Accepted Article Introgression Adaptive Supergenes, selection, dependent Frequency Linkage, Mate choice, Keywords polymorphisms colour on selection Sexual head: Running [email protected] Email: author *corresponding SWEDEN SWEDEN 2 1 Maren Wellenreuther* ReviewsSyntheses and Invited : typeArticle 19-Sep-2014 : Date Accepted Revised Date : 17-Sep-2014 08-Jun-2014 : Received Date This article This protectedis by Allcopyright. rights reserved. 10.1111/mec.12935doi: lead to differencesthis between version and the Version of Record. Please cite this article as through pagination typesetting, maywhich thecopyediting, been andproofreading process, articleThis has been publicationaccepted for and fullundergone peer review but has not and analysis technology in sequencing advances and divergence speciation. With population selection, nature, in changes frequency allele to measure markers visual were used as simple colourmorphs regimes. Traditionally, to complex selection and often subjected across animals widespread are Genetic colour polymorphisms Abstract Molecular Ecology, Department of Biology, Lund University, SE-223 62 Lund, 62 Lund, SE-223 University, Lund Biology, of Department Ecology, Molecular 62Lund, SE-223 University, Biology, Lund of Department Ecology, Evolutionary Sexual selection andgeneticcolour : Colour polymorphisms, Sexual selection, Recombination, Inversions, Inversions, Recombination, selection, Sexual : polymorphisms, Colour polymorphisms in animals 1 , Erik I Svensson Erik I, 1 and Bengt Hansson 2 Accepted Article genetics era (Ford 1945). By following morph Bygenetics era in over morph frequencies following (Ford natural populations 1945). ecological pre-molecular in were popular systems study the and unnoticed, they The suitability of genetic colour polymorphisms as marker phenotypes did not go wild. the in selection examining for markers visual easyprovide and thus individuals of number alarge in unambiguously be can scored morphs colour discrete havea heritability. high and basis show many genetic simple Second, colour morphs First, several reasons. processes for evolutionary tostudy idealsystems model 1) constitute and (Figure nature ubiquitous in are polymorphisms colour Genetic Introduction maintenance. ofsexualselection onpolymorphism evolutionary consequences intoinsights the of colourgain to targets sexual oncolourof withtheunderlying molecular selection consequences fitness integrate explicitly that needed are more studies that highlight We polymorphisms. fuelling in variation regulatory and introgression of role the and determination, or sex preferences and mate loci colour between linkage include findings interesting Other structures. supergene and inversions of case as inthe such loci, trait withother loci colour of tightclustering of importance the towards point polymorphism colour of architecture theof genetic Studies these. by constrained or be facilitated might suchpolymorphisms of maintenance how the discuss (3) diversification and phenotypic colour basis underlying developmental and molecular architecture, genetic the highlighting (2) polymorphisms, on colour sexual selection of the evidence at (1) reviewing aiming polymorphisms, colour sexually selected we Here areselection discuss described. studies on recent being the genetics of of targets molecular wherethe emerging are systems model several methods, This article This protectedis by Allcopyright. rights reserved. laboratory classical of equivalent are the field polymorphisms colour of heritable studies Inthis sense, 1961). 1945; Kettlewell Ford and space (e.g. changes over time frequency infer allele and thus frequencies scientists easily genotype could observe generations, multiple genetic diversity genetic diversity (Hughes maintaining and fitness specific morph altering thereby selection, correlational and NFDS through interactions mating sexual affect commonly morphs of the colour is finding Yetanother that 1961). 1945; Kettlewell (Ford a have selective advantage morphs therare where (NFDS) selection dependent frequency negative This causes the more frequently than rare morphmorph. upon whereby the common is preyed and aposematism, mimicry crypsis, camouflage, ofe.g. selection interms natural by affected are often morphs colour these studiesisthat from general finding A 2012). Stuart-Fox & (Hugall negatively or positively either rates, extinction and/or rates speciation affect can polymorphisms maintaining and generating processes the 2010) and that & Pierotti inMcKinnon traits (reviewed with other correlated Hughes 2009; Svensson & (Gosden scales time over short selection and sexual natural strong to be exposed can morphs colour that shown have and since approach were used tophenotypes study evolution. this Several studies have employed et al. et 2013; Iserbyt 2013; et al. etal. 2013; 2013; Iserbyt 2013), that colour morphs are often genetically genetically often are morphs colour that 2013), Drosophila studies, in which visual eye marker eye marker which visual in studies, et al. et

