Maximum-likelihood analysis of molecular adaptation in abalone sperm lysin reveals variable selective pressures among lineages and sites.

Maximum-likelihood models of codon substitution were used to analyze sperm lysin genes of 25 abalone (HALIOTIS:) species to identify lineages and amino acid sites under diversifying selection. The models used the nonsynonymous/synonymous rate ratio (omega = d(N)/d(S)) as an indicator of selective pressure and allowed the ratio to vary among lineages or sites. Likelihood ratio tests suggested significant variation in selective pressure among lineages. The variable selective pressure provided an explanation for the previous observation that the omega ratio is >1 in comparisons of closely related species and <1 in comparisons of distantly related species. Computer simulations demonstrated that saturation of nonsynonymous substitutions and constraint on lysin structure were unlikely to account for the observed pattern. Lineages linking closely related sympatric species appeared to be under diversifying selection, while lineages separating distantly related species from different geographic locations were associated with low evolutionary rates. The selective pressure indicated by the omega ratio was found to vary greatly among amino acid sites in lysin. Sites under potential diversifying selection were identified. Ancestral lysins were inferred to trace the route of evolution at individual sites and to provide lysin sequences for future laboratory studies.

[1]  M. Hellberg,et al.  Rapid evolution of fertilization selectivity and lysin cDNA sequences in teguline gastropods. , 1999, Molecular biology and evolution.

[2]  S. Fabry,et al.  Rapid evolution of sex-related genes in Chlamydomonas. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[3]  C D Stout,et al.  1.35 and 2.07 A resolution structures of the red abalone sperm lysin monomer and dimer reveal features involved in receptor binding. , 2000, Acta crystallographica. Section D, Biological crystallography.

[4]  W. Swanson,et al.  Acrosomal Proteins of Abalone Spermatozoa , 1999 .

[5]  N. Goldman,et al.  A codon-based model of nucleotide substitution for protein-coding DNA sequences. , 1994, Molecular biology and evolution.

[6]  S. Palumbi,et al.  Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra). , 1991, Molecular biology and evolution.

[7]  T. Ohta Slightly Deleterious Mutant Substitutions in Evolution , 1973, Nature.

[8]  J. Elder,et al.  Concerted Evolution of Repetitive DNA Sequences in Eukaryotes , 1995, The Quarterly Review of Biology.

[9]  C. Wu,et al.  Positive selection and the molecular evolution of a gene of male reproduction, Acp26Aa of Drosophila. , 1997, Molecular biology and evolution.

[10]  A. Civetta,et al.  Sex-related genes, directional sexual selection, and speciation. , 1998, Molecular biology and evolution.

[11]  T. Dobzhansky Speciation as a Stage in Evolutionary Divergence , 1940, The American Naturalist.

[12]  C. Biermann The molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae). , 1998, Molecular biology and evolution.

[13]  N. Goldman,et al.  Codon-substitution models for heterogeneous selection pressure at amino acid sites. , 2000, Genetics.

[14]  Gerald J. Wyckoff,et al.  Rapid evolution of male reproductive genes in the descent of man , 2000, Nature.

[15]  D. McRee,et al.  The crystal structure of lysin, a fertilization protein. , 1993, Science.

[16]  S. Palumbi,et al.  Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin. , 1996, Molecular biology and evolution.

[17]  Z. Yang,et al.  Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. , 2000, Molecular biology and evolution.

[18]  T. Ota,et al.  Positive selection is a general phenomenon in the evolution of abalone sperm lysin. , 1995, Molecular biology and evolution.

[19]  Ziheng Yang,et al.  Phylogenetic Analysis by Maximum Likelihood (PAML) , 2002 .

[20]  C. Stout,et al.  The high resolution crystal structure of green abalone sperm lysin: implications for species-specific binding of the egg receptor. , 2000, Journal of molecular biology.

[21]  V. Vacquier,et al.  Evolution and systematics in Haliotidae (Mollusca: Gastropoda): inferences from DNA sequences of sperm lysin , 1995 .

[22]  A. Shaw,et al.  Crystal structure and subunit dynamics of the abalone sperm lysin dimer: egg envelopes dissociate dimers, the monomer is the active species , 1995, The Journal of cell biology.

[23]  Z. Yang,et al.  Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. , 1998, Molecular biology and evolution.

[24]  W. Swanson,et al.  Concerted evolution in an egg receptor for a rapidly evolving abalone sperm protein. , 1998, Science.

[25]  M. Hellberg,et al.  Positive selection and propeptide repeats promote rapid interspecific divergence of a gastropod sperm protein. , 2000, Molecular biology and evolution.

[26]  S. Palumbi Genetic Divergence, Reproductive Isolation, and Marine Speciation , 1994 .

[27]  M. Nei,et al.  Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. , 1986, Molecular biology and evolution.

[28]  M. Nei,et al.  A new method of inference of ancestral nucleotide and amino acid sequences. , 1995, Genetics.

[29]  W. Swanson,et al.  Extraordinary divergence and positive Darwinian selection in a fusagenic protein coating the acrosomal process of abalone spermatozoa. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[30]  V. Vacquier,et al.  Abalone sperm lysin: unusual mode of evolution of a gamete recognition protein , 1993, Zygote.

[31]  R. Nielsen,et al.  Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. , 1998, Genetics.

[32]  V. Vacquier,et al.  Nonsynonymous substitution in abalone sperm fertilization genes exceeds substitution in introns and mitochondrial DNA. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[33]  V. Vacquier,et al.  Interspecies chimeric sperm lysins identify regions mediating species-specific recognition of the abalone egg vitelline envelope. , 1999, Developmental biology.