Sexual size dimorphism predicts rates of sequence evolution of SPerm Adhesion Molecule 1 (SPAM1, also PH-20) in monkeys, but not in hominoids (apes including humans)

Prothmann, Andreas; Laube, Irina; Dietz, Johanna; Roos, Christian; Mengel, Katja; Zischler, Hans; Herlyn, Holger

doi:10.1016/j.ympev.2011.12.008

Cited by 11 publications

(10 citation statements)

References 79 publications

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“…[8–13]; see also [35,53]). Consistently, we observed significantly increased d N / d S values in post-mating relative to pre-mating sperm and non-reproductive proteins for the branch to common chimpanzee and for foreground 2 comprising chimpanzee and Rhesus branches.…”

Section: Discussionmentioning

confidence: 99%

“…At the molecular level, the size of semen coagulation proteins has been reported to covary with levels of sexual selection in hominoid primates and murine rodents ([5,6]; see also [7]). Other authors observed correlations between evolutionary rates of murine and primate seminal and sperm proteins with species-specific levels of sexual selection as derived from mating systems, testis sizes, number of periovulatory partners or sexual dimorphism of body weight [8–13]. Such associations point to post-mating competition between sperm of different males (sperm competition) as a force enhancing evolutionary rates of male reproductive genes and proteins.…”

Section: Introductionmentioning

confidence: 99%

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Mating systems and protein–protein interactions determine evolutionary rates of primate sperm proteins

Schumacher

Rosenkranz²,

Herlyn³

2014

Proc. R. Soc. B.

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To assess the relative impact of functional constraint and post-mating sexual selection on sequence evolution of reproductive proteins, we examined 169 primate sperm proteins. In order to recognize potential genome-wide trends, we additionally analysed a sample of altogether 318 non-reproductive (brain and postsynaptic) proteins. Based on cDNAs of eight primate species (Anthropoidea), we observed that pre-mating sperm proteins engaged in sperm composition and assembly show significantly lower incidence of site-specific positive selection and overall lower non-synonymous to synonymous substitution rates (dN/dS) across sites as compared with post-mating sperm proteins involved in capacitation, hyperactivation, acrosome reaction and fertilization. Moreover, database screening revealed overall more intracellular protein interaction partners in pre-mating than in post-mating sperm proteins. Finally, post-mating sperm proteins evolved at significantly higher evolutionary rates than pre-mating sperm and non-reproductive proteins on the branches to multi-male breeding species, while no such increase was observed on the branches to unimale and monogamous species. We conclude that less protein–protein interactions of post-mating sperm proteins account for lowered functional constraint, allowing for stronger impact of post-mating sexual selection, while the opposite holds true for pre-mating sperm proteins. This pattern is particularly strong in multi-male breeding species showing high female promiscuity.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Mating systems and protein–protein interactions determine evolutionary rates of primate sperm proteins

Schumacher

Rosenkranz²,

Herlyn³

2014

Proc. R. Soc. B.

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“…SPAM1 is a hyaluronidase which can bind to sperm during capacitation and increase cumulus dispersal efficiency and ability of sperm to penetrate the cumulus of oocytes (Griffiths et al 2008; Martin-DeLeon 2006). Prothmann et al (2012) found that the rate of evolution of the gene encoding SPAM1 could be correlated with relative testis weight in monkeys as well as the uni-male versus multi-male breeding system. This suggests that different levels of sperm competition might account for species-specific sequence evolution of SPAM1 in these species.…”

Section: Discussionmentioning

confidence: 99%

Genes Encoding Mammalian Oviductal Proteins Involved in Fertilization are Subjected to Gene Death and Positive Selection