2013; Ducrest 2013; Roulin & 2013; Accepted Article reasons) that the absence of sex limitation indicates a sex indicates lack sexual selection. of limitation that of the absence reasons) or incorrect correct (for assumed then and researchers expression, their sex in one to restricted arenot polymorphisms colour thatmany fact the reflect partly might selection natural towards bias 2). This Figure 1961, Kettlewell (e.g. abiotic factors tovarious and inrelation risk predation of terms in tradition genetics ecological population (i.e. polychromatism), with the rarest morph being too common to be the toocommon being morph with the rarest (i.e.polychromatism), population an within interbreeding coexisting in at least one sex adult morphs discrete two atleast of co-occurrence the as define we which polymorphisms colour heritable focus on We substitutions. nucleotide specific and the genes in even to mutations cases, exceptional insome or regions, genomic to mapped been have loci colour andthe in maintenance role their apotential to play has been selection suggested where sexual polymorphisms colour ongenetic studies Here recent we review gene networks. integrated nodes in central form they whether and/or patterns dominance vicinity, their the genes in selected chromosomal linked to other are tightly they whether effects, pleiotropic multiple show pigmentation in involved thegenes whether to according influenced will be on coloration selection to response evolutionary the example, For particular. in selection and sexual general, in selection to genes colour of responses theevolutionary the study of we improve can basisof colour traits, molecular al. and genes underlying mutations have been identified (e.g. Kunte the cases some in and species polymorphic several in described been recently has colour of location genomic the advances, Dueto these resources. genomic available of absence by the been impeded has research where organisms, non-model many the for relevant particularly are advancements colouration. These of basis genetic the into delve to opportunity unprecedented an offer technologies genomic emerging as rapidly is Thissituation changing these of traits. evolution the into insights deeper basis colour of our ability inmostpolymorphic has hampered systems to develop genetic themolecular about knowledge lackof However, fitness. and phenotypes between covariance on the acts selection of how multivariate understanding our increased 2010). These insights significantly & Takahashi have Watanabe This article This protectedis by Allcopyright. rights reserved. betularia moth peppered on the studies polymorphism classiccolour most For instance, was to onselection assumed polymorphisms. operate natural Traditionally, colour genetic colour polymorphisms Evidence ofcolour assortative ma patterns. incolour diversity sexual of genetics the on light shed promise to that systems emerging highlight also research. We future for priorities and gaps knowledge identify and to theory sexualselection tothe data genomic emerging the integrate conceptually isto review this key of focus The guppy). (e.g.the axis aalong continuous more instead varies but discrete, truly not is variation which colour speciesfor polymorphic studies on we 1955). In instances, also some mutations cover (Huxley of recurrent product 2011). With this new knowledge and much improved methods for elucidating the forelucidating methods improved this new and much 2011). knowledge With and the grove snail snail grove the and Cepaea

