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Sexual selection drives weak positive selection in protamine genes and high promoter divergence, enhancing sperm competitiveness.

Martin-Coello J, Dopazo H, Arbiza L, Ausió J, Roldan ER, Gomendio M - Proc. Biol. Sci. (2009)

Bottom Line: In addition, sperm competition levels across all species are strongly associated with high divergence in protamine 2 promoters that, in turn, are associated with sperm swimming speed.Such phenotypic changes are adaptive because sperm swimming speed may be a major determinant of fertilization success under sperm competition.Thus, when species have diverged recently, few changes in gene-coding sequences are found, while high divergence in promoters seems to be associated with the intensity of sexual selection.

View Article: PubMed Central - PubMed

Affiliation: Reproductive Ecology and Biology Group, Museo Nacional de Ciencias Naturales (CSIC), c/José Gutiérrez Abascal 2, 28006 Madrid, Spain.

ABSTRACT
Phenotypic adaptations may be the result of changes in gene structure or gene regulation, but little is known about the evolution of gene expression. In addition, it is unclear whether the same selective forces may operate at both levels simultaneously. Reproductive proteins evolve rapidly, but the underlying selective forces promoting such rapid changes are still a matter of debate. In particular, the role of sexual selection in driving positive selection among reproductive proteins remains controversial, whereas its potential influence on changes in promoter regions has not been explored. Protamines are responsible for maintaining DNA in a compacted form in chromosomes in sperm and the available evidence suggests that they evolve rapidly. Because protamines condense DNA within the sperm nucleus, they influence sperm head shape. Here, we examine the influence of sperm competition upon protamine 1 and protamine 2 genes and their promoters, by comparing closely related species of Mus that differ in relative testes size, a reliable indicator of levels of sperm competition. We find evidence of positive selection in the protamine 2 gene in the species with the highest inferred levels of sperm competition. In addition, sperm competition levels across all species are strongly associated with high divergence in protamine 2 promoters that, in turn, are associated with sperm swimming speed. We suggest that changes in protamine 2 promoters are likely to enhance sperm swimming speed by making sperm heads more hydrodynamic. Such phenotypic changes are adaptive because sperm swimming speed may be a major determinant of fertilization success under sperm competition. Thus, when species have diverged recently, few changes in gene-coding sequences are found, while high divergence in promoters seems to be associated with the intensity of sexual selection.

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Related in: MedlinePlus

(a) Relationship between body weight and testes weight in murid rodents (r2=0.4463, n=32, p<0.0001). Open circles (our own data): 1, M. cookii; 2, M. famulus; 3, M. macedonicus; 4, M. m. bactrianus; 5, M. m. castaneus; 6, M. m. domesticus; 7, M. m. musculus; 8, M. pahari; 9, M. spicilegus; 10, M. spretus. Filled circles (data from Kenagy & Trombulak 1986): Apodemus agrarius, Apodemus flavicollis, Apodemus microps, A. sylvaticus, Micromys minutus, Notomys alexis, Notomys cervinus, Notomys fuscus, Notomys mitchelli, Praomys natalensis, Pseudomys apodemoides, Pseudomys australis, Pseudomys delicatulus, Pseudomys desertor, Pseudomys gracilicaudatus, Pseudomys hermannsburgensis, Pseudomys nanus, Pseudomys novaehollandiae, Pseudomys shortridgei, Rattus exulans, Rattus norvegicus, Rattus rattus. (b) Bayesian phylogenetic reconstruction of the 10 species of Mus. Note the low mean number of amino acid substitutions per site measured in the branches. Grey and black nodes represent clusters with 1.00 and 0.79 posterior probability values, respectively (table S1 in the electronic supplementary material).
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fig1: (a) Relationship between body weight and testes weight in murid rodents (r2=0.4463, n=32, p<0.0001). Open circles (our own data): 1, M. cookii; 2, M. famulus; 3, M. macedonicus; 4, M. m. bactrianus; 5, M. m. castaneus; 6, M. m. domesticus; 7, M. m. musculus; 8, M. pahari; 9, M. spicilegus; 10, M. spretus. Filled circles (data from Kenagy & Trombulak 1986): Apodemus agrarius, Apodemus flavicollis, Apodemus microps, A. sylvaticus, Micromys minutus, Notomys alexis, Notomys cervinus, Notomys fuscus, Notomys mitchelli, Praomys natalensis, Pseudomys apodemoides, Pseudomys australis, Pseudomys delicatulus, Pseudomys desertor, Pseudomys gracilicaudatus, Pseudomys hermannsburgensis, Pseudomys nanus, Pseudomys novaehollandiae, Pseudomys shortridgei, Rattus exulans, Rattus norvegicus, Rattus rattus. (b) Bayesian phylogenetic reconstruction of the 10 species of Mus. Note the low mean number of amino acid substitutions per site measured in the branches. Grey and black nodes represent clusters with 1.00 and 0.79 posterior probability values, respectively (table S1 in the electronic supplementary material).

