title: Do the same genes underlie parallel phenotypic divergence in different Littorina saxatilis populations?
abstract: Parallel patterns of adaptive divergence and speciation are cited as powerful evidence for the role of selection driving these processes. However, it is often not clear whether parallel phenotypic divergence is underlain by parallel genetic changes. Here, we asked about the genetic basis of parallel divergence in the marine snail Littorina saxatilis, which has repeatedly evolved coexisting ecotypes adapted to either crab predation or wave action. We sequenced the transcriptome of snails of both ecotypes from three distant geographical locations (Spain, Sweden and United Kingdom) and mapped the reads to the L. saxatilis reference genome. We identified genomic regions potentially under divergent selection between ecotypes within each country, using an outlier approach based on F(ST) values calculated per locus. In line with previous studies indicating that gene reuse is generally common, we expected to find extensive sharing of outlier loci due to recent shared ancestry and gene flow between at least two of the locations in our study system. Contrary to our expectations, we found that most outliers were country specific, suggesting that much of the genetic basis of divergence is not shared among locations. However, we did find that more outliers were shared than expected by chance and that differentiation of shared outliers is often generated by the same SNPs. We discuss two mechanisms potentially explaining the limited amount of sharing we observed. First, a polygenic basis of divergent traits might allow for multiple distinct molecular mechanisms generating the same phenotypic patterns. Second, additional, location-specific axes of selection that we did not focus on in this study may produce distinct patterns of genetic divergence within each site.
authors.affiliation: Animal and Plant Sciences, University of Sheffield, Sheffield, S102TN, UK.
authors.forename: A M
authors.initials: AM
authors.lastname: Westram
authors.forename: J
authors.initials: J
authors.lastname: Galindo
authors.forename: M
authors.initials: M
authors.lastname: Alm Rosenblad
authors.forename: J W
authors.initials: JW
authors.lastname: Grahame
authors.forename: M
authors.initials: M
authors.lastname: Panova
authors.forename: R K
authors.initials: RK
authors.lastname: Butlin
mesh_terms: D000220:Adaptation, Biological / Q000235:genetics; D000818:Animals; D060146:Ecotype; D005828:Genetics, Population; D010641:Phenotype; D020641:Polymorphism, Single Nucleotide; D012641:Selection, Genetic; D017422:Sequence Analysis, DNA; D012908:Snails / Q000235:genetics*; D013030:Spain; D013548:Sweden; D059467:Transcriptome; D006113:United Kingdom
keywords: adaptive divergence; parallel evolution; speciation; transcriptome scan
references.citation: Mol Ecol. 2004 Nov;13(11):3415-24
references.pmid: 15488000
references.citation: J Evol Biol. 2010 Sep 1;23(9):2004-16
references.pmid: 20695960
references.citation: J Evol Biol. 2013 Jul;26(7):1472-87
references.pmid: 23663115
references.citation: Mol Biol Evol. 2013 Nov;30(11):2383-400
references.pmid: 23927992
references.citation: Evolution. 2011 Jul;65(7):1897-911
references.pmid: 21729046
references.citation: Philos Trans R Soc Lond B Biol Sci. 2010 Jun 12;365(1547):1783-800
references.pmid: 20439281
references.citation: Mol Ecol. 2012 Nov;21(21):5265-79
references.pmid: 22681397
references.citation: Bioinformatics. 2009 Aug 15;25(16):2078-9
references.pmid: 19505943
references.citation: Nature. 2012 Jul 5;487(7405):94-8
references.pmid: 22722851
references.citation: Trends Ecol Evol. 2011 Jun;26(6):298-306
references.pmid: 21459472
references.citation: Mol Ecol. 2013 Sep;22(18):4606-18
references.pmid: 23906376
references.citation: Trends Ecol Evol. 2008 Jan;23(1):38-44
references.pmid: 18006185
references.citation: Nat Rev Genet. 2003 Dec;4(12):981-94
references.pmid: 14631358
references.citation: Mol Ecol. 2008 Apr;17(7):1850-70
references.pmid: 18312278
references.citation: Heredity (Edinb). 2009 Oct;103(4):283-4
references.pmid: 19654610
references.citation: Science. 2009 Nov 13;326(5955):998-1001
references.pmid: 19797625
references.citation: Evolution. 2012 Feb;66(2):402-18
references.pmid: 22276537
references.citation: Mol Ecol. 2006 Apr;15(5):1239-49
references.pmid: 16626451
references.citation: Mol Ecol. 2014 Jul;23(13):3133-57
references.pmid: 24845075