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et al. et 2014; Reed Biston Biston et Accepted Article lesser snow goose lesser snow arctic skua polymorphic asthe such other birds, several shown in been hasalso colour by mating mating. Assortative assortative maintain to helps and interbreed the morphs when associations downthese breaking from association recombination 2010). Thisthe genetic (Pryke prevents Z chromosomes on hybrids intermorph of fitness low and expression colour preferences, mating of inheritance coupled the through flow gene some despite maintained are preferences gouldiae finch the Gouldian of morphs head colour the include mating assortative of Examples rare. isgenerally mating disassortative while taxa, diverse across manifold is the mating literature is that colour assortative clear emerges from A that pattern been quantified. on selection have colour aspects sexual where of examples weBelow and in 1, list Table representative some This article This protectedis by Allcopyright. rights reserved. is combined coloration conspicuous where species several of existence the despite so far, colourof maintenance aspect unexplored a inNFDS relatively is aggression described in another polymorphic cichlid species (Dijkstra polymorphic cichlidspecies in described another been whathas to similar preference on by NFDS female creating polymorphism afemale-preference of evolution the to contribute which could biases, aggression morphs (plain, orangeor white blotched morphs)have significant own-morph (Roberts locus determining sex female a dominant to pattern blotch the of linkage tight by resolved can be conflict sexual the that has shown Malawi in Lake polymorphism blotch/plain on the (Roberts recognition mate for used patterns malespecific colour while blotches males reducein byspecies- fitness habitat background, disrupting mottled the against crypsis provide females in blotches because conflict a sexual by caused is species cichlid some in females blotched of predominance The mating. (Lande occurs polymorphism the which for all species nearly in populations natural in males blotched of scarcity (Pierotti experiments choice is Midas complex inthe species studied best probably The 2004). Meyer & (Barluenga morphs between differentiation genetic mating significant cichlidcreates and assortative in complex Nicaragua Midas the is found in polymorphism The barred/gold polymorphisms. blotch/plain and barred/gold the displaying cichlids in beendemonstrated has mating assortative (Krüger choice imprinting onmate based sexual with non-genetic coupled advantage, heterozygote by maintained is polymorphism et al. suggesting a balanced polymorphism 1983). acichlid (Barlow The balanced suggesting polymorphism 10%), are they present of in (around population the populations most species, the of percentage asmall up only makes morph thegolden Although colouration. the body pairs same share of breeding 95% around in species 1973) and this (Barlow morph barred white and black widespread amore with morph co-segregates morph frequencies in the wild (Seehausen the in frequencies morph comes from species inthis mating assortative colour Evidence for Lake cichlids. African other in several found isalso polymorphism identical an and interestingly, female, predominantly are morphs blotched the though 1D), (Figure morphs blotched omnicaeruleus 2001; Mundy 2001; . Both red and black morphs mate colour assortatively and colour and colour assortatively mate colour and black morphs red Both . in Lake Victoria occurs either as a plain brown or as one of two orasone of two brown asa either plain occurs Victoria Lake in Anser c. caerulescens c. Anser et al. et et al. et et al. 2004, Table 1). In the latter case, the plumage plumage the case, 1). latter the In Table 2004, etal. 2009). Interestingly, females of the three colour colour three the of females Interestingly, 2009). 2009; Seehausen 2009; 2001) limits the opportunity for assortative assortative theopportunity for limits 2001) and common buzzard and common Amphilophus citrinellus, Amphilophus et al. et 1999b) and from laboratory mate mate laboratory and from 1999b)

etal. et al. et etal. Stercorarius parasiticus Stercorarius 2001). In fish, colour 1999b). However, the Buteo buteo buteo Buteo 2010). Therole of et al. et where a golden a where golden 2009). Work 2009). Work Neochromis Erythrura Erythrura (Krüger ,

