The egg coat zona pellucida 3 glycoprotein – evolution of its putative sperm-binding region in Old World murine rodents (Rodentia: Muridae)
Christine A. Swann A D , Steven J. B. Cooper B C D and William G. Breed A C D
+ Author Affiliations
- Author Affiliations
A Discipline of Anatomy and Pathology, Medical School, and Robinson Research Institute, Faculty of Health Sciences, The University of Adelaide, SA 5005, Australia.
B Evolutionary Biology Unit, South Australian Museum, North Terrace, Adelaide, SA 5000, Australia.
C Australian Centre for Evolutionary Biology and Biodiversity, The University of Adelaide, SA 5005, Australia.
D School of Biological Sciences, Faculty of Sciences, The University of Adelaide, SA 5005, Australia.
E Corresponding author. Email: bill.breed@adelaide.edu.au
Reproduction, Fertility and Development 29(12) 2376-2386 https://doi.org/10.1071/RD16455
Submitted: 14 November 2016 Accepted: 26 March 2017 Published: 13 April 2017
Abstract
In eutherian mammals, before fertilisation can occur the spermatozoon has to bind to, and penetrate, the egg coat, the zona pellucida (ZP). In the laboratory mouse there is good evidence that the primary sperm-binding site is a protein region encoded by Exon 7 of the ZP3 gene and it has been proposed that binding is species specific and evolves by sexual selection. In the present study we investigate these hypotheses by comparing Exon 6 and 7 sequences of ZP3 in 28 species of murine rodents of eight different divisions from Asia, Africa and Australasia, in which a diverse array of sperm morphologies occurs. We found considerable nucleotide (and corresponding amino acid) sequence divergence in Exon 7, but not in Exon 6, across these species, with evidence for positive selection at five codon positions. This molecular divergence does not appear to be due to reinforcement to reduce hybridisation, nor does it correlate with divergence in sperm head morphology or tail length, thus it is unlikely to be driven by inter-male sperm competition. Other forms of post-copulatory sexual selection therefore appear to have resulted in the molecular divergence of this region of ZP3 in this highly speciose group of mammals.
Additional keywords: mouse egg coat, positive selection, spermatozoa binding.
References
Akatsuka, K., Yoshida-Komiya, H., Tulsiani, D. R. P., Orgebin-Crist, M.-C., Hiroi, M., and Araki, Y. (1998). Rat zona pellucida glycoproteins: molecular cloning and characterisation of the three major components. Mol. Reprod. Dev. 51, 454–467.| Rat zona pellucida glycoproteins: molecular cloning and characterisation of the three major components.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXnt1Ort78%3D&md5=a67d3b5ad2dfdb308654363ded1d1b5cCAS |
Amaral, A. R., Silva, M. C., Möller, L. M., Beheregaray, L. B., and Coelho, M. M. (2011). Evolution of two reproductive proteins ZP3 and PKDREJ in Cetaceans. J. Hered. 102, 275–282.
| Evolution of two reproductive proteins ZP3 and PKDREJ in Cetaceans.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXkvFaqtbs%3D&md5=0d900d468e45272a999c6d30d6f43161CAS |
Birkhead, T. R., and Møller, A. P. (1998). ‘Sperm Competition and Sexual Selection’. (Academic Press: London.)
Birkhead, T. R., Hosken, D. J., and Pitnick, S. (2009). ‘Sperm Biology: an Evolutionary Perspective’. (Academic Press: Burlington, MA, USA.)
Bleil, J. D., and Wasserman, P. M. (1980). Mammalian sperm–egg interaction: identification of a glycoprotein in mouse egg zona pellucida possessing receptor activity for sperm. Cell 20, 873–882.
| Mammalian sperm–egg interaction: identification of a glycoprotein in mouse egg zona pellucida possessing receptor activity for sperm.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXlt12ksbk%3D&md5=0097abe0d32e4a9a8b63807934570b07CAS |
Bleil, J. D., and Wasserman, P. M. (1983). Sperm–egg interaction in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein. Dev. Biol. 95, 317–324.
| Sperm–egg interaction in the mouse: sequence of events and induction of the acrosome reaction by a zona pellucida glycoprotein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3sXhtVGitL4%3D&md5=a57dc1a1b5d949affbccd35ae301ca8eCAS |
Breed, W. G. (1995). Spermatozoa of murid rodents from Africa: morphological diversity and evolutionary trends. J. Zool. (Lond.) 237, 625–651.
