Rapid divergence of a gamete recognition gene promoted macroevolution of Eutheria.
Bioinformatics
Fertilization
Gamete recognition
Mammals
Molecular evolution
Phylogenetics
Reproductive isolation
Speciation
Species specificity
Zonadhesin
Journal
Genome biology
ISSN: 1474-760X
Titre abrégé: Genome Biol
Pays: England
ID NLM: 100960660
Informations de publication
Date de publication:
11 07 2022
11 07 2022
Historique:
received:
18
11
2021
accepted:
29
06
2022
entrez:
12
7
2022
pubmed:
13
7
2022
medline:
15
7
2022
Statut:
epublish
Résumé
Speciation genes contribute disproportionately to species divergence, but few examples exist, especially in vertebrates. Here we test whether Zan, which encodes the sperm acrosomal protein zonadhesin that mediates species-specific adhesion to the egg's zona pellucida, is a speciation gene in placental mammals. Genomic ontogeny reveals that Zan arose by repurposing of a stem vertebrate gene that was lost in multiple lineages but retained in Eutheria on acquiring a function in egg recognition. A 112-species Zan sequence phylogeny, representing 17 of 19 placental Orders, resolves all species into monophyletic groups corresponding to recognized Orders and Suborders, with <5% unsupported nodes. Three other rapidly evolving germ cell genes (Adam2, Zp2, and Prm1), a paralogous somatic cell gene (TectA), and a mitochondrial gene commonly used for phylogenetic analyses (Cytb) all yield trees with poorer resolution than the Zan tree and inferior topologies relative to a widely accepted mammalian supertree. Zan divergence by intense positive selection produces dramatic species differences in the protein's properties, with ordinal divergence rates generally reflecting species richness of placental Orders consistent with expectations for a speciation gene that acts across a wide range of taxa. Furthermore, Zan's combined phylogenetic utility and divergence exceeds those of all other genes known to have evolved in Eutheria by positive selection, including the only other mammalian speciation gene, Prdm9. Species-specific egg recognition conferred by Zan's functional divergence served as a mode of prezygotic reproductive isolation that promoted the extraordinary adaptive radiation and success of Eutheria.
Sections du résumé
BACKGROUND
Speciation genes contribute disproportionately to species divergence, but few examples exist, especially in vertebrates. Here we test whether Zan, which encodes the sperm acrosomal protein zonadhesin that mediates species-specific adhesion to the egg's zona pellucida, is a speciation gene in placental mammals.
RESULTS
Genomic ontogeny reveals that Zan arose by repurposing of a stem vertebrate gene that was lost in multiple lineages but retained in Eutheria on acquiring a function in egg recognition. A 112-species Zan sequence phylogeny, representing 17 of 19 placental Orders, resolves all species into monophyletic groups corresponding to recognized Orders and Suborders, with <5% unsupported nodes. Three other rapidly evolving germ cell genes (Adam2, Zp2, and Prm1), a paralogous somatic cell gene (TectA), and a mitochondrial gene commonly used for phylogenetic analyses (Cytb) all yield trees with poorer resolution than the Zan tree and inferior topologies relative to a widely accepted mammalian supertree. Zan divergence by intense positive selection produces dramatic species differences in the protein's properties, with ordinal divergence rates generally reflecting species richness of placental Orders consistent with expectations for a speciation gene that acts across a wide range of taxa. Furthermore, Zan's combined phylogenetic utility and divergence exceeds those of all other genes known to have evolved in Eutheria by positive selection, including the only other mammalian speciation gene, Prdm9.
CONCLUSIONS
Species-specific egg recognition conferred by Zan's functional divergence served as a mode of prezygotic reproductive isolation that promoted the extraordinary adaptive radiation and success of Eutheria.
Identifiants
pubmed: 35821049
doi: 10.1186/s13059-022-02721-y
pii: 10.1186/s13059-022-02721-y
pmc: PMC9275260
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
155Informations de copyright
© 2022. The Author(s).
