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MBE Advance Access published online on March 9, 2005

Molecular Biology and Evolution, doi:10.1093/molbev/msi133
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© The Author 2005. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved. For permissions, please e-mail: journals.permissions@oupjournals.org
Accepted February 28, 2005

Research Article

Sociality and the Rate of Molecular Evolution

Lindell Bromham 1* and Remko Leys 2

1 Centre for the Study of Evolution, School of Life Sciences, University of Sussex, Falmer, Brighton BN1 9QG, UNITED KINGDOM; Department of ZEN (Zoology and Entomology), University of Queensland, Brisbane 4072, AUSTRALIA
2 Evolutionary Biology Unit, South Australian Museum, Adelaide 5000, and Adelaide University, South Australia, AUSTRALIA

* To whom correspondence should be addressed.
Lindell Bromham, E-mail: L.D.Bromham{at}sussex.ac.uk


   Abstract

The molecular clock does not tick at a uniform rate in all taxa, but may be influenced by species characteristics. Eusocial species (those with reproductive division of labour) have been predicted to have faster rates of molecular evolution than their non-social relatives because of greatly reduced population size: if most individuals in a population are non-reproductive and only one or few queens produce all of the offspring, then eusocial animals could have much lower effective population sizes than their solitary relatives, which should increase the substitution of "nearly neutral" mutations. An earlier study reported faster rates in eusocial honey bees and vespid wasps, but failed to correct for phylogenetic non-independence or to distinguish between potential causes of rate variation. Because sociality has evolved independently in many different lineages, it is possible to conduct a more wide-ranging study to test the generality of the relationship. We have conducted a comparative analysis of 25 phylogenetically-independent pairs of social lineages and their non-social relatives, including bees, wasps, ants, termites, shrimps and molerats, using a range of available DNA sequences (mitochondrial and nuclear DNA coding for proteins and RNAs, and non-translated sequences). By including a wide range of social taxa we were able to test whether there is a general influence of sociality on rates of molecular evolution, and to test specific predictions of the hypothesis: (i) that social species have faster rates because they have reduced effective population sizes; (ii) that mitochondrial genes would show a greater effect of sociality than nuclear genes; and (iii) that rates of molecular evolution should be correlated with the degree of sociality. We find no consistent pattern in rates of molecular evolution between social and non-social lineages, and no evidence that mitochondrial genes show faster rates in social taxa. However, we show that the most highly eusocial hymenoptera do have faster rates than their non-social relatives. We also find that social parasites (that utilize the workers from related species to produce their own offspring) have faster rates than their social relatives, which is consisted with an effect of lower effective population size on rate of molecular evolution. Our results illustrate the importance of allowing for phylogenetic non-independence when conducting investigations of determinants of variation in rate of molecular evolution.

Keywords: eusocial; substitution rate; nearly neutral theory; molecular clock; effective population size; comparative method.
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