| Spermatozoa of murid rodents from Africa: morphological diversity and evolutionary trends.Crossref | GoogleScholarGoogle Scholar |
Breed, W. G. (2004). The spermatozoon of Eurasian murine rodents; its morphological diversity and evolution. J. Morphol. 261, 52–69.
| The spermatozoon of Eurasian murine rodents; its morphological diversity and evolution.Crossref | GoogleScholarGoogle Scholar |
Breed, W. G., and Taylor, J. (2000). Body mass, testes mass, and sperm size in murine rodents. J. Mammal. 81, 758–768.
| Body mass, testes mass, and sperm size in murine rodents.Crossref | GoogleScholarGoogle Scholar |
Chen, S., Costa, V., and Beja-Pereira, A. (2011). Evolutionary patterns of two major reproduction candidate genes (Zp2 and Zp3) reveal no contribution to reproductive isolation between bovine species. BMC Evol. Biol. 11, 24.
| Evolutionary patterns of two major reproduction candidate genes (Zp2 and Zp3) reveal no contribution to reproductive isolation between bovine species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhvFahurw%3D&md5=bdb071a50f0bb38a84467673d0e19461CAS |
Clark, G. F. (2011a). Molecular models for sperm–oocyte binding. Glycobiology 21, 3–5.
| Molecular models for sperm–oocyte binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFGru7rI&md5=56edb844d2726a0bf900d8d6e273e563CAS |
Clark, G. F. (2011b). The molecular basis of mouse sperm–zona pellucida binding: a still unresolved issue in developmental biology. Reproduction 142, 377–381.
| The molecular basis of mouse sperm–zona pellucida binding: a still unresolved issue in developmental biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Cjur3P&md5=8be1e5a785f9ec1b87d2060448da6c18CAS |
Clark, G. F., and Dell, A. (2006). Molecular models for murine sperm–egg binding. J. Biol. Chem. 281, 13853–13856.
| Molecular models for murine sperm–egg binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XksFejurk%3D&md5=97fcc7fcd6f68e33c7865c92f7a84911CAS |
Clark, N. L., Aagaard, J. E., and Swanson, W. J. (2006). Evolution of reproductive proteins from animals and plants. Reproduction 131, 11–22.
| Evolution of reproductive proteins from animals and plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhsFehu7s%3D&md5=8a901ea0afc797b71bf6e6f30aead9d7CAS |
Conner, S. J., Lefièvre, L., Hughes, D. C., and Barratt, C. L. R. (2005). Cracking the egg: increased complexity in the zona pellucida. Hum. Reprod. 20, 1148–1152.
| Cracking the egg: increased complexity in the zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD2M3ps1OlsA%3D%3D&md5=ea1731d0ce43eb9185c9b36c906626a6CAS |
Eberhard, W. G. (2009). Postcopulatory sexual selection: Darwin’s omission and its consequences. Proc. Natl. Acad. Sci. USA 106, 10025–10032.
| Postcopulatory sexual selection: Darwin’s omission and its consequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXotF2lsrc%3D&md5=43ec0da66ec07ff9e1b47148890b6264CAS |
Fitzpatrick, J. L., and Lüpold, S. (2014). Sexual selection and the evolution of sperm quality. Mol. Hum. Reprod. 20, 1180–1189.
| Sexual selection and the evolution of sperm quality.Crossref | GoogleScholarGoogle Scholar |
Florman, H. M., and Wassarman, P. M. (1985). O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity. Cell 41, 313–324.
| O-linked oligosaccharides of mouse egg ZP3 account for its sperm receptor activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL2MXktFylsLk%3D&md5=e27e0d6b5755ab1f097a4ca7f6a6865aCAS |
Ford, F. (2006). A splitting headache: relationships and generic boundaries among Australian murids. Biol. J. Linn. Soc. Lond. 89, 117–138.
| A splitting headache: relationships and generic boundaries among Australian murids.Crossref | GoogleScholarGoogle Scholar |
Fox, B. J., and Murray, J. D. (1979). Laboratory hybridization of Australian Rattus fuscipes and Rattus lutreolus and its karyotypic confirmation. Aust. J. Zool. 27, 691–698.