Accepted Article are also common in many butterflies (e.g. (e.g. butterflies inmany common also are white-throated sparrow sparrow white-throated (Pryke finch Gouldian such asinthe behaviour, with aggressive This article This protectedis by Allcopyright. rights reserved. & (Gosden common Sánchez-Guillén Svensson 2009; is harassment mating male pre-copulatory where males, and lower rates than mating from benefit females where rates, mating optimal over conflict sexual of result bethe in and general, in in damselflies polymorphism (Svensson disadvantages facewhereby fitness the common female morphs frequency-dependent, are they that 2008) Svensson & Gosden 2009; Svensson & (Gosden spatially and temporally vary of morphs rates mating that demonstrated have damselfly elegans Ischnura damselfly blue-tailed is the maintenance polymorphisms and colour selection species (Fincke 100 than more for described hasbeen polymorphism colour trans-species odonates, (Galeotti polymorphism female-limited birds, 23 In show species Tsubaki 2000). & females access(Plaistow to receptive for competition inmale–male arole plays males, it mostly in found exclusively polymorphisms (Svensson polymorphisms colour female-limited of and maintenance generation the implicated in been rates has mating optimal over conflict Sexual common. are polymorphisms colour and male-limited both female- variation, colour with sex-limited In species 2003). (Tuttle population the in 50/50% at roughly polymorphism the maintains mating disassortative (Huynh the inversion tan in both sexes 1), and morphs white(Table areheterozygous for since morphs and white separates inversion chromosomal A morphs. with tan-striped mate always almost morphs white-striped that ensures mating disassortative Here 1C). (Figure sparrow the of white-throated morphs crown stripe the white and tan comes from mating disassortative of example best probably The rare. are systems polymorphic from 1), but examples (Box phenotypes of rare loss the prevent alone matingcan disassortative mating, assortative Unlike 1996). Lively & (Sinervo strategy sneaker a yellow adopt and males guarders mate are monogamous blue usurpers, territorial are Orange males NFDS: isunder strategy male mating The neighbourhood. social intheir male dominant theby other males of exclusion competitive wildby inthe overridden is preference but 2007) this Sinervo (Bleay & laboratory stansburiana lizard side-blotched the of morphs colour the throat is case 1). One (Box morphs between mating assortative and morphs on colour selection sexual separated clearly that have polymorphisms on colour studies quantitative is rigorous Therea lackof NFDS 2). with (Figure of or some form buzzard, selection or correlational co-occur common as inthe such advantage with heterozygote be linked needs to it For this, (Box 1). does not alone mating polymorphism help assortative to maintain however, ofreproduction, is used pursuit in species the polymorphic inthat colour several demonstrate mating assortative colour describing examples aforementioned The (Figure 1A). Here females show a preference for colour matching inthe matching colour for apreference show Herefemales 1A). (Figure et al. , which has three female morphs (Figure 1B). , which on 1B). has Studies (Figure this three female morphs et al. et Zonotrochia albicollis albicollis Zonotrochia 2005). An emerging odonate model system for sexual sexual for system model odonate emerging An 2005). et al. et et al. 2011), while tan-striped birds are homozygous, birds are homozygous, tan-striped while 2011), 2009), while when colour polymorphism is polymorphism when colour while 2009), 2005). The prevalence of of female The colour prevalence 2005). et al. et Papilio polytes Papilio 2003), and female-limited colour morphs colour morphs and female-limited 2003), (Figure 1C) (Tuttle 2003, see below). 2003, see below). 1C) (Tuttle (Figure I. elegans elegans I.

et al. et ) and odonates. In fact, in in fact, In odonates. and ) in particular, is thought isthought to particular, in 2013b). By contrast, By contrast, 2013b). et al. 2007) and the and the 2007) Uta Uta Accepted Article purging disadvantageous alleles, except when sexual selection is negatively negatively is selection sexual when except alleles, disadvantageous purging or alleles fixing advantageous by either allele frequencies selection alters Sexual frequencies. orgenotype alter allele they how particularly genetic consequences, of their population processes terms in different two these todefine convenient itmost find particular. We in colourmorphs of the study and in general, in both other, each affect can they how and differ how they we clarify Below, systems. polymorphic Sexual selection in are associatedmales with polychromatism (Lank plumage ruff isthe polymorphism (Hughes selection mediated sexual by NFDS demonstrating thus mates sire more andoffspring, also more acquire patterns colour with rare males to show that able were populations guppy of the polymorphism Tsubaki In the male-limited & (Plaistow 2000). comparable is success reproductive lifetime estimated the however, male morphs, of lifetime less. the span and life is Across longevity reproductive buttheir Tsubaki 2000) (Plaistow & rate dailyhave mating ahigher and males thanclear-winged larger are males Orange-winged males. 'sneaker' clear-winged non-territorial or males damselfly mating. of the This is Japanese the colourcase inpolymorphism the male-limited for females intercepting succeedsin and andphenotype inbehaviour females conspecific resembles that male a‘sneaky’ and male fighter a territorial include often Gossum (Van rare more are polymorphisms colour male-limited This article This protectedis by Allcopyright. rights reserved. mating ofassortative effect selection This sexual homozygotes). (rare morphs rare disfavours that selection stabilizing or directional through selection, sexual influence with and interfere also can mating Assortative advantage. mating dependent afrequency- obtain (genotypes) morphs rare if diversity, genetic maintain can mating”) assortative called mating “negative (sometimes In disassortative contrast, polymorphisms. genetic over theother, and does not also favour one allele maintain in does not, itself, mating Assortative heterozygotes. at of the expense populations, local in homozygotes of frequency the increases mating”) assortative “positive called (sometimes morphs similar between mating Assortative subpopulations. among fragmentation demographic due to arises mating non-random where 2005) Troy & structure (Hendry population & 2012) or Bolnick temporal (Snowberg spatial to due arise simply canit to,and need does not it choice,but mate alters mating Assortative rare morphs, have higher fitness. alleles, i.e. rare of asthe bearers drift, genetic by thepopulation from lost being from alleles rare rescues NFDS Incontrast, alleles. certain by favouring variation, genetic erode but diversity, rather not genetic do maintain classicalof selection sexual forms forms These pool. gene thelocal of frequencies allele the may change selection inwhich or case maybe directional stabilizing, selection Sexual maintained. is insteadgeneticbeing variation and over generations in allele frequencies change long-term directional no net be will there whichcase in frequency-dependent, Poecilia reticulata Poecilia Box 1: Disentangling sexual selection from assortative mating mating assortative from selection sexual Disentangling Box 1: Mnais costalis and and et al. assortative mating assortative where morphs include territorial orange-winged 'fighter' 'fighter' orange-winged include territorial where morphs genotype frequencies genotype Philomachus pugnax Philomachus , replicated experimental manipulations of natural natural of manipulations experimental replicated , 2013). Another for male-limited example famous 2013). Another are two important processes in colour colour in processes important two are where alternative mating strategies mating strategies alternative where . Assortative mating can result fromcan result mating Assortative .

