Bird of the week: When sluts rule…the genetic advantages of promiscuity

Until a few years ago there was a common perception that cooperative breeding systems in birds were altruistic and mutually beneficial systems of social organisation. Generally it was believed that the whole group – centred on monogamous pairs bonded for life – benefited from the selfless actions of a number of sub-adult individuals.

Birds of an age at which they  might normally be regarded as sexually mature – called ‘auxilliaries’ – would apparently temporarily surrender themselves as helpers to the breeding activity of dominant adult birds in the group. The common understanding was that auxilliaries gained additional ‘fitness’ by gaining familiarity with the rigours of the breeding processes.

Like all theories it was open to challenges and, as often seems to happen, Australian birds led the way as subjects for important research that has turned much of what we previously believed about cooperative breeding systems on its head.

What researchers began to find was that within many apparently stable cooperative breeding systems was a remarkable degree of “playing away“, with high rates of promiscuity in bird species previously thought to have breeding systems characterised by high levels of bonded pair faithfulness.  Typical of this work is a 2004 paper by Michael S. Webster of the School of Biological Sciences and Center for Reproductive Biology, Washington State University and his associates published in Behavioural Ecology and entitled Reproductive promiscuity in the Splendid Fairy-wren: effects of group size and auxiliary reproduction. There they found, in part, that:

Extrapair fertilizations complicate our understanding of cooperative breeding in a number of ways. For example, auxiliaries may reduce the costs of seeking extrapair fertilizations for breeding males or females, and auxiliary males may themselves seek copulations with the breeding female in their own group.

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Our study population exhibited a relatively high level of extrapair paternity (42% of 386 offspring) with considerable annual variation (range = 24–52%). Across years the proportion of offspring sired by extrapair males was significantly correlated with the average number of auxiliaries per group…Promiscuity complicates our understanding of cooperative breeding in several important ways. First, promiscuity can affect the Hamiltonian cost/benefit analysis for helping behavior…Second, in complex social systems like those of cooperative breeders, individual breeding strategies might be affected by group composition…Thus, there is now a need to better understand the causes and consequences of reproductive promiscuity in complex social systems. Fairy-wrens (Maluridae) have emerged as a model group for studying both cooperative breeding and reproductive promiscuity.

Later research led by Andrew Cockburn of the Evolutionary Ecology Group at the School of Botany and Zoology, Australian National University – also looking at fairy-wrens – examined the techniques involved in extra-pair infidelity. The title of that paper – Superb fairy-wren males aggregate into hidden leks to solicit extragroup fertilizations before dawn – says it all. It is an exquisite piece of research based on a longitudinal research at the National Botanical Gardens in Canberra on local populations of Superb Fairy-wrens. Cockburn and his colleagues found:

Female superb fairy-wrens Malurus cyaneus initiate extragroup fertilizations by forays to the territory of preferred males, just before sunrise, 2–4 days before egg laying. Over a prolonged breeding season, males advertise their availability to foraying females by singing during the dawn chorus.

I cannot do justice to the comprehensive research done by these – and many other – researchers in this brief post. For that you should follow the links to the papers – and then follow your nose with your own further research.

But in the last few weeks another piece of work – which, depending on your views may either clarify or complicate our already confused understanding of this aspect of bird breeding behaviour – has emerged.

Working with captive Australian Zebra Finches Taeniopygia guttata Wolfgang Forstmeier of the Max Planck Institute for Ornithology in Germany asked the question* – and I paraphrase – “While the benefits of extra-pair mating provide clear benefits for males, why – when the benefits for females are less clear – do females actively solicit extra-pair matings?

In many species that form socially monogamous pair bonds, a considerable proportion of the offspring is sired by extrapair males. This observation has remained a puzzle for evolutionary biologists: although mating outside the pair bond can obviously increase the offspring production of males, the benefits of such behavior to females are less clear, yet females are known to actively solicit extrapair copulations.

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Here we show that in the socially monogamous zebra finch, individual differences in extrapair mating behavior have a hereditary component. Intriguingly, this genetic basis is shared between the sexes, as shown by a strong genetic correlation between male and female measurements of extrapair mating behavior. Hence, positive selection on males to sire extrapair young will lead to increased extrapair mating by females as a correlated evolutionary response. This behavior leads to a fundamentally different view of female extrapair mating: it may exist even if females obtain no net benefit from it, simply because the corresponding alleles were positively selected in the male ancestors.

I think what Forstmeier is saying is that notwithstanding the lack of any clear benefit to females from extra-pair promiscuity – they run the twin risks of additional exposure to disease and the loss of the original mate-relationship – a pre-disposition to that behaviour is transmissable from a promiscuous male to his female offspring and that same pre-disposition is transferred to that females’ male offspring.

For some this research is ground-breaking. In his piece at i09.com Alasdair Wilkins has this quote from Sidney Griffith of Australia’s Macquarie University with his take on Forstmeier’s research:

This is an excellent and very important study that I am very excited about. Their study is the most intensive study to date to investigate the behaviour associated with extra-pair paternity. What they have demonstrated really nicely is a genetic correlation between promiscuous behaviour in males and females. It is important to realise that any mating behaviour in sexually reproducing animals may be shaped by the same kind of genetic architecture – genes that are carried by both sexes and may be expressed in both males and females but where strong selection in one sex drives behaviour in the other sex that at first does not appear to make sense.

Others are more cautious. Over at ScienceNews, Susan Milius notes that Andrew Cockburn – whose work with Fairy-wrens I noted above – urges caution in making broad-based assumptions about Forstmeier’s work:

While male and female infidelity genetics may be linked, says Andrew Cockburn of the Australian National University in Canberra, he’s not convinced of the by-product explanation for females, that they always suffer. “Another explanation of a strong positive correlation is that extrapair mating is beneficial to both sexes,” he says. And in theory, strong selection on females to be faithful could just as easily spill over in males and rein in philandering.

In any case, he says, females of different species, such as the fairy wrens Cockburn studies, may find different benefits from extrapair mating, like upgrades in genes for the chicks. “The problem is to determine the relative importance of these mechanisms,” he says, “not to assume that there is a single explanation that can be extrapolated across all species.”

* I cannot find a direct link to this paper, but it may emerge soon: Forstmeier, W., Martin, K., Bolund, E., Schielzeth, H., Kempenaers, B.: Female extra-pair mating behavior can evolve via indirect selection on males. Proceedings of the National Academy of Sciences, in press