| Laboratory hybridization of Australian Rattus fuscipes and Rattus lutreolus and its karyotypic confirmation.Crossref | GoogleScholarGoogle Scholar |
Gahlay, G., Gauthier, L., Baibakov, B., Epifano, O., and Dean, J. (2010). Gamete recognition in mice depends on the cleavage status of an egg’s zona pellucida protein. Science 329, 216–219.
| Gamete recognition in mice depends on the cleavage status of an egg’s zona pellucida protein.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXosVWgurc%3D&md5=27bc3b6073fe58b62aa55c5c9c9740e6CAS |
Gavrilets, S. (2000). Rapid evolution of reproductive barriers driven by sexual conflict. Nature 403, 886–889.
| Rapid evolution of reproductive barriers driven by sexual conflict.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhs1Ols7k%3D&md5=e12a8e5cc2c6f47f75e18e8289ddabf1CAS |
Gupta, S. K., Bhandari, B., Shrestha, A., Biswel, B. K., Palaniappan, C., Malhotra, S. S., and Gupta, N. (2012). Mammalian zona pellucida glycoproteins: structure and function during fertilisation. Cell Tissue Res. 349, 665–678.
| Mammalian zona pellucida glycoproteins: structure and function during fertilisation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xht1yltb3I&md5=05b030a45222543ef409e3f66eed7814CAS |
Jansa, S. A., Lundrigan, B. L., and Tucker, P. K. (2003). Tests for positive selection on immune and reproductive genes in closely related species of the murine genus. J. Mol. Evol. 56, 294–307.
| Tests for positive selection on immune and reproductive genes in closely related species of the murine genus.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhslWhsr8%3D&md5=8073643b4ce1b9109f35af3cd2fd5a02CAS |
Kinloch, R. A., Sakai, Y., and Wassarman, P. M. (1995). Mapping the mouse ZP3 combining site for sperm by exon swapping and site-directed mutagenesis. Proc. Natl. Acad. Sci. USA 92, 263–267.
| Mapping the mouse ZP3 combining site for sperm by exon swapping and site-directed mutagenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXjtVens74%3D&md5=b9de36969b06e6927b439d560e5bfd48CAS |
Lecompte, E., Aplin, K., Denys, C., Catzeflis, F., Chades, M., and Chevret, P. (2008). Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily. BMC Evol. Biol. 8, 199.
| Phylogeny and biogeography of African Murinae based on mitochondrial and nuclear gene sequences, with a new tribal classification of the subfamily.Crossref | GoogleScholarGoogle Scholar |
Li, D., Cao, S., and Xu, G. (2007). Polypeptide backbone derived from carboxyl terminal of mouse ZP3 inhibits sperm–zona binding. Mol. Reprod. Dev. 74, 1327–1336.
| Polypeptide backbone derived from carboxyl terminal of mouse ZP3 inhibits sperm–zona binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtVCmtr7M&md5=96a5789f29249fdcd96c35fa30f326d3CAS |
Lidicker, W. Z., and Laurance, W. F. (1990). Field identification of sympatric Rattus (Rodentia: Muridae) in north Queensland rainforest. Aust. Mammal. 13, 55–56.
Litscher, E. S., Juntunen, K., Seppo, A., Penttila, L., Niemela, R., Renkonen, O., and Wassarman, P. M. (1995). Oligosaccharide constructs with defined structures that inhibit binding of mouse sperm to unfertilized eggs in vitro. Biochemistry 34, 4662–4669.
| Oligosaccharide constructs with defined structures that inhibit binding of mouse sperm to unfertilized eggs in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXks1Kitb0%3D&md5=c8aa979dc17872cc3a962905ea96b10aCAS |
Litscher, E. S., Williams, Z., and Wassarman, P. M. (2009). Zona pellucida glycoprotein ZP3 and fertilization in mammals. Mol. Reprod. Dev. 76, 933–941.
| Zona pellucida glycoprotein ZP3 and fertilization in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtVGju77E&md5=714edb19acbfc7ee310c3603aba9f133CAS |
McLennan, H. J., Lüpold, S., Smissen, P., Rowe, K. C., and Breed, W. G. (2016). Greater sperm complexity in the Australasian old endemic rodents (Tribe: Hydromyini) is associated with increased levels of inter-male sperm competition. Reprod. Fertil. Dev. , .
