Pervasive genetic associations between traits causing reproductive isolation in Heliconius butterflies.
Ecological speciation proceeds through the accumulation of divergent traits that contribute to reproductive isolation, but in the face of gene flow traits that characterize incipient species may become disassociated through recombination. Heliconius butterflies are well known for bright mimetic warning patterns that are also used in mate recognition and cause both pre- and post-mating isolation between divergent taxa. Sympatric sister taxa representing the final stages of speciation, such as Heliconius cydno and Heliconius melpomene, also differ in ecology and hybrid fertility. We examine mate preference and sterility among offspring of crosses between these species and demonstrate the clustering of Mendelian colour pattern loci and behavioural loci that contribute to reproductive isolation. In particular, male preference for red patterns is associated with the locus responsible for the red forewing band. Two further colour pattern loci are associated, respectively, with female mating outcome and hybrid sterility. This genetic architecture in which 'speciation genes' are clustered in the genome can facilitate two controversial models of speciation, namely divergence in the face of gene flow and hybrid speciation.
Merrill
Richard M
RM
Department of Zoology, University of Cambridge, , Downing Street, Cambridge CB2 3EJ, UK. r.merrill@zoo.cam.ac.uk
Van Schooten
Bas
B
Scott
Janet A
JA
Jiggins
Chris D
CD
D000818:Animals; D002080:Butterflies / Q000145:classification / Q000235:genetics* / Q000502:physiology; D003433:Crosses, Genetic; D005260:Female; D008040:Genetic Linkage; D049810:Genetic Speciation; D006824:Hybridization, Genetic; D008297:Male; D010858:Pigmentation / Q000235:genetics*; D012098:Reproduction / Q000235:genetics / Q000502:physiology*; D012726:Sexual Behavior, Animal / Q000502:physiology; D014921:Wings, Animal / Q000254:growth & development
J Evol Biol. 2005 Mar;18(2):247-56
15715831
Evolution. 2003 Mar;57(3):447-59
12703935
Mol Ecol. 2008 Nov;17(21):4699-712
18828780
BMC Biol. 2006 Apr 21;4:11
16630334
Hereditas. 1992;117(2):109-25
1459855
Evolution. 1971 Sep;25(3):471-482
28565031
Science. 1978 Aug 25;201(4357):745-7
17750235
Genetics. 2008 Nov;180(3):1567-77
18791259
Science. 2007 Oct 5;318(5847):95-7
17916732
Heredity (Edinb). 2009 Jan;102(1):4-15
18781167
Proc Natl Acad Sci U S A. 2006 Apr 25;103(17):6575-80
16611733
Evolution. 2009 Jun;63(6):1660-5
19492995
Genetics. 1999 Jun;152(2):713-27
10353912
Genetics. 2002 Aug;161(4):1517-26
12196397
Evolution. 2001 Mar;55(3):512-21
11327159
J Evol Biol. 2007 Jan;20(1):278-85
17210020
Heredity (Edinb). 2009 Jan;102(1):51-6
18813328
Nature. 2006 Jun 15;441(7095):868-71
16778888
Genetics. 2007 Sep;177(1):417-26
17603110
Heredity (Edinb). 2001 Jan;86(Pt 1):68-77
11298817
Nature. 2001 May 17;411(6835):302-5
11357131
Evolution. 2001 Aug;55(8):1631-8
11580022
J Evol Biol. 2004 May;17(3):680-91
15149410
Evol Dev. 2003 May-Jun;5(3):269-80
12752766
Nature. 2001 Aug 30;412(6850):904-7
11528477
Genetics. 2005 Oct;171(2):557-70
15489522
Proc Biol Sci. 2003 Jan 7;270(1510):53-9
12590771
Evolution. 2006 Jun;60(6):1254-68
16892975
Trends Ecol Evol. 2001 Jul 1;16(7):351-358
11403867
J Evol Biol. 2010 Jun 1;23(6):1312-20
20456567
Genet Res. 1996 Oct;68(2):117-23
8940900
Evolution. 1981 Jan;35(1):124-138
28563447
Philos Trans R Soc Lond B Biol Sci. 2008 Sep 27;363(1506):3047-54
18579480
Proc Natl Acad Sci U S A. 2001 Oct 9;98(21):12084-8
11593019
J Evol Biol. 2008 May;21(3):749-60
18312559
Proc Natl Acad Sci U S A. 2009 Jun 16;106(24):9737-42
19487670
Evolution. 1989 Mar;43(2):421-431
28568556
Science. 2009 Nov 6;326(5954):847-50
19892982
Proc Biol Sci. 2001 Sep 7;268(1478):1849-54
11522205