Molecular Diversification of the Seminal Fluid Proteome in a Recently Diverged Passerine Species Pair.
cryptic female choice
fertility
immunity
positive selection
reproduction
selective sweep
sperm competition
Journal
Molecular biology and evolution
ISSN: 1537-1719
Titre abrégé: Mol Biol Evol
Pays: United States
ID NLM: 8501455
Informations de publication
Date de publication:
01 02 2020
01 02 2020
Historique:
pubmed:
31
10
2019
medline:
21
10
2020
entrez:
31
10
2019
Statut:
ppublish
Résumé
Seminal fluid proteins (SFPs) mediate an array of postmating reproductive processes that influence fertilization and fertility. As such, it is widely held that SFPs may contribute to postmating, prezygotic reproductive barriers between closely related taxa. We investigated seminal fluid (SF) diversification in a recently diverged passerine species pair (Passer domesticus and Passer hispaniolensis) using a combination of proteomic and comparative evolutionary genomic approaches. First, we characterized and compared the SF proteome of the two species, revealing consistencies with known aspects of SFP biology and function in other taxa, including the presence and diversification of proteins involved in immunity and sperm maturation. Second, using whole-genome resequencing data, we assessed patterns of genomic differentiation between house and Spanish sparrows. These analyses detected divergent selection on immunity-related SF genes and positive selective sweeps in regions containing a number of SF genes that also exhibited protein abundance diversification between species. Finally, we analyzed the molecular evolution of SFPs across 11 passerine species and found a significantly higher rate of positive selection in SFPs compared with the rest of the genome, as well as significant enrichments for functional pathways related to immunity in the set of positively selected SF genes. Our results suggest that selection on immunity pathways is an important determinant of passerine SF composition and evolution. Assessing the role of immunity genes in speciation in other recently diverged taxa should be prioritized given the potential role for immunity-related proteins in reproductive incompatibilities in Passer sparrows.
Identifiants
pubmed: 31665510
pii: 5610084
doi: 10.1093/molbev/msz235
pmc: PMC6993853
doi:
Substances chimiques
Avian Proteins
0
Types de publication
Comparative Study
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
488-506Subventions
Organisme : NICHD NIH HHS
ID : R21 HD088910
Pays : United States
Informations de copyright
© The Author(s) 2019. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
Références
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
Cell Rep. 2016 Feb 2;14(4):695-707
pubmed: 26776522
Poult Sci. 2016 Apr;95(4):948-55
pubmed: 26769269
Genome Biol. 2009;10(6):R67
pubmed: 19538722
J Proteomics. 2016 Mar 1;135:26-37
pubmed: 26476146
Nucleic Acids Res. 2016 Jan 4;44(D1):D447-56
pubmed: 26527722
Immunol Rev. 2005 Aug;206:306-35
pubmed: 16048557
Trends Ecol Evol. 2001 Jul 1;16(7):364-371
pubmed: 11403869
Syst Biol Reprod Med. 2012 Aug;58(4):218-28
pubmed: 22788534
Proc Biol Sci. 2009 Mar 22;276(1659):1175-81
pubmed: 19129098
Proc Biol Sci. 2008 Sep 7;275(1646):1975-83
pubmed: 18495616
J Mol Evol. 2007 Nov;65(5):555-63
pubmed: 17909693
Genetics. 2005 Nov;171(3):1083-101
pubmed: 16085702
Nat Rev Genet. 2017 Feb;18(2):87-100
pubmed: 27840429
Mol Ecol. 2012 Jun;21(12):3032-47
pubmed: 22582810
Int J Androl. 1996 Oct;19(5):271-7