| Greater sperm complexity in the Australasian old endemic rodents (Tribe: Hydromyini) is associated with increased levels of inter-male sperm competition.Crossref | GoogleScholarGoogle Scholar |
Monné, M., and Jovine, L. (2011). A structural view of egg coat architecture and function in fertilisation. Biol. Reprod. 85, 661–669.
| A structural view of egg coat architecture and function in fertilisation.Crossref | GoogleScholarGoogle Scholar |
Musser, G. G., and Carleton, M. D. (2005). Superfamily Muroidea. In ‘Mammal Species of the World. A Taxonomic and Geographical Reference. Vol. 2’. 3rd edn. (Eds D. E. Wilson and D. M. Reeder.) pp. 894–1531. (John Hopkins University Press: Baltimore, MD. USA.)
Nei, M., and Gojobori, T. (1986). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol. Biol. Evol. 3, 418–426.
| 1:CAS:528:DyaL28Xmt1aisbs%3D&md5=1ad12e7fb87ce613d1f4a10fc9b22b84CAS |
Nicholas, K. B., Nicholas, H. B. J., and Deerfield, D. W. I. (1997). GeneDoc: analysis and visualization of genetic variation. EMBNET NEWS 4, 14.
Nielsen, R., and Yang, Z. (1998). Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148, 929–936.
| 1:CAS:528:DyaK1cXks1eitr8%3D&md5=26bc0d29f8600f7d3c9df48e8569356aCAS |
Oko, R., and Clermont, Y. (1988). Isolation, structure and protein composition of the perforatorium of rat spermatozoa. Biol. Reprod. 39, 673–687.
| Isolation, structure and protein composition of the perforatorium of rat spermatozoa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1cXmt1Omsrg%3D&md5=c8f2304c84ab10a95466ec37956e0e1dCAS |
Pitnick, S., Hosken, D. J., and Birkhead, T. R. (2009). Sperm morphological diversity. In ‘Sperm Biology: An Evolutionary Perspective’. (Eds T. R. Birkhead, D. J. Hosken and S. Pitnick.) pp. 69–149. (Academic Press: London.)
Ramm, S. A., Scharer, L., Ehmcke, J., and Wistuba, J. (2014). Sperm competition and the evolution of spermatogenesis. Mol. Hum. Reprod. 20, 1169–1179.
| Sperm competition and the evolution of spermatogenesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XitVyhtrbL&md5=9018e5b1a54e7cc582c3777e740c8e75CAS |
Rankin, T. L., Coleman, J. S., Epifano, O., Hoodbhoy, T., Turner, S. G., Castle, P. E., Lee, E., Gore-Langton, R., and Dean, J. (2003). Fertility and taxon-specific sperm binding persist after replacement of mouse sperm receptors with human homologs. Dev. Cell 5, 33–43.
| Fertility and taxon-specific sperm binding persist after replacement of mouse sperm receptors with human homologs.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXmt1SmsLw%3D&md5=2e2d2e511787b89f22558c6eb0cf35cfCAS |
Ringuette, M. J., Chamberlin, M. E., Baur, A. W., Sobieski, D. A., and Dean, J. (1988). Molecular analysis of cDNA coding for ZP3, a sperm binding protein of the mouse zona pellucida. Dev. Biol. 127, 287–295.
| Molecular analysis of cDNA coding for ZP3, a sperm binding protein of the mouse zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL1MXlt1Sqtw%3D%3D&md5=c430ac352dee2c0df195ea612e68b6ccCAS |
Robins, J. H., McLenachan, P. A., Phillips, M. J., McComish, B. J., Matisoo-Smith, E., and Ross, H. A. (2010). Evolutionary relationships and divergence times among the native rats of Australia. BMC Evol. Biol. 10, 375.
| Evolutionary relationships and divergence times among the native rats of Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFGqur3E&md5=802e7ffd3e117b55c7c807bd948eac5cCAS |
Rosiere, T. K., and Wassarman, P. M. (1992). Identification of a region of mouse zona pellucida mZP3 that possesses sperm receptor activity. Dev. Biol. 154, 309–317.
| Identification of a region of mouse zona pellucida mZP3 that possesses sperm receptor activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1yqsrk%3D&md5=b37066d685961b2cdb52924ce584738aCAS |
Rowe, K. C., Reno, M. L., Richmond, D. M., Akins, R. M., and Steppan, S. J. (2008). Pliocene colonization and adaptive radiations in Australia and New Guinea (Sahul): multilocus systematics of the old endemic rodents (Muroidea: Murinae). Mol. Phylogenet. Evol. 47, 84–101.
