Sexual selection and the adaptive evolution of mammalian ejaculate proteins

Ramm SA, Oliver PL, Ponting CP, Stockley P, Emes RD (2008)
Molecular Biology and Evolution 25(1): 207-219.

Zeitschriftenaufsatz | Veröffentlicht | Englisch
 
Download
Es wurden keine Dateien hochgeladen. Nur Publikationsnachweis!
Autor*in
Ramm, Steven A.UniBi ; Oliver, Peter L.; Ponting, Chris P.; Stockley, Paula; Emes, Richard D.
Abstract / Bemerkung
An elevated rate of substitution characterizes the molecular evolution of reproductive proteins from a wide range of taxa. Although the selective pressures explaining this rapid evolution are yet to be resolved, recent evidence implicates sexual selection as a potentially important explanatory factor. To investigate this hypothesis, we sought evidence of a high rate of adaptive gene evolution linked to postcopulatory sexual selection in muroid rodents, a model vertebrate group displaying a broad range of mating systems. Specifically, we sequenced 7 genes from diverse rodents that are expressed in the testes, prostate, or seminal vesicles, products of which have the potential to act in sperm competition. We inferred positive Darwinian selection in these genes by estimation of the ratio of nonsynonymous (d(N), amino acid changing) to synonymous (d(S), amino acid retaining) substitution rates (omega = d(N)/d(S)). Next, we tested whether variation in this ratio among lineages could be attributed to interspecific variation in mating systems, as inferred from the variation in these rodents' relative testis sizes (RTS). Four of the 7 genes examined (Prm1, Sva, Acrv1, and Svs2, but not Svp2, Msmb, or Spink3) exhibit unambiguous evidence of positive selection. One of these, the seminal vesicle-derived protein Svs2, also shows some evidence for a concentration of positive selection in those lineages in which sperm competition is common. However, this was not a general trend among all the rodent genes we examined. Using the same methods, we then reanalyzed previously published data on 2 primate genes, SEMG1 and SEMG2. Although SEMG2 also shows evidence of positive selection concentrated in lineages subject to high levels of sperm competition, no such trend was found for SEMG1. Overall, despite a high rate of positive selection being a feature of many ejaculate proteins, these results indicate that the action of sexual selection potentially responsible for elevated evolutionary rates may be difficult to detect on a gene-by-gene basis. Although the extreme diversity of reproductive phenotypes exhibited in nature attests to the power of sexual selection, the extent to which this force predominates in driving the rapid molecular evolution of reproductive genes therefore remains to be determined.
Stichworte
positive selection; adaptive evolution; primates; rodents; selection; sperm competition; sexual
Erscheinungsjahr
2008
Zeitschriftentitel
Molecular Biology and Evolution
Band
25
Ausgabe
1
Seite(n)
207-219
ISSN
0737-4038
eISSN
1537-1719
Page URI
https://pub.uni-bielefeld.de/record/2491890

Zitieren

Ramm SA, Oliver PL, Ponting CP, Stockley P, Emes RD. Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Molecular Biology and Evolution. 2008;25(1):207-219.
Ramm, S. A., Oliver, P. L., Ponting, C. P., Stockley, P., & Emes, R. D. (2008). Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Molecular Biology and Evolution, 25(1), 207-219. doi:10.1093/molbev/msm242
Ramm, Steven A., Oliver, Peter L., Ponting, Chris P., Stockley, Paula, and Emes, Richard D. 2008. “Sexual selection and the adaptive evolution of mammalian ejaculate proteins”. Molecular Biology and Evolution 25 (1): 207-219.
Ramm, S. A., Oliver, P. L., Ponting, C. P., Stockley, P., and Emes, R. D. (2008). Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Molecular Biology and Evolution 25, 207-219.
Ramm, S.A., et al., 2008. Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Molecular Biology and Evolution, 25(1), p 207-219.
S.A. Ramm, et al., “Sexual selection and the adaptive evolution of mammalian ejaculate proteins”, Molecular Biology and Evolution, vol. 25, 2008, pp. 207-219.
Ramm, S.A., Oliver, P.L., Ponting, C.P., Stockley, P., Emes, R.D.: Sexual selection and the adaptive evolution of mammalian ejaculate proteins. Molecular Biology and Evolution. 25, 207-219 (2008).
Ramm, Steven A., Oliver, Peter L., Ponting, Chris P., Stockley, Paula, and Emes, Richard D. “Sexual selection and the adaptive evolution of mammalian ejaculate proteins”. Molecular Biology and Evolution 25.1 (2008): 207-219.