pubmed: 8985775
BMC Genomics. 2018 Jun 22;19(1):488
pubmed: 29929489
Evolution. 2009 Sep;63(9):2466-73
pubmed: 19453726
Evolution. 2016 Aug;70(8):1844-55
pubmed: 27312694
Mol Ecol. 2016 May;25(9):2015-28
pubmed: 26928872
Evolution. 2013 Dec;67(12):3653-61
pubmed: 24299416
Mol Biol Evol. 2008 Nov;25(11):2301-10
pubmed: 18718917
Mol Ecol. 2011 Sep;20(18):3812-22
pubmed: 21771138
J Insect Physiol. 2009 Jun;55(6):538-43
pubmed: 19232404
Elife. 2019 Jan 08;8:
pubmed: 30620335
Trends Ecol Evol. 2007 May;22(5):266-72
pubmed: 17306413
PLoS One. 2015 Nov 10;10(11):e0140650
pubmed: 26556802
OMICS. 2014 May;18(5):280-97
pubmed: 24660652
Nat Rev Genet. 2002 Feb;3(2):137-44
pubmed: 11836507
Arch Androl. 1996 Mar-Apr;36(2):109-18
pubmed: 8907671
Genetics. 2008 Oct;180(2):921-31
pubmed: 18757944
Mol Biol Evol. 2013 Apr;30(4):772-80
pubmed: 23329690
Biol Reprod. 2000 Apr;62(4):1016-23
pubmed: 10727272
Electrophoresis. 1999 Dec;20(18):3551-67
pubmed: 10612281
Nucleic Acids Res. 2015 Jan;43(Database issue):D447-52
pubmed: 25352553
Heredity (Edinb). 2002 Feb;88(2):85-93
pubmed: 11932766
Science. 2011 Oct 14;334(6053):255-8
pubmed: 21998396
PLoS Genet. 2007 Nov;3(11):e197
pubmed: 17997610
Mol Reprod Dev. 2013 Feb;80(2):80-101
pubmed: 23109270
J Reprod Fertil. 1970 Dec;23(3):375-81
pubmed: 5492024
BMC Genomics. 2014 Mar 12;15:189
pubmed: 24621199
Genetics. 2004 Oct;168(2):1041-51
pubmed: 15514074
J Insect Physiol. 2011 Mar;57(3):409-14
pubmed: 21192944
OMICS. 2012 May;16(5):284-7
pubmed: 22455463
Anim Reprod Sci. 2010 Jul;120(1-4):95-104
pubmed: 20427136
Sci Rep. 2017 Jan 16;7:40236
pubmed: 28091518
Insect Mol Biol. 2009 Aug;18(4):465-75
pubmed: 19453766
Mol Ecol Resour. 2017 Jan;17(1):78-90
pubmed: 27863062
Mol Biol Evol. 2011 Jan;28(1):423-35
pubmed: 20805188
Mol Ecol. 2019 Mar;28(6):1246-1262
pubmed: 30230092
Mol Immunol. 2006 Jan;43(1-2):57-67
pubmed: 16023728
Genetics. 2013 Feb;193(2):501-13
pubmed: 23172857
Parasitol Res. 1992;78(3):215-21
pubmed: 1375380
Mol Biol Evol. 1998 Jul;15(7):901-9
pubmed: 9656489
Proc Natl Acad Sci U S A. 2011 Oct 25;108(43):17743-8
pubmed: 21987817
Science. 2010 Aug 20;329(5994):964-7
pubmed: 20724639
Bioinformatics. 2017 Jul 1;33(13):2037-2039
pubmed: 28205675
Genetics. 2007 Nov;177(3):1321-35
pubmed: 18039869
Mol Cell Proteomics. 2019 Mar 15;18(Suppl 1):S46-S58
pubmed: 30287546
Infect Immun. 2003 Nov;71(11):6648-52
pubmed: 14573690
J Biol Chem. 2010 Jan 15;285(3):2184-92
pubmed: 19920146
Mol Biol Evol. 2012 Aug;29(8):1969-73
pubmed: 22367748
Clin Gastroenterol Hepatol. 2014 May;12(5):749-55
pubmed: 24632348
J Reprod Fertil. 1964 Aug;8:39-47
pubmed: 14195706
PLoS Biol. 2008 Jul 29;6(7):e178
pubmed: 18666829
Biol Lett. 2011 Oct 23;7(5):740-2
pubmed: 21490006
Hum Genomics Proteomics. 2009 Dec 08;2009:null
pubmed: 20948568
Dev Cell. 2018 Aug 20;46(4):481-494.e6
pubmed: 30057273
PLoS Genet. 2014 Apr 17;10(4):e1004234
pubmed: 24743097
Trends Ecol Evol. 2017 May;32(5):368-382
pubmed: 28318651
BMC Genomics. 2017 Dec 2;18(1):931
pubmed: 29197336
Proteomics. 2009 Apr;9(8):2085-97
pubmed: 19322787
Nature. 2012 Nov 15;491(7424):444-8
pubmed: 23123857
Curr Top Dev Biol. 2019;135:287-313
pubmed: 31155361
J Biol Chem. 2011 Oct 21;286(42):36875-87
pubmed: 21880732
J Insect Physiol. 2001 Jun;47(6):617-622
pubmed: 11249950
Dev Biol. 2006 Aug 15;296(2):279-97
pubmed: 16828734
BMC Bioinformatics. 2008 Dec 09;9:529
pubmed: 19068132
Nat Genet. 2011 May;43(5):491-8
pubmed: 21478889
Evolution. 2013 Aug;67(8):2348-62
pubmed: 23888856