references.citation: Mol Ecol. 2009 Feb;18(3):375-402
references.pmid: 19143936
references.citation: Mol Ecol. 2009 Mar;18(5):919-30
references.pmid: 19207246
references.citation: Nat Rev Genet. 2007 Mar;8(3):206-16
references.pmid: 17304246
references.citation: Mol Ecol. 2012 Oct;21(19):4770-86
references.pmid: 22934802
references.citation: Evolution. 2007 Jul;61(7):1600-12
references.pmid: 17598743
references.citation: Evolution. 2008 Feb;62(2):316-36
references.pmid: 17999721
references.citation: Mol Ecol. 2011 Feb;20(3):545-59
references.pmid: 21143332
references.citation: Behav Ecol Sociobiol. 2011 Mar;65(3):461-480
references.pmid: 21423338
references.citation: Evolution. 1995 Dec;49(6):1180-1190
references.pmid: 28568522
references.citation: Science. 2010 Jan 15;327(5963):302-5
references.pmid: 20007865
references.citation: Proc Biol Sci. 2012 Apr 7;279(1732):1277-86
references.pmid: 21976692
references.citation: Mol Ecol. 2014 Feb;23(3):513-21
references.pmid: 24354648
references.citation: Mol Ecol. 2011 May;20(10):2044-72
references.pmid: 21476991
references.citation: Nat Rev Genet. 2014 Mar;15(3):176-92
references.pmid: 24535286
references.citation: Proc Natl Acad Sci U S A. 1995 Mar 28;92(7):2602-6
references.pmid: 7708692
references.citation: Nature. 2008 Oct 2;455(7213):620-6
references.pmid: 18833272
references.citation: New Phytol. 2002 Jun;154(3):591-608
references.pmid: 33873446
references.citation: Genetics. 2010 Sep;186(1):207-18
references.pmid: 20457880
references.citation: Mol Ecol. 2006 Nov;15(13):4021-31
references.pmid: 17054500
references.citation: Trends Ecol Evol. 2001 Mar 1;16(3):148-153
references.pmid: 11179579
references.citation: Evolution. 2014 Apr;68(4):935-49
references.pmid: 24299519
references.citation: PLoS Genet. 2010 Feb 26;6(2):e1000862
references.pmid: 20195501
references.citation: Mol Biol Evol. 2006 Apr;23(4):773-83
references.pmid: 16396915
references.citation: Evolution. 2013 Sep;67(9):2483-97
references.pmid: 24033162
references.citation: Philos Trans R Soc Lond B Biol Sci. 2008 Sep 27;363(1506):2997-3007
references.pmid: 18522915
references.citation: Bioinformatics. 2010 Apr 1;26(7):873-81
references.pmid: 20147302
references.citation: Genetica. 2010 Apr;138(4):409-18
references.pmid: 18777099
references.citation: Mol Biol Evol. 1998 May;15(5):538-43
references.pmid: 9580982
references.citation: BMC Evol Biol. 2012 Jun 22;12:94
references.pmid: 22726891
references.citation: Evolution. 1993 Dec;47(6):1770-1787
references.pmid: 28568008
references.citation: Science. 2000 Jan 14;287(5451):306-8
references.pmid: 10634785
references.citation: Genet Res. 1997 Oct;70(2):155-74
references.pmid: 9449192
references.citation: PLoS One. 2012;7(7):e41901
references.pmid: 22848651
references.citation: Science. 2014 May 16;344(6185):738-42
references.pmid: 24833390
references.citation: Mol Ecol. 2012 Oct;21(20):5042-58
references.pmid: 22989336
references.citation: Proc Biol Sci. 2012 Dec 22;279(1749):5039-47
references.pmid: 23075840
references.citation: Philos Trans R Soc Lond B Biol Sci. 2012 Feb 5;367(1587):409-21
references.pmid: 22201170
references.citation: Philos Trans R Soc Lond B Biol Sci. 2012 Feb 5;367(1587):354-63
references.pmid: 22201165
references.citation: Science. 2005 Mar 25;307(5717):1928-33
references.pmid: 15790847
references.citation: Mol Ecol. 2011 Dec;20(24):5123-40
references.pmid: 22066935
references.citation: Proc Biol Sci. 2011 Nov 7;278(1722):3175-83
references.pmid: 21429920
references.citation: Trends Ecol Evol. 2005 Aug;20(8):435-40
references.pmid: 16701414
references.citation: Mol Ecol. 2004 Jun;13(6):1341-56
references.pmid: 15140081
references.citation: Philos Trans R Soc Lond B Biol Sci. 2010 Jun 12;365(1547):1735-47
references.pmid: 20439278
references.citation: PLoS One. 2011 Mar 11;6(3):e17511
references.pmid: 21412417
references.citation: Nat Commun. 2013;4:1827
references.pmid: 23652015
references.citation: Mol Ecol. 2013 Jun;22(11):2941-52
references.pmid: 23710896
references.citation: Nature. 2012 Apr 04;484(7392):55-61
references.pmid: 22481358
references.citation: Trends Genet. 2004 Mar;20(3):113-6
references.pmid: 15049300
references.citation: Bioinformatics. 2011 Dec 15;27(24):3435-6
references.pmid: 22025480
references.citation: Nature. 2002 May 23;417(6887):440-3
references.pmid: 12024213
references.citation: Heredity (Edinb). 2009 Oct;103(4):285-98
references.pmid: 19623208