71 Zitationen in Europe PMC

Daten bereitgestellt von Europe PubMed Central.

Evolution of gene expression levels in the male reproductive organs of Anopheles mosquitoes.
Izquierdo A, Fahrenberger M, Persampieri T, Benedict MQ, Giles T, Catteruccia F, Emes RD, Dottorini T., Life Sci Alliance 2(1), 2019
PMID: 30623175
A targeted in situ hybridization screen identifies putative seminal fluid proteins in a simultaneously hermaphroditic flatworm.
Weber M, Wunderer J, Lengerer B, Pjeta R, Rodrigues M, Schärer L, Ladurner P, Ramm SA., BMC Evol Biol 18(1), 2018
PMID: 29848299
Quantitative evolutionary proteomics of seminal fluid from primates with different mating systems.
Claw KG, George RD, MacCoss MJ, Swanson WJ., BMC Genomics 19(1), 2018
PMID: 29929489
Novel seminal fluid proteins in the seed beetle Callosobruchus maculatus identified by a proteomic and transcriptomic approach.
Bayram H, Sayadi A, Goenaga J, Immonen E, Arnqvist G., Insect Mol Biol 26(1), 2017
PMID: 27779332
Sperm competition risk drives rapid ejaculate adjustments mediated by seminal fluid.
Bartlett MJ, Steeves TE, Gemmell NJ, Rosengrave PC., Elife 6(), 2017
PMID: 29084621
Some assembly required: evolutionary and systems perspectives on the mammalian reproductive system.
Mordhorst BR, Wilson ML, Conant GC., Cell Tissue Res 363(1), 2016
PMID: 26254045
Sexual Selection of Protamine 1 in Mammals.
Lüke L, Tourmente M, Roldan ER., Mol Biol Evol 33(1), 2016
PMID: 26429923
Proteomics of reproductive systems: Towards a molecular understanding of postmating, prezygotic reproductive barriers.
McDonough CE, Whittington E, Pitnick S, Dorus S., J Proteomics 135(), 2016
PMID: 26476146
Cross-species proteomics in analysis of mammalian sperm proteins.
Bayram HL, Claydon AJ, Brownridge PJ, Hurst JL, Mileham A, Stockley P, Beynon RJ, Hammond DE., J Proteomics 135(), 2016
PMID: 26768581
Selective constraints on protamine 2 in primates and rodents.
Lüke L, Tourmente M, Dopazo H, Serra F, Roldan ER., BMC Evol Biol 16(), 2016
PMID: 26801756
LMAP: Lightweight Multigene Analyses in PAML.
Maldonado E, Almeida D, Escalona T, Khan I, Vasconcelos V, Antunes A., BMC Bioinformatics 17(1), 2016
PMID: 27597435
The molecular basis and reproductive function(s) of copulatory plugs.
Schneider MR, Mangels R, Dean MD., Mol Reprod Dev 83(9), 2016
PMID: 27518218
Sexual selection and the adaptive evolution of PKDREJ protein in primates and rodents.
Vicens A, Gómez Montoto L, Couso-Ferrer F, Sutton KA, Roldan ER., Mol Hum Reprod 21(2), 2015
PMID: 25304980
On a matter of seminal importance.
McGraw LA, Suarez SS, Wolfner MF., Bioessays 37(2), 2015
PMID: 25379987
Variation in promiscuity and sexual selection drives avian rate of Faster-Z evolution.
Wright AE, Harrison PW, Zimmer F, Montgomery SH, Pointer MA, Mank JE., Mol Ecol 24(6), 2015
PMID: 25689782
Genetic and phenotypic influences on copulatory plug survival in mice.
Mangels R, Young B, Keeble S, Ardekani R, Meslin C, Ferreira Z, Clark NL, Good JM, Dean MD., Heredity (Edinb) 115(6), 2015
PMID: 26103947
