A higher male susceptibility to disease has helped shape the evolution of social insect behavior

What might be called the "sick-male" theory has been proposed by animal behaviorists Sean O'Donnell of the University of Washington and Samuel Beshers of the University of Illinois at Urbana-Champaign, and appears in the current issue of Proceedings Biological Sciences, published by the Royal Society of London.

Among behaviors possibly affected are the division of labor between males and females and the relative social isolation experienced by males in many social insect colonies.

The researchers looked at Hymenoptera, an order of insects, including bees, ants and wasps, some of which have highly complicated societies and an unusual genetic makeup. These insects are called haplodiploids because males and females have a different number of sets of chromosomes. The females, like most animals, including humans, are diploid and have two sets of chromosomes, one from each parent. Hymenopteran males, however, hatch from unfertilized eggs and are haploids with just one set of chromosomes.

"Disease and infections are a very powerful and ongoing force in natural selection, and natural selection should favor individuals that possess forms of genes, or alleles, that make them more resistant to infection," said O'Donnell, a UW associate professor of psychology. "In some cases, an individual that has more than one form of a gene can ward off more parasites. In humans, for example, there are different forms of a blood gene that can help ward off malaria parasites. People with two different alleles for this gene are more resistant to malaria."

Because they are haploid, Hymenopteran males can't have alternate forms of any genes, or in other words, individual males have no genetic variability. This, O'Donnell and Beshers contend, puts males at a higher susceptibility to disease.

The researchers, who are trying to understand the basis of social behavior in these creatures, suggest that this male vulnerability has shaped certain behaviors in social insect colonies. These behaviors, they say, are designed to minimize the risk of disease transmission in a colony.

Division of labor is a prime example. While colonies vary widely in the total number of individuals, females vastly outnumber males and seem to do most of the work.

"Males typically do not do very much work for their colonies," said O'Donnell. "In some instances males do small amounts of labor inside the nest. But they rarely are allowed outside of the nest and they do not forage for food or building materials, activities that might expose them to disease pathogens.

"If males were exposed to disease we would expect females to avoid, and possibly to attack and kill those males to minimize disease being brought into the colony."

The sick-male theory proposes that female-biased societies, and differences in male and female behavior, may be responses to higher risks of infection to males, he said. The theory also predicts that in some cases males may be segregated or shunned inside the nest, again to reduce the colony’s potential exposure to disease.

O'Donnell said much research still needs to be done to support the sick-male model and test whether males are less resistant to disease than females.

"We hope our study will inspire scientists to these ideas. Researchers need to challenge different species of social insects with disease pathogens to see whether males and females differ in disease resistance," he said. "Our understanding of the genetic basis of disease resistance is pretty weak, even medically. There actually is little evidence to show how genetic variability at the individual level is effective in fighting off disease, even though this is often assumed to be the case by biologists."

The National Science Foundation funded the research.

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