Mentions: A phylogenetic tree was constructed using sequences available in GenBank for the species used in this study (table S1 in the electronic supplementary material). CDSs were aligned using translated protein sequences as templates by means of Muscle (Edgar 2004) and default parameters. Phylogenetic testing of the best nucleotide substitution model was done using Modeltest program (Posada & Crandall 1998). The ungapped number of characters ranged from 11 038 to 13 073 for M. m. domesticus, M. cookii, M. macedonicus, M. m. castaneus, M. m. musculus, M. spretus and M. spicilegus, from 4894 to 8397 for M. famulus, M. pahari and A. sylvaticus, and were 1645 for M. m. bactrianus. Maximum-likelihood and Bayesian analyses were run in PhyML (Guindon & Gascuel 2003) and MrBayes (Ronquist & Huelsenbeck 2003) programs according to the best-fit model of DNA. Convergence of the four Markov chains was obtained in 1 000 000 generations, and 500 samples out of 1000 were used to summarize the posterior probability of all the trees. Note that the species with the lower number of ungapped characters produces a polytomy with the lowest posterior probability value (0.79) observed in the tree (figure 1b).


Sexual selection drives weak positive selection in protamine genes and high promoter divergence, enhancing sperm competitiveness.

Martin-Coello J, Dopazo H, Arbiza L, Ausió J, Roldan ER, Gomendio M - Proc. Biol. Sci. (2009)

(a) Relationship between body weight and testes weight in murid rodents (r2=0.4463, n=32, p<0.0001). Open circles (our own data): 1, M. cookii; 2, M. famulus; 3, M. macedonicus; 4, M. m. bactrianus; 5, M. m. castaneus; 6, M. m. domesticus; 7, M. m. musculus; 8, M. pahari; 9, M. spicilegus; 10, M. spretus. Filled circles (data from Kenagy & Trombulak 1986): Apodemus agrarius, Apodemus flavicollis, Apodemus microps, A. sylvaticus, Micromys minutus, Notomys alexis, Notomys cervinus, Notomys fuscus, Notomys mitchelli, Praomys natalensis, Pseudomys apodemoides, Pseudomys australis, Pseudomys delicatulus, Pseudomys desertor, Pseudomys gracilicaudatus, Pseudomys hermannsburgensis, Pseudomys nanus, Pseudomys novaehollandiae, Pseudomys shortridgei, Rattus exulans, Rattus norvegicus, Rattus rattus. (b) Bayesian phylogenetic reconstruction of the 10 species of Mus. Note the low mean number of amino acid substitutions per site measured in the branches. Grey and black nodes represent clusters with 1.00 and 0.79 posterior probability values, respectively (table S1 in the electronic supplementary material).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2690471&req=5

