Contributions to Zoology, 84 (3) – 2015Camille Meslin; Michel Laurin; Isabelle Callebaut; Xavier Druart; Philippe Monget: Evolution of species-specific major seminal fluid proteins in placental mammals by gene death and positive selection

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Adams TE, Hockin MF, Mann KG, Everse SJ. 2004. The crystal structure of activated protein C-inactivated bovine factor Va: Implications for cofactor function. Proceedings of the National Academy of Sciences of the United States of America 101: 8918-8923.

Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic acids research 25: 3389-3402.

Andrés JA, Maroja LS, Bogdanowicz SM, Swanson WJ, Harrison RG. 2006. Molecular evolution of seminal proteins in field crickets. Molecular Biology and Evolution 23: 1574-1584.

Batruch I, Lecker I, Kagedan D, Smith CR, Mullen BJ, Grober E, Lo KC, Diamandis EP, Jarvi KA. 2011. Proteomic analysis of seminal plasma from normal volunteers and post-vasectomy patients identifies over 2000 proteins and candidate biomarkers of the urogenital system. Journal of proteome research 10: 941-953.

Bax B, Blundell TL, Murray-Rust J, McDonald NQ. 1997. Structure of mouse 7S NGF: a complex of nerve growth factor with four binding proteins. Structure 5: 1275-1285.

Begun DJ, Lindfors HA. 2005. Rapid evolution of genomic Acp complement in the melanogaster subgroup of Drosophila. Molecular Biology and Evolution 22: 2010-2021.

Begun DJ, Lindfors HA, Thompson ME, Holloway AK. 2006. Recently evolved genes identified from Drosophila yakuba and D. erecta accessory gland expressed sequence tags. Genetics 172: 1675-1681.

Belleannée C, Labas V, Teixeira-Gomes A-P, Gatti JL, Dacheux J-L, Dacheux F. 2011. Identification of luminal and secreted proteins in bull epididymis. Journal of proteomics 74: 59-78.

Bennett-Lovsey RM, Herbert AD, Sternberg MJ, Kelley LA. 2008. Exploring the extremes of sequence/structure space with ensemble fold recognition in the program Phyre. Proteins: Structure, Function, and Bioinformatics 70: 611-625.

Burtnick LD, Urosev D, Irobi E, Narayan K, Robinson RC. 2004. Structure of the N-terminal half of gelsolin bound to actin: roles in severing, apoptosis and FAF. The EMBO journal 23: 2713-2722.

Busset J, Cabau C, Meslin C, Pascal G. 2011. PhyleasProg: a user-oriented web server for wide evolutionary analyses. Nucleic acids research 39: W479-W485.

Callebaut I, Labesse G, Durand P, Poupon A, Canard L, Chomilier J, Henrissat B, Mornon J. 1997. Deciphering protein sequence information through hydrophobic cluster analysis (HCA): current status and perspectives. Cellular and Molecular Life Sciences CMLS 53: 621-645.

Carvalho AL, Sanz L, Barettino D, Romero A, Calvete JJ, Romão MJ. 2002. Crystal structure of a prostate kallikrein isolated from stallion seminal plasma: a homologue of human PSA. Journal of molecular biology 322: 325-337.

Castella S, Fouchécourt S, Teixeira-Gomes AP, Vinh J, Belghazi M, Dacheux F, Dacheux J-L. 2004. Identification of a member of a new RNase a family specifically secreted by epididymal caput epithelium. Biology of reproduction 70: 319-328.

Chapman T, Arnqvist G, Bangham J, Rowe L. 2003. Sexual conflict. Trends in Ecology & Evolution 18: 41-47.

Chapman T, Davies SJ. 2004. Functions and analysis of the seminal fluid proteins of male Drosophila melanogaster fruit flies. Peptides 25: 1477-1490.

Cho S, Beintema JJ, Zhang J. 2005. The ribonuclease A superfamily of mammals and birds: identifying new members and tracing evolutionary histories. Genomics 85: 208-220.

Civetta A, Clark AG. 2000. Correlated effects of sperm competition and postmating female mortality. Proceedings of the National Academy of Sciences 97: 13162-13165.

Clark AG, Begun DJ, Prout T. 1999. Female× male interactions in Drosophila sperm competition. Science 283: 217-220.