Moros-Nicolás¹,

Fouchécourt²,

Goudet³

et al. 2018

J Mol Evol

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Oviductal proteins play an important role in mammalian fertilization, as proteins from seminal fluid. However, in contrast with the latter, their phylogenetic evolution has been poorly studied. Our objective was to study in 16 mammals the evolution of 16 genes that encode oviductal proteins involved in at least one of the following steps: (1) sperm–oviduct interaction, (2) acrosome reaction, and/or (3) sperm–zona pellucida interaction. Most genes were present in all studied mammals. However, some genes were lost along the evolution of mammals and found as pseudogenes: annexin A5 (ANXA5) and deleted in malignant brain tumor 1 (DMBT1) in tarsier; oviductin (OVGP1) in megabat; and probably progestagen-associated endometrial protein (PAEP) in tarsier, mouse, rat, rabbit, dolphin, and megabat; prostaglandin D2 synthase (PTGDS) in microbat; and plasminogen (PLG) in megabat. Four genes [ANXA1, ANXA4, ANXA5, and heat shock 70 kDa protein 5 (HSPA5)] showed branch-site positive selection, whereas for seven genes [ANXA2, lactotransferrin (LTF), OVGP1, PLG, S100 calcium-binding protein A11 (S100A11), Sperm adhesion molecule 1 (SPAM1), and osteopontin (SPP1)] branch-site model and model-site positive selection were observed. These results strongly suggest that genes encoding oviductal proteins that are known to be important for gamete fertilization are subjected to positive selection during evolution, as numerous genes encoding proteins from mammalian seminal fluid. This suggests that such a rapid evolution may have as a consequence that two isolated populations become separate species more rapidly.

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“…; Finn and Civetta ; Prothmann et al. ). Moreover, average rates of reproductive protein evolution are higher in polyandrous lineages in comparison with monandrous lineages in primates and in Drosophila (Wagstaff and Begun , ; Kelleher et al.…”

Section: Introductionmentioning

confidence: 99%

“…Consistent with the hypothesis that sexual selection is a primary cause of rapid reproductive protein evolution, comparative studies indicate a correlation between mating system and the rates of evolution of some reproductive proteins, including SFPs. That is, for some individual proteins, rates of evolution are higher in polyandrous lineages than in monandrous lineages, where postcopulatory sexual selection is less likely to occur (e.g., Ramm et al 2008;Finn and Civetta 2010;Prothmann et al 2012). Moreover, average rates of reproductive protein evolution are higher in polyandrous lineages in comparison with monandrous lineages in primates and in Drosophila Begun 2005b, 2007;Kelleher et al 2007;Almeida and Desalle 2009), again suggesting that sexual conflict is important in the evolution of reproductive proteins.…”

Section: Introductionmentioning

confidence: 99%

Selection on the Drosophila seminal fluid protein Acp62F

Wong

Rundle

2013

Ecology and Evolution

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Sperm competition and sexual conflict are thought to underlie the rapid evolution of reproductive proteins in many taxa. While comparative data are generally consistent with these hypotheses, few manipulative tests have been conducted and those that have provided contradictory results in some cases. Here, we use both comparative and experimental techniques to investigate the evolution of the Drosophila melanogaster seminal fluid protein Acp62F, a protease inhibitor for which extensive functional tests have yielded ambiguous results. Using between-species sequence comparisons, we show that Acp62F has been subject to recurrent positive selection. In addition, we experimentally evolved populations polymorphic for an Acp62F null allele over eight generations, manipulating the opportunities for natural and sexual selection. We found that the Acp62F null allele increased in frequency in the presence of natural selection, with no effect of sexual selection.

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Sexual size dimorphism predicts rates of sequence evolution of SPerm Adhesion Molecule 1 (SPAM1, also PH-20) in monkeys, but not in hominoids (apes including humans)

Cited by 11 publications

References 79 publications

Mating systems and protein–protein interactions determine evolutionary rates of primate sperm proteins

Mating systems and protein–protein interactions determine evolutionary rates of primate sperm proteins

Genes Encoding Mammalian Oviductal Proteins Involved in Fertilization are Subjected to Gene Death and Positive Selection

Selection on the Drosophila seminal fluid protein Acp62F

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