Findings published this week in PLoS Biology claim that worker policing in social insects has a more complex evolutionary basis than even their unusual patterns of genetic relatedness allow. Instead, it is the 'colony efficiency'—the cost that reproducing workers impose on the colony as a whole—that determines how many are tolerated, according to the study.

Rob Hammond and Laurent Keller, both at the University of Lausanne's Department of Ecology and Evolution, carried out a metaanalysis on previously published data on 50 species of social Hymenoptera—colonial ants, bees, and wasps. These species have a haplodiploid genetic system, which results in extremely high levels of relatedness among workers. This means that a typical worker's long-term genetic prospects are usually better served by raising the queen's brood than by reproducing herself.

In most species, however, workers can lay haploid eggs, which develop into males—nephews to the other workers and grandsons to the queen. Destruction of these eggs by other workers—and in some species by the queen—is usually sufficient to ensure that the vast majority of adult males are the queen's offspring. Policing levels vary among species, and the source of this variation was the focus of Hammond and Keller's study.

The Swiss university pair points out that colony relatedness has often been used to explain differences in worker reproduction. "Kinship is obviously central to kin selection, and over the past 10 years, molecular techniques have allowed the rapid and accurate assessment of both kinship and parentage. Understandably, this has led to kinship being the focus of much research," Hammond told The Scientist.

However, their analysis found no evidence for relatedness as the determining factor in worker policing levels. Instead, they suggest that colony efficiency provides the key. "Our study looked for large-scale patterns, but at this scale, there is no relationship between relatedness and worker reproduction," said Hammond. "At a more local scale, however, there may be significant relationships between relatedness and worker reproduction.

Francis Ratnieks, who leads the Apiculture and Social Insect Laboratory at the University of Sheffield and who was the principle architect of the theory of insect worker policing, viewed the study's conclusions with caution. "The set of species used appears to be somewhat selective," he told The Scientist. "Some excellent studies have been left out of Hammond's and Keller's analysis, and at least one of the studies they use is almost certainly unreliable."

Ratnieks, who was not involved in the study, agreed that too much emphasis has previously been placed on relatedness and not enough on the costs of worker reproduction. "Many factors influence the production of males by workers, only one of which is relatedness," he said, welcoming the fact that the new study at least shifts the emphasis elsewhere. "Inclusive fitness is not simply determined by the mating system of the colony, but through numerous other variables too."

Koos Boomsma, at the University of Copenhagen agreed. "In principle, the data set used is defendable, although it's clear that other meaningful sources might have been missed. Hammond and Keller argue convincingly that some older studies were inaccurate, but that doesn't mean they all were," said Boomsma, who was not involved with the study. He also echoed Ratnieks' assertion, adding "there may well be no single explanation of male parentage conflict across the Hymenoptera."

David Queller, professor of evolutionary biology at Rice University, was intrigued by the new findings. "The main conclusion—that relatedness explains little or nothing about who produces males—is certainly interesting if it's true," said Queller, who was not involved with the study. "The authors rightly argue for the need to look at all aspects of kin selection, not just relatedness. Colony efficiency might be an important factor, but it's not the only plausible mechanism."

"Our work draws attention to the importance of costs and benefits of social actions," said Hammond, who said he is optimistic about future progress. "Measuring costs in kin selection is a lot more difficult than measuring relatedness. We hope that by highlighting the importance of costs, our work will inspire researchers to develop elegant and novel ways to test kin selection."