Références
J Biol Chem. 1997 Mar 28;272(13):8791-801
pubmed: 9079715
Science. 2006 Jun 16;312(5780):1614-20
pubmed: 16778047
Mol Ecol. 2017 Jan;26(1):277-290
pubmed: 27230590
Trends Ecol Evol. 2004 Aug;19(8):430-8
pubmed: 16701301
Mol Biol Evol. 2018 Jun 1;35(6):1547-1549
pubmed: 29722887
Genetics. 2017 Nov;207(3):825-842
pubmed: 29097397
Proc Natl Acad Sci U S A. 2005 May 3;102 Suppl 1:6522-6
pubmed: 15851676
Curr Biol. 2013 Nov 18;23(22):2262-2267
pubmed: 24184098
Gene. 2002 Apr 17;288(1-2):111-7
pubmed: 12034500
Am J Hum Genet. 2006 Nov;79(5):820-30
pubmed: 17033959
Biol Reprod. 1987 Aug;37(1):189-99
pubmed: 3115322
Natl Sci Rev. 2020 Aug;7(8):1387-1397
pubmed: 34692166
Bioessays. 2000 Dec;22(12):1085-94
pubmed: 11084624
Curr Biol. 2016 Apr 25;26(8):R325-8
pubmed: 27115689
Front Plant Sci. 2018 Jun 28;9:907
pubmed: 30002669
Proc Natl Acad Sci U S A. 2009 Jun 16;106 Suppl 1:9955-62
pubmed: 19528639
Curr Top Dev Biol. 2018;130:443-488
pubmed: 29853187
PLoS Biol. 2019 Dec 4;17(12):e3000494
pubmed: 31800571
Nat Genet. 1998 May;19(1):60-2
pubmed: 9590290
J Cell Biol. 2014 Jun 23;205(6):801-9
pubmed: 24934154
J Biol Chem. 1994 Jul 22;269(29):19000-4
pubmed: 8034657
Syst Biol. 2012 Mar;61(2):204-13
pubmed: 21873376
Nature. 2000 Jan 20;403(6767):304-9
pubmed: 10659848
Mol Biol Evol. 2001 Feb;18(2):132-43
pubmed: 11158372
Nat Methods. 2012 Jul 30;9(8):772
pubmed: 22847109
Science. 2010 Jul 9;329(5988):216-9
pubmed: 20616279
J Biol Chem. 2007 Jun 15;282(24):17900-7
pubmed: 17439939
Mol Biol Evol. 2006 Sep;23(9):1656-69
pubmed: 16774977
Nat Rev Genet. 2002 Feb;3(2):137-44
pubmed: 11836507
Philos Trans R Soc Lond B Biol Sci. 2016 Jul 19;371(1699):
pubmed: 27325836
Proc Natl Acad Sci U S A. 2005 Dec 20;102(51):18514-9
pubmed: 16339909
Trends Ecol Evol. 2011 Apr;26(4):160-7
pubmed: 21310503
PLoS One. 2014 Oct 08;9(10):e107472
pubmed: 25295521
Proc Natl Acad Sci U S A. 2011 May 3;108(18):7511-6
pubmed: 21502500
Integr Comp Biol. 2011 Sep;51(3):456-65
pubmed: 21700571
Ann Bot. 2010 Sep;106(3):439-55
pubmed: 20576737
Evolution. 1974 Dec;28(4):576-592
pubmed: 28564832
Mol Biol Evol. 2002 Nov;19(11):1973-80
pubmed: 12411606
Genet Mol Res. 2015 Jan 30;14(1):680-90
pubmed: 25730005
Curr Opin Genet Dev. 2004 Dec;14(6):675-9
pubmed: 15531163
Mol Biol Evol. 2003 Jan;20(1):18-20
pubmed: 12519901
Biochem J. 2003 Oct 15;375(Pt 2):477-88
pubmed: 12882646
Nature. 2007 Mar 29;446(7135):507-12
pubmed: 17392779
J Mol Biol. 2000 Sep 8;302(1):205-17
pubmed: 10964570