Clark NL, Swanson WJ. 2005. Pervasive adaptive evolution in primate seminal proteins. PLoS Genetics 1: e35.

Dean MD, Findlay GD, Hoopmann MR, Wu CC, MacCoss MJ, Swanson WJ, Nachman MW. 2011. Identification of ejaculated proteins in the house mouse (Mus domesticus) via isotopic labeling. BMC genomics 12: 306.

Dorus S, Evans PD, Wyckoff GJ, Choi SS, Lahn BT. 2004. Rate of molecular evolution of the seminal protein gene SEMG2 correlates with levels of female promiscuity. Nature genetics 36: 1326-1329.

Druart X, Rickard J, Mactier S, Kohnke P, Kershaw-Young C, Bathgate R, Gibb Z, Crossett B, Tsikis G, Labas V. 2013. Proteomic characterization and cross species comparison of mammalian seminal plasma. Journal of proteomics 91: 13-22.

Drummond DA, Bloom JD, Adami C, Wilke CO, Arnold FH. 2005. Why highly expressed proteins evolve slowly. Proceedings of the National Academy of Sciences of the United States of America 102: 14338-14343.

Faith DP. 1992. Conservation evaluation and phylogenetic diversity. Biological Conservation 61: 1-10.

Felsenstein J. 1985. Phylogenies and the comparative method. American Naturalist: 1-15.

Findlay GD, MacCoss MJ, Swanson WJ. 2009. Proteomic discovery of previously unannotated, rapidly evolving seminal fluid genes in Drosophila. Genome research 19: 886-896.

Fornůsková A, Vinkler M, Pagès M, Galan M, Jousselin E, Cerqueira F, Morand S, Charbonnel N, Bryja J, Cosson J-F. 2013. Contrasted evolutionary histories of two Toll-like receptors (Tlr4 and Tlr7) in wild rodents (MURINAE). BMC evolutionary biology 13: 194.

Galindo BE, Vacquier VD, Swanson WJ. 2003. Positive selection in the egg receptor for abalone sperm lysin. Proceedings of the National Academy of Sciences 100: 4639-4643.

Hassanin A, Delsuc F, Ropiquet A, Hammer C, van Vuuren BJ, Matthee C, Ruiz-Garcia M, Catzeflis F, Areskoug V, Nguyen TT. 2012. Pattern and timing of diversification of Cetartiodactyla (Mammalia, Laurasiatheria), as revealed by a comprehensive analysis of mitochondrial genomes. Comptes rendus biologies 335: 32-50.

Holland B, Rice WR. 1999. Experimental removal of sexual selection reverses intersexual antagonistic coevolution and removes a reproductive load. Proceedings of the National Academy of Sciences 96: 5083-5088.

Hurle B, Swanson W, Green ED. 2007. Comparative sequence analyses reveal rapid and divergent evolutionary changes of the WFDC locus in the primate lineage. Genome research 17: 276-286.

Jensen-Seaman MI, Li W-H. 2003. Evolution of the hominoid semenogelin genes, the major proteins of ejaculated semen. Journal of molecular evolution 57: 261-270.

Josse S, Moreau T, Laurin M. 2006. Stratigraphic tools for Mesquite. See

Karn RC, Clark NL, Nguyen ED, Swanson WJ. 2008. Adaptive evolution in rodent seminal vesicle secretion proteins. Molecular Biology and Evolution 25: 2301-2310.

Kelly VC, Kuy S, Palmer DJ, Xu Z, Davis SR, Cooper GJ. 2006. Characterization of bovine seminal plasma by proteomics. Proteomics 6: 5826-5833.

LaPatra SE, Evilia C, Winston V. 2008. Positively selected sites on the surface glycoprotein (G) of infectious hematopoietic necrosis virus. Journal of general virology 89: 703-708.

Maddison WP. 2000. Testing character correlation using pairwise comparisons on a phylogeny. Journal of Theoretical Biology 202: 195-204.

Maddison WP, Maddison DR. 2015. Mesquite: a modular system for evolutionary analysis. Version 3.02.

Marques PI, Bernardino R, Fernandes T, Green ED, Hurle B, Quesada V, Seixas S. 2012. Birth-and-death of KLK3 and KLK2 in primates: evolution driven by reproductive biology. Genome biology and evolution 4: 1331-1338.

