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MBE Advance Access published online on February 12, 2004
Molecular Biology and Evolution, doi:10.1093/molbev/msh071
Molecular Biology and Evolution © Society for Molecular Biology and Evolution 2004; all rights reserved
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Accepted December 2, 2003
© 2004 Society for Molecular Biology and Evolution

Original Articles

Adaptive Evolution of Sperm Bindin Tracks Egg Incompatibility in Neotropical Sea Urchins of the Genus Echinometra

Michael A. McCartney 1* and H. A. Lessios 1

1 Smithsonian Tropical Research Institute, Box 2072, Balboa, Republic of Panama

* To whom correspondence should be addressed. E-mail: McCartneyM{at}uncw.edu.


  Abstract

Bindin is a gamete recognition protein known to control species-specific sperm-egg adhesion and membrane fusion in sea urchins. Previous analyses have shown that diversifying selection on bindin amino acid sequence is found when gametically incompatible species are compared, but not when species are compatible. The present study analyzes bindin polymorphism and divergence in the three closely related species of Echinometra in Central America: E. lucunter and E. viridis from the Caribbean, and E. vanbrunti from the eastern Pacific. The eggs of E. lucunter have evolved a strong block to fertilization by sperm of its neotropical congeners, whereas those of the other two species have not. As in the Indo-West Pacific (IWP) Echinometra, the neotropical species show high intraspecific bindin polymorphism in the same gene regions as in the IWP species. Maximum Likelihood analysis shows that many of the polymorphic codon sites are under mild positive selection. Of the fixed amino acid replacements, most have accumulated along the bindin lineage of E. lucunter. We analyzed the data with maximum likelihood models of variation in positive selection across lineages and codon sites, and with models that consider sites and lineages simultaneously. Our results show that positive selection is concentrated along the E. lucunter bindin lineage, and that codon sites with amino acid replacements fixed in this species show by far the highest signal of positive selection. Lineage-specific positive selection paralleling egg incompatibility provides support that adaptive evolution of sperm proteins acts to maintain recognition of bindin by changing egg receptors. Because both egg incompatibility and bindin divergence are greater between allopatric than between sympatric species, the hypothesis of selection against hybridization (reinforcement) cannot explain why adaptive evolution has been confined to a single lineage in the American Echinometra. Instead, processes acting to varying degrees within species (e.g. sperm competition, sexual selection, and sexual conflict) are more promising explanations for lineage-specific positive selection on bindin.

Key Words: gamete recognition, sea urchin, bindin, speciation, Echinometra


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