Gene. 2005 Dec 5;362:85-97
pubmed: 16185823
BMC Genomics. 2005 Nov 22;6:165
pubmed: 16303057
J Biol Chem. 1998 Feb 6;273(6):3415-21
pubmed: 9452463
Nat Rev Genet. 2014 Mar;15(3):176-92
pubmed: 24535286
Evolution. 1980 May;34(3):437-444
pubmed: 28568697
Trends Ecol Evol. 1998 Mar;13(3):105-9
pubmed: 21238221
Nat Rev Genet. 2010 Mar;11(3):175-80
pubmed: 20051985
Evolution. 2012 Dec;66(12):3643-57
pubmed: 23206125
Nature. 2010 Jul 22;466(7305):486-9
pubmed: 20592730
PLoS One. 2016 Jun 24;11(6):e0158321
pubmed: 27341348
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
Biol Reprod. 2004 Oct;71(4):1128-34
pubmed: 15175237
J Mol Evol. 1995 Mar;40(3):260-72
pubmed: 7723053
Genetics. 2000 Apr;154(4):1663-79
pubmed: 10747061
Annu Rev Plant Biol. 2009;60:561-88
pubmed: 19575590
Syst Biol. 2002 Jun;51(3):492-508
pubmed: 12079646
J Mol Evol. 2018 Dec;86(9):655-667
pubmed: 30456442
Gene. 2012 Oct 1;507(1):36-43
pubmed: 22841792
Trends Ecol Evol. 2012 Jan;27(1):27-39
pubmed: 21978464
BMC Evol Biol. 2013 Sep 30;13:217
pubmed: 24079728
Trends Ecol Evol. 2004 Jun;19(6):315-22
pubmed: 16701277
Eur J Hum Genet. 1999 Feb-Mar;7(2):255-8
pubmed: 10196713
Mol Biol Evol. 1996 Feb;13(2):397-406
pubmed: 8587504
PLoS Biol. 2004 Dec;2(12):e416
pubmed: 15550988
PLoS One. 2014 Sep 30;9(9):e108433
pubmed: 25268856
Trends Genet. 2008 Jul;24(7):336-43
pubmed: 18514967
PLoS Genet. 2009 Dec;5(12):e1000753
pubmed: 19997497
Mol Biol Evol. 2020 Jun 1;37(6):1547-1562
pubmed: 32076722
Front Genet. 2017 Jan 10;7:227
pubmed: 28119736
Biol Reprod. 1988 Mar;38(2):423-37
pubmed: 3282555
Genet Res. 1992 Apr;59(2):73-80
pubmed: 1628819
Int J Dev Biol. 2008;52(5-6):769-80
pubmed: 18649289
Protein Pept Lett. 2011 Aug;18(8):755-71
pubmed: 21443489
Evolution. 1975 Sep;29(3):411-426
pubmed: 28563177
Elife. 2014 Dec 09;3:
pubmed: 25487987
Proc Biol Sci. 2019 Mar 27;286(1899):20182535
pubmed: 30900533
J Mammal. 2006 Aug 1;87(4):643-662
pubmed: 19890476
Mol Phylogenet Evol. 2005 Oct;37(1):62-72
pubmed: 15927490
J Biol Chem. 1995 Nov 3;270(44):26025-8
pubmed: 7592795
Int J Dev Biol. 2008;52(5-6):781-90
pubmed: 18649290
Nat Rev Genet. 2004 Feb;5(2):114-22
pubmed: 14735122
Syst Biol. 2012 May;61(3):539-42
pubmed: 22357727
BMC Evol Biol. 2019 Jun 27;19(1):135
pubmed: 31248363
Biol Reprod. 2010 Feb;82(2):413-21
pubmed: 19794156
J Hered. 2014;105 Suppl 1:810-20
pubmed: 25149256
Biol Reprod. 2014 Mar 27;90(3):67
pubmed: 24522148
J Clin Invest. 2017 Mar 1;127(3):1046-1060
pubmed: 28218625