Marshall JL, Huestis DL, Garcia C, Hiromasa Y, Wheeler S, Noh S, Tomich JM, Howard DJ. 2011. Comparative proteomics uncovers the signature of natural selection acting on the ejaculate proteomes of two cricket species isolated by postmating, prezygotic phenotypes. Molecular Biology and Evolution 28: 423-435.

Martí-Renom MA, Stuart AC, Fiser A, Sánchez R, Melo F, Šali A. 2000. Comparative protein structure modeling of genes and genomes. Annual review of biophysics and biomolecular structure 29: 291-325.

Meslin C, Brimau F, Meillour PN, Callebaut I, Pascal G, Monget P. 2011. The evolutionary history of the SAL1 gene family in eutherian mammals. BMC evolutionary biology 11: 148.

Meslin C, Mugnier S, Callebaut I, Laurin M, Pascal G, Poupon A, Goudet G, Monget P. 2012. Evolution of genes involved in gamete interaction: evidence for positive selection, duplications and losses in vertebrates. PloS one 7: e44548.

Midford P, Garland Jr T, Maddison W. 2008. PDAP package of Mesquite, version 1.16. See

Milardi D, Grande G, Vincenzoni F, Messana I, Pontecorvi A, De Marinis L, Castagnola M, Marana R. 2012. Proteomic approach in the identification of fertility pattern in seminal plasma of fertile men. Fertility and sterility 97: 67-73. e61.

Moura AA, Chapman DA, Koc H, Killian GJ. 2007. A comprehensive proteomic analysis of the accessory sex gland fluid from mature Holstein bulls. Animal reproduction science 98: 169-188.

Mueller JL, Ram KR, McGraw LA, Qazi MB, Siggia ED, Clark AG, Aquadro CF, Wolfner MF. 2005. Cross-species comparison of Drosophila male accessory gland protein genes. Genetics 171: 131-143.

Murphy WJ, Eizirik E. 2009. Placental mammals (Eutheria). In: Hedges SB, S. K, editors. The timetree of life. New York: Oxford Univeristy Press. p. 474-474.

Nag S, Ma Q, Wang H, Chumnarnsilpa S, Lee WL, Larsson M, Kannan B, Hernandez-Valladares M, Burtnick LD, Robinson RC. 2009. Ca2+ binding by domain 2 plays a critical role in the activation and stabilization of gelsolin. Proceedings of the National Academy of Sciences 106: 13713-13718.

Nielsen R, Yang Z. 1998. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148: 929-936.

Pagel M. 1994. Detecting correlated evolution on phylogenies: a general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London. Series B: Biological Sciences 255: 37-45.

Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSF Chimera—a visualization system for exploratory research and analysis. Journal of computational chemistry 25: 1605-1612.

Pilch B, Mann M. 2006. Large-scale and high-confidence proteomic analysis of human seminal plasma. Genome biology 7: R40.

Poiani A. 2006. Complexity of seminal fluid: a review. Behavioral Ecology and Sociobiology 60: 289-310.

Pond SLK, Murrell B, Fourment M, Frost SD, Delport W, Scheffler K. 2011. A random effects branch-site model for detecting episodic diversifying selection. Molecular Biology and Evolution: msr125.

Ramm SA, McDonald L, Hurst JL, Beynon RJ, Stockley P. 2009. Comparative proteomics reveals evidence for evolutionary diversification of rodent seminal fluid and its functional significance in sperm competition. Molecular Biology and Evolution 26: 189-198.

Ramm SA, Oliver PL, Ponting CP, Stockley P, Emes RD. 2008. Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Molecular Biology and Evolution 25: 207-219.

Raymond A, Ensslin MA, Shur BD. 2009. SED1/MFG-E8: A Bi-Motif protein that orchestrates diverse cellular interactions. Journal of cellular biochemistry 106: 957-966.

Rees GN, Baldwin DS, Watson GO, Perryman S, Nielsen DL. 2005. Ordination and significance testing of microbial community composition derived from terminal restriction fragment length polymorphisms: application of multivariate statistics. Antonie van Leeuwenhoek 86: 339-347.

Rice WR. 1996. Sexually antagonistic male adaptation triggered by experimental arrest of female evolution. Nature 381: 232-234.

Rodrigues M, Souza C, Martins J, Rego J, Oliveira J, Domont G, Nogueira F, Moura A. 2013. Seminal plasma proteins and their relationship with sperm motility in Santa Ines rams. Small Ruminant Research 109: 94-100.

