to the paper of Cornwallis et al., which is based on this prediction. The authors analyzed 267 bird species for which there was information about cooperative breeding, promiscuity of females, and their position in the phylogenetic tree of birds. There’s a lot of new information about promiscuity (or “extra-pair fertilization”—EPF) from DNA-based or other genetic evidence. It shows that birds are committing adultery all over the place: roughly three-quarters of bird species that appear monogamous because they breed in pairs (“social monogamy”) are actually promiscuous to some degree.
Correlating the data on cooperative breeding with that on promiscuity (and controlling the whole lot with the phylogeny), Cornwallis et al. showed the following:
- The level of promiscuity (that is, the number of broods containing at least “illegal” chick) was much lower in cooperatively breeding (about 12%) than in non cooperatively breeding species (about 24%).
- There was a significant negative relationship among species between levels of promiscuity and percentage of nests having cooperative breeders. In other words, those species that had very promiscuous females showed virtually no nests with cooperative breeding.
These might be taken as verifications of the prediction, but there’s a problem with that. Suppose that cooperative breeders formed a fairly closely related group, and the non-cooperative breeders another closely related group. Then the data points from the different species would not be independent: if promiscuity had evolved only once, on the branch separating these species, and likewise cooperative breeding (on the nonpromiscuous branch), your correlation among species would reflect only this single evolutionary branching. But Cornwallis wanted to see if there was a recurrent evolutionary pattern of cooperative breeding being associated with evolutionary decreases of promiscuity (and the converse). So they looked at the data using the evolutionary tree, which tells you about when these events took place. Doing this, they found that
- There was still a very strong negative correlation between the evolution of cooperative breeding and the evolution of promiscuity.
- Looking at those species that had evolved cooperative breeding from non-cooperative ancestors, those ancestors were less promiscuous than the non-cooperative ancestors of non-cooperative descendants. In other words, if you’re a non-cooperative species, you’re more likely to evolve cooperative breeding if you’re not too promiscuous.
- There was some suggestion (though it wasn’t statistically significant) that, if you look at cooperative ancestors, those that produced non-cooperative descendants were more promiscuous than those that produced only non-cooperative descendants.
On the whole, these data provide pretty strong support for the idea that cooperative breeding is more likely to evolve when females mate with fewer males. This verifies the kin-selection prediction that cooperative behaviors are favored when you are more related to those you help. It’s a nice piece of work. I’m a bit worried about reconstructing the level of promiscuity in ancestors (something that’s derived from inferences based on living species), which is problematic if the characters change too often; and there’s a potentially confounding factor if the degree of promiscuity is related to the likelihood of forming new species (which is plausible). Nevertheless, the paper gives some intriguing data supporting social evolution via kin selection, and, apart from the evolution of paternal/maternal behavior itself, we don’t have a lot of that kind of data.
C. K. Cornwallis, S. A. West, K. E. Davis, and A. S. Griffin. 2010. Promiscuity and the evolutionary transition to complex societies. Nature 466:969-972.