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MBE Advance Access published online on June 14, 2006
Molecular Biology and Evolution, doi:10.1093/molbev/msl035
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© The Author 2006. 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@oxfordjournals.org
Accepted May 19, 2006

Research Article

Adaptive Evolution of Fertilization Proteins within a Genus: Variation in ZP2 and ZP3 in Deer Mice (Peromyscus)

Leslie M. Turner 1 * and Hopi E. Hoekstra 1

1 Division of Biological Sciences, University of California, San Diego, La Jolla, CA 92093-0116

* To whom correspondence should be addressed.
Leslie M. Turner, E-mail: lturner{at}biomail.ucsd.edu


  Abstract

Rapid evolution of reproductive proteins has been documented in a wide variety of taxa. In internally fertilized species, knowledge about the evolutionary dynamics of these proteins between closely related taxa is primarily limited to accessory gland proteins in the semen of Drosophila. Investigation of additional taxa and functional classes of proteins is necessary in order to determine if there is a general pattern of adaptive evolution of reproductive proteins between recently diverged species. We performed an evolutionary analysis of two egg coat proteins, ZP2 and ZP3, in fifteen species of deer mice (genus Peromyscus). Both of these proteins are involved in egg-sperm binding, a critical step in maintaining species-specific fertilization. Here, we show that Zp2 and Zp3 gene trees are not consistent with trees based on non-reproductive genes, Mc1r and Lcat, where species formed monophyletic clades. In fact, for both of the reproductive genes, intraspecific amino acid variation was extensive and alleles were sometimes shared across species. We document positive selection acting on ZP2 and ZP3 and identify specific amino acid sites that are likely targets of selection using both maximum likelihood approaches and patterns of parallel amino acid change. In ZP3, positively selected sites are clustered in and around the region implicated in sperm binding in Mus, suggesting changes may impact egg-sperm binding and fertilization potential. Finally, we identify lineages with significantly elevated rates of amino acid substitution using a Bayesian mapping approach. These findings demonstrate that the pattern of adaptive reproductive protein evolution found at higher taxonomic levels can be documented between closely related mammalian species, where reproductive isolation has evolved recently.

Keywords: adaptive evolution; fertilization; Peromyscus; positive selection; reproductive isolation; reproductive proteins.
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