fig1: (a) Relationship between body weight and testes weight in murid rodents (r2=0.4463, n=32, p<0.0001). Open circles (our own data): 1, M. cookii; 2, M. famulus; 3, M. macedonicus; 4, M. m. bactrianus; 5, M. m. castaneus; 6, M. m. domesticus; 7, M. m. musculus; 8, M. pahari; 9, M. spicilegus; 10, M. spretus. Filled circles (data from Kenagy & Trombulak 1986): Apodemus agrarius, Apodemus flavicollis, Apodemus microps, A. sylvaticus, Micromys minutus, Notomys alexis, Notomys cervinus, Notomys fuscus, Notomys mitchelli, Praomys natalensis, Pseudomys apodemoides, Pseudomys australis, Pseudomys delicatulus, Pseudomys desertor, Pseudomys gracilicaudatus, Pseudomys hermannsburgensis, Pseudomys nanus, Pseudomys novaehollandiae, Pseudomys shortridgei, Rattus exulans, Rattus norvegicus, Rattus rattus. (b) Bayesian phylogenetic reconstruction of the 10 species of Mus. Note the low mean number of amino acid substitutions per site measured in the branches. Grey and black nodes represent clusters with 1.00 and 0.79 posterior probability values, respectively (table S1 in the electronic supplementary material).
Mentions: A phylogenetic tree was constructed using sequences available in GenBank for the species used in this study (table S1 in the electronic supplementary material). CDSs were aligned using translated protein sequences as templates by means of Muscle (Edgar 2004) and default parameters. Phylogenetic testing of the best nucleotide substitution model was done using Modeltest program (Posada & Crandall 1998). The ungapped number of characters ranged from 11 038 to 13 073 for M. m. domesticus, M. cookii, M. macedonicus, M. m. castaneus, M. m. musculus, M. spretus and M. spicilegus, from 4894 to 8397 for M. famulus, M. pahari and A. sylvaticus, and were 1645 for M. m. bactrianus. Maximum-likelihood and Bayesian analyses were run in PhyML (Guindon & Gascuel 2003) and MrBayes (Ronquist & Huelsenbeck 2003) programs according to the best-fit model of DNA. Convergence of the four Markov chains was obtained in 1 000 000 generations, and 500 samples out of 1000 were used to summarize the posterior probability of all the trees. Note that the species with the lower number of ungapped characters produces a polytomy with the lowest posterior probability value (0.79) observed in the tree (figure 1b).

Bottom Line: In addition, sperm competition levels across all species are strongly associated with high divergence in protamine 2 promoters that, in turn, are associated with sperm swimming speed.Such phenotypic changes are adaptive because sperm swimming speed may be a major determinant of fertilization success under sperm competition.Thus, when species have diverged recently, few changes in gene-coding sequences are found, while high divergence in promoters seems to be associated with the intensity of sexual selection.

View Article: PubMed Central - PubMed

Affiliation: Reproductive Ecology and Biology Group, Museo Nacional de Ciencias Naturales (CSIC), c/José Gutiérrez Abascal 2, 28006 Madrid, Spain.

ABSTRACT
Phenotypic adaptations may be the result of changes in gene structure or gene regulation, but little is known about the evolution of gene expression. In addition, it is unclear whether the same selective forces may operate at both levels simultaneously. Reproductive proteins evolve rapidly, but the underlying selective forces promoting such rapid changes are still a matter of debate. In particular, the role of sexual selection in driving positive selection among reproductive proteins remains controversial, whereas its potential influence on changes in promoter regions has not been explored. Protamines are responsible for maintaining DNA in a compacted form in chromosomes in sperm and the available evidence suggests that they evolve rapidly. Because protamines condense DNA within the sperm nucleus, they influence sperm head shape. Here, we examine the influence of sperm competition upon protamine 1 and protamine 2 genes and their promoters, by comparing closely related species of Mus that differ in relative testes size, a reliable indicator of levels of sperm competition. We find evidence of positive selection in the protamine 2 gene in the species with the highest inferred levels of sperm competition. In addition, sperm competition levels across all species are strongly associated with high divergence in protamine 2 promoters that, in turn, are associated with sperm swimming speed. We suggest that changes in protamine 2 promoters are likely to enhance sperm swimming speed by making sperm heads more hydrodynamic. Such phenotypic changes are adaptive because sperm swimming speed may be a major determinant of fertilization success under sperm competition. Thus, when species have diverged recently, few changes in gene-coding sequences are found, while high divergence in promoters seems to be associated with the intensity of sexual selection.

Show MeSH
Related in: MedlinePlus