et al. 1995). 1995). et al. et 2008) and and 2008) Accepted Article melpomene, H.cydno melpomene, Table1), though most species in this genus vary along geographic gradients (e.g. (e.g. morphs colour co-occurring have sympatrically change. Molecular work change. onMolecular wing patterns in colour evolutionary rapid prone to facilitate genesare unusually that some demonstrating inthisgenus, patterns wing distinct of hundreds code for regions genomic genus the of Neotropical butterflies defended andchemically of the brightly coloured clade from diverse morphs comes colour underlying architecture asupergene of cases documented best the One of phenotypes. colour alternative of production the control supergenes where cases representative describe some insertions, duplications, and translocations (Schwander translocations and duplications, insertions, deletions, inversions, as chromosomal such variations structural by beenhanced whichreside, can they where region chromosomal rate inthe recombination effective the is importance particular but of loci, between distance physical on the depends clusters linkage these supergene of in degree The intermediates. non-optimal create combinations that allelic and preventing phenotypes yet complementary separate for hardcoding thereby unit, intoone segregating genes link multiple supergenes colour loci clusterwith functionally unrelated genes to formsupergenes. Such many shown that has methods sequencing wide genome of advent The recent colour colour Emerging knowledge aboutgenomics as NFDS. of balancing by such selection, some form are probably maintained polymorphisms most sparrows), white-throated (e.g. systems some in polymorphisms colour maintain might mating disassortative although Finally, maintained. are being orthat initself these morphs selection provides hard any evidence sexual notdemonstrate speciesdoes polymorphic a within colour assortatively mate that morphs demonstrating being lost. Conversely, from the polymorphism protects nor mating assortative morph requires which neither success, mating higher have some morphs requires that morphs on sexual colour selection of demonstration a instance, For other. each with interact might how they and investigate processes theseof different importance relative should try the quantify systems to polymorphic colour mating in assortative and selection on sexual empirical studies Future Nuismer 2004). & (Kirkpatrick phenotype own their of mates finding in disadvantage dependent frequency a willexperience morphs rarer asthe mates, of costs the affects search This article This protectedis by Allcopyright. rights reserved.

Supergenes, inversions and tight linkage linkage tight and inversions Supergenes, and The genetic architecture of colour of colour architecture The genetic H. erato H. ). Genetic mapping has revealed that only a few afew only that has revealed mapping ). Genetic Heliconius . Some of the species in this group group inthis thespecies of Some . and genetic architecture of