| Pliocene colonization and adaptive radiations in Australia and New Guinea (Sahul): multilocus systematics of the old endemic rodents (Muroidea: Murinae).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXktV2jtLo%3D&md5=d1aab5080d34f45422b584270ae7639dCAS |
Rowe, K. C., Aplin, K. P., Baverstock, P. R., and Moritz, C. (2011). Recent and rapid speciation with limited morphological disparity in the genus Rattus. Syst. Biol. 60, 188–203.
| Recent and rapid speciation with limited morphological disparity in the genus Rattus.Crossref | GoogleScholarGoogle Scholar |
Swann, C. A., Cooper, S. J. B., and Breed, W. G. (2007). Molecular evolution of the carboxy terminal region of the zona pellucida 3 glycoprotein in murine rodents. Reproduction 133, 697–708.
| Molecular evolution of the carboxy terminal region of the zona pellucida 3 glycoprotein in murine rodents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXmsFeku7w%3D&md5=421283b58cece7befb65e6f1980b718cCAS |
Swanson, W. J., Yang, Z., Wolfner, M. F., and Aquadro, C. F. (2001). Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals. Proc. Natl. Acad. Sci. USA 98, 2509–2514.
| Positive Darwinian selection drives the evolution of several female reproductive proteins in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhslKms78%3D&md5=cef6f0be41537d5a16426a2f3387c805CAS |
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729.
| MEGA6: Molecular Evolutionary Genetics Analysis version 6.0.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVKhurzP&md5=48f84d5a98f7c128ce10064013bf70d6CAS |
Tardif, S., and Cormier, N. (2011). Role of zonadhesin during sperm–egg interaction: a species-specific acrosomal molecule with multiple functions. Mol. Hum. Reprod. 17, 661–668.
| Role of zonadhesin during sperm–egg interaction: a species-specific acrosomal molecule with multiple functions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlGrsrrF&md5=07af25b76a48ed7ed8682ef6d95200eeCAS |
Tardif, S., Wilson, M. D., Wagner, R., Hunt, P., Gertsenstein, M., Nagy, A., Lobe, C., Koop, B. F., and Hardy, D. M. (2010). Zonadhesin is essential for species specificity of sperm adhesion to the egg zona pellucida. J. Biol. Chem. 285, 24863–24870.
| Zonadhesin is essential for species specificity of sperm adhesion to the egg zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpsFemt7k%3D&md5=8412a33195d94563755c99d330572ef8CAS |
Thitipramote, N., Suwanjarat, J., Leigh, C. M., and Breed, W. G. (2011). Variation in sperm morphology of a murine rodent from south-east Asia: the Greater Bandicoot rat, Bandicota indica. Acta Zool. 92, 201–205.
| Variation in sperm morphology of a murine rodent from south-east Asia: the Greater Bandicoot rat, Bandicota indica.Crossref | GoogleScholarGoogle Scholar |
Turner, L. M., and Hoekstra, H. E. (2006). Adaptive evolution of fertilization proteins within a genus: variation in ZP2 and ZP3 in deer mice (Peromyscus). Mol. Biol. Evol. 23, 1656–1669.
| Adaptive evolution of fertilization proteins within a genus: variation in ZP2 and ZP3 in deer mice (Peromyscus).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVWhtLY%3D&md5=3ecbf344125e3be66a2295e11d8caeb3CAS |
van der Horst, G., and Maree, L. (2014). Sperm form and function in absence of sperm competition. Mol. Reprod. Dev. 81, 204–216.
| Sperm form and function in absence of sperm competition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVaitLbO&md5=b4baf3f130f099bcac2bdc699703e1d7CAS |
Varea-Sánchez, M., Montoto, L. G., Tourmente, M., and Roldan, E. R. S. (2014). Postcopulatory sexual selection results in spermatozoa with more uniform head and flagellum sizes in rodents. PLoS One 9, e108148.