Nat Rev Genet. 2005 Aug;6(8):654-62
pubmed: 16136655
Science. 2011 Oct 28;334(6055):521-4
pubmed: 21940861
BMC Evol Biol. 2008 Apr 09;8:105
pubmed: 18400093
Mol Biol Evol. 2004 May;21(5):851-9
pubmed: 14963094
Mol Reprod Dev. 2008 Jul;75(7):1196-207
pubmed: 18247330
Proc Natl Acad Sci U S A. 1997 Jun 24;94(13):6724-9
pubmed: 9192632
R Soc Open Sci. 2015 Dec 16;2(12):150296
pubmed: 27019721
Nature. 2007 Mar 15;446(7133):279-83
pubmed: 17361174
Mol Biol Evol. 2010 Jan;27(1):193-203
pubmed: 19767347
Nucleic Acids Res. 2001 Mar 15;29(6):1352-65
pubmed: 11239002
PLoS Genet. 2008 Aug 01;4(8):e1000144
pubmed: 18670650
Proc Biol Sci. 2009 Jul 7;276(1666):2427-36
pubmed: 19364735
Proc Natl Acad Sci U S A. 2018 May 8;115(19):E4433-E4442
pubmed: 29686068
Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12632-7
pubmed: 10535974
J Biol Chem. 2001 Nov 2;276(44):41502-9
pubmed: 11526117
Evolution. 2005 Nov;59(11):2399-404
pubmed: 16396180
J Biol Chem. 2010 Aug 6;285(32):24863-70
pubmed: 20529856
Science. 2001 Dec 14;294(5550):2348-51
pubmed: 11743200
Heredity (Edinb). 2009 Jan;102(1):1-3
pubmed: 19088743
J Mol Evol. 2010 Sep;71(3):231-40
pubmed: 20730583
Mol Reprod Dev. 1996 Jun;44(2):221-9
pubmed: 9115720
Mol Biol Evol. 2017 Nov 1;34(11):3006-3022
pubmed: 28962009
Mol Ecol. 2011 Dec;20(24):5119-22
pubmed: 22066839
Nature. 2005 Nov 17;438(7066):374-8
pubmed: 16292313
Syst Biol. 2013 Mar;62(2):220-30
pubmed: 23103589
Proc Natl Acad Sci U S A. 2008 Feb 12;105(6):1993-8
pubmed: 18268333
Reproduction. 2016 May;151(5):R55-70
pubmed: 26850883
Curr Zool. 2016 Apr;62(2):145-154
pubmed: 29491902
Trends Ecol Evol. 2006 Jul;21(7):386-93
pubmed: 16765478
Genetics. 2008 Aug;179(4):2075-89
pubmed: 18689890
Proc Natl Acad Sci U S A. 2009 Jun 16;106 Suppl 1:9939-46
pubmed: 19528641
J Evol Biol. 2017 Aug;30(8):1450-1477
pubmed: 28786193
Int J Dev Biol. 2008;52(5-6):511-22
pubmed: 18649264
Heredity (Edinb). 2009 Jan;102(1):66-76
pubmed: 19018273
Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):13875-9
pubmed: 19667210
Front Immunol. 2018 Oct 01;9:2246
pubmed: 30327653
Philos Trans R Soc Lond B Biol Sci. 2010 Jun 12;365(1547):1717-33
pubmed: 20439277
BMC Bioinformatics. 2009 Dec 15;10:421
pubmed: 20003500
Science. 2009 Jan 16;323(5912):373-5
pubmed: 19074312
Mol Biol Evol. 2012 Feb;29(2):457-72
pubmed: 21873298
Science. 1998 Jul 31;281(5377):710-2
pubmed: 9685267
Nat Commun. 2017 Feb 10;8:14363
pubmed: 28186104
Science. 2007 Aug 17;317(5840):910-4
pubmed: 17702935