Sperm competition risk drives plasticity in seminal fluid composition.
Ramm SA, Edward DA, Claydon AJ, Hammond DE, Brownridge P, Hurst JL, Beynon RJ, Stockley P., BMC Biol 13(), 2015
PMID: 26507392
Within-species divergence in the seminal fluid proteome and its effect on male and female reproduction in a beetle.
Goenaga J, Goenaga J, Yamane T, Rönn J, Arnqvist G., BMC Evol Biol 15(), 2015
PMID: 26627998
SEMG1 may be the candidate gene for idiopathic asthenozoospermia.
Yu Q, Zhou Q, Wei Q, Li J, Feng C, Mao X., Andrologia 46(2), 2014
PMID: 23289976
Mating systems and protein-protein interactions determine evolutionary rates of primate sperm proteins.
Schumacher J, Rosenkranz D, Herlyn H., Proc Biol Sci 281(1775), 2014
PMID: 24307672
Divergent positive selection in rhodopsin from lake and riverine cichlid fishes.
Schott RK, Refvik SP, Hauser FE, López-Fernández H, Chang BS., Mol Biol Evol 31(5), 2014
PMID: 24509690
Sexual selection on protamine and transition nuclear protein expression in mouse species.
Lüke L, Campbell P, Varea Sánchez M, Nachman MW, Roldan ER., Proc Biol Sci 281(1783), 2014
PMID: 24671975
Evolution of protamine genes and changes in sperm head phenotype in rodents.
Lüke L, Vicens A, Tourmente M, Roldan ER., Biol Reprod 90(3), 2014
PMID: 24522148
Genetic signatures for enhanced olfaction in the African mole-rats.
Stathopoulos S, Bishop JM, O'Ryan C., PLoS One 9(4), 2014
PMID: 24699281
[What the study of seminal fluid proteins in Drosophila tells us about the evolution of reproduction].
Ben Chehida Y, Denis B, Claisse G, Joly D., Med Sci (Paris) 30(6-7), 2014
PMID: 25014456
Selective constraint dominates the evolution of genes expressed in a novel reproductive gland.
Finseth FR, Bondra E, Harrison RG., Mol Biol Evol 31(12), 2014
PMID: 25193339
Reproductive isolation among allopatric Drosophila montana populations.
Jennings JH, Snook RR, Hoikkala A., Evolution 68(11), 2014
PMID: 25302639
Sexual conflict and seminal fluid proteins: a dynamic landscape of sexual interactions.
Sirot LK, Wong A, Chapman T, Wolfner MF., Cold Spring Harb Perspect Biol 7(2), 2014
PMID: 25502515
Reproduction and immunity-driven natural selection in the human WFDC locus.
Ferreira Z, Seixas S, Andrés AM, Kretzschmar WW, Mullikin JC, Cherukuri PF, Cruz P, Swanson WJ, NISC Comparative Sequencing Program, Clark AG, Green ED, Hurle B., Mol Biol Evol 30(4), 2013
PMID: 23292442
Comparative population genomics of the ejaculate in humans and the great apes.
Good JM, Wiebe V, Albert FW, Burbano HA, Kircher M, Green RE, Halbwax M, André C, Atencia R, Fischer A, Pääbo S., Mol Biol Evol 30(4), 2013
PMID: 23329688
Polyandry as a mediator of sexual selection before and after mating.
Kvarnemo C, Simmons LW., Philos Trans R Soc Lond B Biol Sci 368(1613), 2013
PMID: 23339234
Selection on the Drosophila seminal fluid protein Acp62F.
Wong A, Rundle H., Ecol Evol 3(7), 2013
PMID: 23919141
Heterogenous turnover of sperm and seminal vesicle proteins in the mouse revealed by dynamic metabolic labeling.