| Postcopulatory sexual selection results in spermatozoa with more uniform head and flagellum sizes in rodents.Crossref | GoogleScholarGoogle Scholar |
Vázquez-Domínguez, E., Paetkau, D., Tucker, N., Hinten, G., and Moritz, C. C. (2001). Resolution of natural groups using iterative assignment tests: an example from two species of Australian native rats (Rattus). Mol. Ecol. 10, 2069–2078.
| Resolution of natural groups using iterative assignment tests: an example from two species of Australian native rats (Rattus).Crossref | GoogleScholarGoogle Scholar |
Vicens, A., Lüke, L., and Roldan, E. R. S. (2014). Proteins involved in motility and sperm–egg interactions evolve more rapidly in mouse spermatozoa. PloS One 9, e91302.
| Proteins involved in motility and sperm–egg interactions evolve more rapidly in mouse spermatozoa.Crossref | GoogleScholarGoogle Scholar |
Wassarman, P. M., and Litscher, E. S. (1995). Sperm–egg recognition mechanisms in mammals. Curr. Top. Dev. Biol. 30, 1–19.
| Sperm–egg recognition mechanisms in mammals.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXoslKlu7g%3D&md5=ca576f6c376b27beda708779c6618369CAS |
Wassarman, P. M., and Litscher, E. S. (2001). Towards the molecular basis of sperm and egg interaction during mammalian fertilization. Cells Tissues Organs 168, 36–45.
| Towards the molecular basis of sperm and egg interaction during mammalian fertilization.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXptVeitLk%3D&md5=155f40bfb2abbd023c2ce999653dda85CAS |
Wassarman, P. M., and Litscher, E. S. (2008). Mammalian fertilization: the egg’s multifunctional zona pellucida. Int. J. Dev. Biol. 52, 665–676.
| Mammalian fertilization: the egg’s multifunctional zona pellucida.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXht12qsL7I&md5=473f43f01da2efa40084b5acf1b998eeCAS |
Wassarman, P. M., Jovine, L., Litscher, E., Qi, H., and Williams, Z. (2004). Egg–sperm interactions at fertilization in mammals. Eur. J. Obstet. Gynecol. Reprod. Biol. 115S, S57–S60.
| Egg–sperm interactions at fertilization in mammals.Crossref | GoogleScholarGoogle Scholar |
Watts, C. H. S., and Baverstock, P. R. (1995). Evolution in the Murinae (Rodentia) assessed by microcomplement fixation of albumin. Aust. J. Zool. 43, 105–118.
| Evolution in the Murinae (Rodentia) assessed by microcomplement fixation of albumin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXns1CksLc%3D&md5=767b0ebb8b35d9f8b50f5d7ff7b9d56cCAS |
Williams, Z., Litscher, E., Jovine, L., and Wassarman, P. M. (2006). Polypeptide encoded by mouse ZP3 exon-7 is necessary and sufficient for binding of mouse sperm in vitro. J. Cell. Physiol. 207, 30–39.
| Polypeptide encoded by mouse ZP3 exon-7 is necessary and sufficient for binding of mouse sperm in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XisFOjsrw%3D&md5=45a4bf4310cfdde28ddfe011051f37a1CAS |
Wong, W. S. W., Yang, Z., Goldman, N., and 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.
| Accuracy and power of statistical methods for detecting adaptive evolution in protein coding sequences and for identifying positively selected sites.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXhtVKms7jN&md5=31ded93de6b409f3b688114b2fee5e69CAS |
Yanagimachi, R. (1994). Mammalian fertilization. In ‘The Physiology of Reproduction’. (Eds E. Knobil and J. D. Neill.) pp. 189–317. (Raven Press: New York.)
Yang, Z. (2007). PAML 4: phylogenetic analysis by maximum likelihood. Mol. Biol. Evol. 24, 1586–1591.
| PAML 4: phylogenetic analysis by maximum likelihood.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpsVGrs7c%3D&md5=a10b9c3dd759cfdf5334eef34c0d7150CAS |
Yang, Z., and Nielsen, R. (2000). Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol. Biol. Evol. 17, 32–43.
| Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXotF2qtA%3D%3D&md5=ff4590ab66c75c7f9c5ccb9c27714e1dCAS |
Yang, Z., Wong, W. S. W., and Nielsen, R. (2005). Bayes Empirical Bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22, 1107–1118.
| Bayes Empirical Bayes inference of amino acid sites under positive selection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjtFaisbk%3D&md5=d3a9211b2ebaf0914d4968a192018329CAS |