Rowe KC, Reno ML, Richmond DM, Adkins RM, Steppan SJ. 2008. Pliocene colonization and adaptive radiations in Australia and New Guinea (Sahul): Multilocus systematics of the old endemic rodents (Muroidea: Murinae). Molecular phylogenetics and evolution 47: 84-101.

Shao C, Novakovic VA, Head JF, Seaton BA, Gilbert GE. 2008. Crystal structure of lactadherin C2 domain at 1.7 Å resolution with mutational and computational analyses of its membrane-binding motif. Journal of Biological Chemistry 283: 7230-7241.

Souza CEA, Rego J, Lobo CH, Oliveira JTA, Nogueira F, Domont GB, Fioramonte M, Gozzo FC, Moreno FB, Monteiro-Moreira A. 2012. Proteomic analysis of the reproductive tract fluids from tropically-adapted Santa Ines rams. J Proteomics 75: 4436-4456.

Stoline MR. 1981. The status of multiple comparisons: simultaneous estimation of all pairwise comparisons in one-way ANOVA designs. The American Statistician 35: 134-141.

Storey JD, Tibshirani R. 2003. Statistical significance for genomewide studies. Proceedings of the National Academy of Sciences 100: 9440-9445.

Suyama M, Torrents D, Bork P. 2006. PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic acids research 34: W609-W612.

Swanson WJ, Clark AG, Waldrip-Dail HM, Wolfner MF, Aquadro CF. 2001. Evolutionary EST analysis identifies rapidly evolving male reproductive proteins in Drosophila. Proceedings of the National Academy of Sciences 98: 7375-7379.

Swanson WJ, Nielsen R, Yang Q. 2003. Pervasive adaptive evolution in mammalian fertilization proteins. Molecular Biology and Evolution 20: 18-20.

Swanson WJ, Wong A, Wolfner MF, Aquadro CF. 2004. Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection. Genetics 168: 1457-1465.

Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic acids research 22: 4673-4680.

Tian X, Pascal G, Fouchécourt S, Pontarotti P, Monget P. 2009. Gene birth, death, and divergence: the different scenarios of reproduction-related gene evolution. Biology of reproduction 80: 616-621.

Vignaud P, Duringer P, Mackaye HT, Likius A, Blondel C, Boisserie J-R, De Bonis L, Eisenmann V, Etienne M-E, Geraads D. 2002. Geology and palaeontology of the Upper Miocene Toros-Menalla hominid locality, Chad. Nature 418: 152-155.

Wagstaff BJ, Begun DJ. 2007. Adaptive evolution of recently duplicated accessory gland protein genes in desert Drosophila. Genetics 177: 1023-1030.

Wagstaff BJ, Begun DJ. 2005a. Comparative genomics of accessory gland protein genes in Drosophila melanogaster and D. pseudoobscura. Molecular Biology and Evolution 22: 818-832.

Wagstaff BJ, Begun DJ. 2005b. Molecular population genetics of accessory gland protein genes and testis-expressed genes in Drosophila mojavensis and D. arizonae. Genetics 171: 1083-1101.

Walters JR, Harrison RG. 2010. Combined EST and proteomic analysis identifies rapidly evolving seminal fluid proteins in Heliconius butterflies. Molecular Biology and Evolution 27: 2000-2013.

Wolfner M. 2002. The gifts that keep on giving: physiological functions and evolutionary dynamics of male seminal proteins in Drosophila. Heredity 88: 85-93.

Wong WS, Yang Z, Goldman N, Nielsen R. 2004. Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites. Genetics 168: 1041-1051.

Yang Z. 2000. Maximum likelihood estimation on large phylogenies and analysis of adaptive evolution in human influenza virus A. Journal of molecular evolution 51: 423-432.

Yang Z. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution 24: 1586-1591.

Yang Z, Nielsen R. 2002. Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Molecular Biology and Evolution 19: 908-917.

Yang Z, Wong WS, Nielsen R. 2005. Bayes empirical Bayes inference of amino acid sites under positive selection. Molecular Biology and Evolution 22: 1107-1118.

Zhang J, Nielsen R, Yang Z. 2005. Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Molecular Biology and Evolution 22: 2472-2479.