Mol Ecol. 2011 Sep;20(18):3823-37
pubmed: 21762432
Ecol Lett. 2009 Jan;12(1):5-12
pubmed: 19087108
Mol Ecol. 2014 Dec;23(23):5831-42
pubmed: 25208037
Bioinformatics. 2015 May 15;31(10):1544-52
pubmed: 25653249
Mol Biol Evol. 2008 Jan;25(1):207-19
pubmed: 18032407
Annu Rev Entomol. 2011;56:21-40
pubmed: 20868282
Int J Dev Biol. 2008;52(5-6):769-80
pubmed: 18649289
Nat Genet. 2016 Oct;48(10):1204-10
pubmed: 27548311
Mol Ecol. 2013 Mar;22(6):1640-9
pubmed: 23294288
J Cell Biol. 2014 Sep 1;206(5):671-88
pubmed: 25154396
PLoS One. 2011 Jan 25;6(1):e15720
pubmed: 21283577
Poult Sci. 2013 Aug;92(8):2174-81
pubmed: 23873566
Nat Genet. 2006 Dec;38(12):1440-5
pubmed: 17099714
Scand J Immunol. 2000 Sep;52(3):240-8
pubmed: 10972899
Bioinformatics. 2005 Mar 1;21(5):650-9
pubmed: 15388519
Biol Reprod. 2017 Jan 1;96(1):2-12
pubmed: 28395326
Bioinformatics. 2011 Aug 1;27(15):2156-8
pubmed: 21653522
Cold Spring Harb Perspect Biol. 2011 Nov 01;3(11):a002931
pubmed: 21730046
J Proteomics. 2016 Mar 1;135:12-25
pubmed: 26074353
Evolution. 2015 Apr;69(4):1044-52
pubmed: 25655075
Mol Biol Evol. 2015 Jan;32(1):244-57
pubmed: 25246699
Sci Rep. 2019 Apr 10;9(1):5852
pubmed: 30971704
Proc Biol Sci. 2018 Aug 8;285(1884):
pubmed: 30089626
Proteomics. 2010 Jun;10(12):2396-401
pubmed: 20391540
J Reprod Fertil. 1992 Mar;94(2):287-93
pubmed: 1593530
Annu Rev Genet. 2013;47:97-120
pubmed: 24274750
Proteomics. 2010 Mar;10(6):1150-9
pubmed: 20101611
Ecol Evol. 2016 Jun 28;6(15):5190-206
pubmed: 27551376
Biol Rev Camb Philos Soc. 2011 May;86(2):367-77
pubmed: 20659104
Evolution. 2013 Dec;67(12):3523-36
pubmed: 24299405
BMC Genomics. 2017 Jan 18;18(1):98
pubmed: 28100167
Curr Biol. 2013 Oct 7;23(19):1853-62
pubmed: 24076241
PLoS One. 2007 Aug 15;2(8):e734
pubmed: 17710134
PLoS Negl Trop Dis. 2011 Mar 15;5(3):e989
pubmed: 21423647
Proc Natl Acad Sci U S A. 2005 May 3;102 Suppl 1:6550-7
pubmed: 15851678
Mol Cell Proteomics. 2013 Nov;12(11):3052-67
pubmed: 23816990
Genome Biol. 2006;7(5):R40
pubmed: 16709260
Integr Comp Biol. 2007 Sep;47(3):427-45
pubmed: 21672851
Biol Rev Camb Philos Soc. 2019 Nov 18;:null
pubmed: 31737992
Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12632-7
pubmed: 10535974
Insect Biochem Mol Biol. 2009 May-Jun;39(5-6):366-71
pubmed: 19328853
Bioinformatics. 2004 Jun 12;20(9):1466-7
pubmed: 14976030
Bioessays. 2015 Feb;37(2):142-7
pubmed: 25379987
Proteomics. 2013 Jan;13(1):22-4
pubmed: 23148064
Reproduction. 2013 Jun 14;146(1):R21-35
pubmed: 23613619
Theriogenology. 1992 Dec;38(6):1107-14
pubmed: 16727208
Proc Natl Acad Sci U S A. 2001 Jun 19;98(13):7375-9
pubmed: 11404480
Am Nat. 2013 Oct;182(4):552-61
pubmed: 24021407
J Evol Biol. 2017 Aug;30(8):1450-1477
pubmed: 28786193
J Mol Biol. 2016 Feb 22;428(4):688-692
pubmed: 26434508
Mol Cell Proteomics. 2019 Mar 15;18(Suppl 1):S6-S22
pubmed: 30552291
J Med Microbiol. 2008 Nov;57(Pt 11):1405-10
pubmed: 18927420
Sci Rep. 2016 Nov 02;6:35864
pubmed: 27804984
PLoS Negl Trop Dis. 2014 Jun 19;8(6):e2946
pubmed: 24945155
Trends Ecol Evol. 2014 Jan;29(1):51-63
pubmed: 24139972
Nature. 2014 Jan 2;505(7481):103-7
pubmed: 24256734
Sci Adv. 2017 Jun 14;3(6):e1602996
pubmed: 28630911
Mol Biol Evol. 2000 Jan;17(1):68-74
pubmed: 10666707
J Proteomics. 2019 Feb 20;193:192-204
pubmed: 30366121
PLoS One. 2015 May 14;10(5):e0127007
pubmed: 25973848
J Innate Immun. 2018;10(5-6):455-464
pubmed: 30149378
Comp Biochem Physiol B. 1991;98(4):549-53
pubmed: 1714367
Genetics. 2010 Feb;184(2):401-10
pubmed: 19917764