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has H. H. Accepted Article P. memnon hindwing tailsin aswellof andthe presence asbodyhindwing, colour forewing and dardanus In the species. related closely even in ways, loci in in bands forewing white versus melpomene (Naisbit control colour in implicated also are groups linkage different several loci on however, species, yellow wing pattern in with major loci the mimicry ( orthologous (Joron loci ancestral linked loosely previously between linkage increasing by assembled have been towhich locus, switch appears a supergene identified single This article This protectedis by Allcopyright. rights reserved. (Seehausen infemales fixed hasbecome although morph some in thespecies blotched the condition, ancestral usually a possess also plainsexes, which inboth morph thelatter of is considered both) or white-blotched (orange-, blotched morphs with 1).Species (Table Victoria and Malawi Lake cichlids occupying of polymorphism supergene blotch suchas the species, fish polymorphic colour several in implicated been also have Supergenes wing pattern of this butterfly (Kunte work detailed that showed subsequent and polypeptides, sex-specific encoding related mRNAs spliced alternatively producing by differentiation sexual somatic regulates that factor transcription a gene, with five genes (Kunte region 300 kb a to location supergene the down narrow able to was tails, hindwing of in locus supergene Pushmipullyu locus the supergene for rearrangements chromosomal possible three create 15 group that on linkage two nested inversions consistsof supergene 2006). The long-held view that supergenes are controlled by a tightly linked cluster of several several of cluster linked a by tightly controlled are supergenes view that long-held (Joron pattern a single gene. The region identified by Kunte Kunte by identified region The gene. a single within mutations linked tightly of multiple, be composed indeed may (1972) Sheppard and by Clarke loci proposed scenario linked the multiple that loci, suggests and essential components for the ancestral function (Kunte for the function ancestral components essential codingparts, suchas the DNA-binding motif or dimerizationdomains, which are key of preservation the through possible waspresumably processes, developmental That butterflies. andnon-mimetic mimetic between protein the doublesex in differences structural ledto haswhich likely mutations, differing accumulate and to thereby alleles allowing to distinct inversion heterozygotes, from eachremain other the flanking breakpoints with the and alleles the mimicry harbouring polymorphism aninversion with signatures consistent data revealed re-sequencing genome whole of analyses and recombination as

a supergene controller a supergene Heliconius Papilio underlie a supergene that controls different colour elements of theof elements colour different controls that supergene a underlie control red wing colour, while while control wingcolour, red (Jones , or simply butterfly group, geographic colour phenotypes in phenotypes colour geographic group, butterfly et al. et demonstrates that phenotypic variation can be achieved in different indifferent beachieved can variation phenotypic that demonstrates P. polytes et al. et 2011; Joron 2011; et al. et al. H. melpomene P , each one of them corresponding to a specific wing colour wing colour toaspecific corresponding them of one , each 2011). Extensive genomic work on a similar colour asimilarcolour workon genomic Extensive 2011). 2014). One gene is the sex determining determining sex isthe gene One 2014). 2003). For instance, instance, For 2003). , , despite being a fundamental gene controlling gene controlling beinga despite fundamental

which controls wing colour pattern and the presence presence the and pattern colour wing controls which H. cydno et al. et etal. etal. dsx , dsx H. cydno H. 2014). This finding is in stark contrast to the the to contrast in stark is finding This 2014). (Naisbit 1999b). The orange-blotch and plain plain and orange-blotch 1999b). The gene. Inversions prevent recombination in recombination prevent gene. Inversions alone acts like a switch between different different between acts like a alone switch Yb, Sb, N Sb, Yb, 2006). The genomic location genomic The 2006). K et al et on linkage group 01 controlsyellow et al. et and B . (2014) was further shown to lack lack to shown was further (2014) . and and