Claydon AJ, Ramm SA, Pennington A, Hurst JL, Stockley P, Beynon R., Mol Cell Proteomics 11(6), 2012
PMID: 22331477
Sperm competition roles and ejaculate investment in a promiscuous mammal.
Lemaître JF, Ramm SA, Hurst JL, Stockley P., J Evol Biol 25(6), 2012
PMID: 22515660
Adaptive evolution of Toll-like receptor 5 in domesticated mammals.
Smith SA, Jann OC, Haig D, Russell GC, Werling D, Glass EJ, Emes RD., BMC Evol Biol 12(), 2012
PMID: 22827462
Positive Selection and the Evolution of izumo Genes in Mammals.
Grayson P, Civetta A., Int J Evol Biol 2012(), 2012
PMID: 22957301
Proteome dynamics: revisiting turnover with a global perspective.
Claydon AJ, Beynon R., Mol Cell Proteomics 11(12), 2012
PMID: 23125033
Social cues of sperm competition influence accessory reproductive gland size in a promiscuous mammal.
Lemaître JF, Ramm SA, Hurst JL, Stockley P., Proc Biol Sci 278(1709), 2011
PMID: 20880887
Adaptive evolution of four microcephaly genes and the evolution of brain size in anthropoid primates.
Montgomery SH, Capellini I, Venditti C, Barton RA, Mundy NI., Mol Biol Evol 28(1), 2011
PMID: 20961963
Identification of ejaculated proteins in the house mouse (Mus domesticus) via isotopic labeling.
Dean MD, Findlay GD, Hoopmann MR, Wu CC, MacCoss MJ, Swanson WJ, Nachman MW., BMC Genomics 12(), 2011
PMID: 21663664
Sexual selection halts the relaxation of protamine 2 among rodents.
Lüke L, Vicens A, Serra F, Luque-Larena JJ, Dopazo H, Roldan ER, Gomendio M., PLoS One 6(12), 2011
PMID: 22216223
Sperm proteomics reveals intensified selection on mouse sperm membrane and acrosome genes.
Dorus S, Wasbrough ER, Busby J, Wilkin EC, Karr TL., Mol Biol Evol 27(6), 2010
PMID: 20080865
Condition-dependent ejaculate size and composition in a ladybird beetle.
Perry JC, Rowe L., Proc Biol Sci 277(1700), 2010
PMID: 20573622
Sexual selection and the molecular evolution of ADAM proteins.
Finn S, Civetta A., J Mol Evol 71(3), 2010
PMID: 20730583
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 276(1666), 2009
PMID: 19364735
Proteomics and comparative genomic investigations reveal heterogeneity in evolutionary rate of male reproductive proteins in mice (Mus domesticus).
Dean MD, Clark NL, Findlay GD, Karn RC, Yi X, Swanson WJ, MacCoss MJ, Nachman MW., Mol Biol Evol 26(8), 2009
PMID: 19420050
Hsp-90 and the biology of nematodes.
Him NA, Gillan V, Emes RD, Maitland K, Devaney E., BMC Evol Biol 9(), 2009
PMID: 19849843
Transglutaminase-mediated semen coagulation controls sperm storage in the malaria mosquito.
Rogers DW, Baldini F, Battaglia F, Panico M, Dell A, Morris HR, Catteruccia F., PLoS Biol 7(12), 2009
PMID: 20027206
Finding the right plugin: mosquitoes have the answer.
Chapman T., PLoS Biol 7(12), 2009
PMID: 20027207
Adaptive evolution in rodent seminal vesicle secretion proteins.
Karn RC, Clark NL, Nguyen ED, Swanson WJ., Mol Biol Evol 25(11), 2008
PMID: 18718917
Export

Markieren/ Markierung löschen
Markierte Publikationen

Open Data PUB

Web of Science

Dieser Datensatz im Web of Science®
Quellen

PMID: 18032407
PubMed | Europe PMC

Suchen in

Google Scholar