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Accepted Article caused by loss of function mutations in the melanocortin 1 receptor ( receptor 1 themelanocortin in mutations function of by loss caused cases are insome polymorphisms, being intraspecific some species, mammalian colours many in and dark coat theyellow/light For example, exists. some evidence but is more limited, polymorphisms of genetic colour evolution in the duplications inBraasch (reviewed families gene pigmentation of evolution the for beimportant to shown has been CNVwhere isacase which in duplication teleost fish, whole-genome the includes example and oneextreme taxa across widespread is (CNV) variation number Copy paralogue. derived newly the of novel functions of evolution allow turn in can andthis constraints, pleiotropic the one copies of release may onegene copy from more than having Moreover, having or few manyindividuals gene differences between copies. expression cause can events which duplication gene historical with may associated be polymorphisms Such ancestral ancestry. common this is explanation for straightforward most andthe taxa, incloselyrelated colour polymorphism of causative frequently same genes are the that toshow arecolour starting genes studieson Genomic above). section (see 2003) (Tuttle NFDS through of mate choicemorphs is sparrow preferences ensured disassortative through white-throated in the supergenes alternative of Maintenance cluster. supergene the within reside traits behavioural these for coding genes the possible) certainly (but whether unclear isyet it although preferences, and mate traits behavioural (Huynh genes of hundreds birds; thus includes passerine in chromosome which is the largest fuelleborni between cross an interspecies using was investigated polymorphism This article This protectedis by Allcopyright. rights reserved. boundaries through introgression. Candidate groups for adaptive introgression of introgression adaptive for groups Candidate introgression. through boundaries acrossspecies alsogenes spread colour can polymorphism, ancestral to In addition 2010; Linnen Schöneberg (Hofreiter & of region promoter within the or mutations gene duplication due to either of expression by increased caused sometimes of the of gene theski with proto-onco associated tightly 30 (Streelman cM approximately paracentric inversions and (ZAL2 inversions ZAL2 paracentric sparrow the white-throated of polymorphism plumage the is asupergene of colour example aIn birds, striking isolation. reproductive of the build-up in abeen key component has choicelikely mate characters and putative of colour, genetic proximity themorphology colour), close (e.g. nuptial patterns on colour and selection sexual morphology) feeding (e.g. traits ecological on selection natural of forces combined involved the probably cichlid speciation Giventhat 2001). Kocher & (Carleton genes opsin threecone of array a tandem (Albertson shape tooth for locus trait quantitative a to proximity close pax7 pax7 and gene (Roberts gene Gene duplications and introgression of colour genes genes of colour introgression and Gene duplications et al. et Metriaclima zebraMetriaclima 2011). Alternative phenotypes in this species differ in differ several species inthis phenotypes 2011). Alternative

etal. (Figure 1C, Table 1). This supergene is regulated by two two by isregulated 1). This supergene 1C,Table (Figure , and could be mapped to a linkage group spanning spanning group alinkage to be mapped and could , etal. 2009; 2009; Streelman et al. et m 2003). The orange-blotch was to shown be The orange-blotch 2003). ) that span almost 90% of span chromosome of almost ) that 90% two, 2009). 2009). c-ski1 etal. Asip et al. et

, and thus production of ASIP, ASIP, of production thus and , and a cis-regulatory mutation and mutation a cis-regulatory 2007). An explicit role of gene of role explicit An 2007). 2003). These genes lie in in lie genes These 2003). etal. Labeotropheus Labeotropheus 2005) and and 2005) mc1r Asip ), ), Accepted Article coalescent analysis indicates repeated introgression of alleles from of alleles from introgression repeated indicates analysis coalescent heurippa association in genotype-phenotype locus, colour Pardo-Diaz red the to unlinked and linked regions sequencing By radiation. wing pattern mimetic Heliconius in patterns wing red regulating on gene studies the Recent hybridizing species. and related closely contain often they since radiations, adaptive are genes colour This article This protectedis by Allcopyright. rights reserved. (e.g. Colombo differences expression gene to colour leading potentially both documented, been have regions mRNA untranslated in diversity a high and mutations trans-regulatory and these, cis- Of 2013). Sefc (Maan & factors regulatory ingene rather to changes but sequences, coding protein in genetic variation little related to comparatively is diversity colour that suggests colouration cichlid in literature rich comparatively The factors. or transcription genes the same in place have taken mutations independent if also and pathways, molecular parallel through occurred has evolution if pinpoint to possible is it species related within closely evolution colour parallel into looking By mutations. coding toprotein relation are in changes regulatory such how frequent it is yet unknown but changes, phenotypic coordinated produce ways to simple relatively provide mechanisms trans-regulatory and cis- in Mutations excluded. cannot be polymorphism ancestral an of sorting although events, hybridization multiple through occurred probably Lake Like Malawi. inhabitingin the genera four multiple speciesacross into incorporated was then subsequently once originated as acolouration allele to novel up-regulate backgrounds. Robertsgenomic role ingenerating adaptive colour diversity bytransferring colour genes into new a crucial have can introgression that view the supports also cichlids in polymorphism into the independent origin of the blotch phenotypes the in lakes origin two of the phenotypes blotch independent (Roberts an andsuggests mechanisms different by are caused lakes two in the that blotches indicating haplotype, female brown-barred ancestral to the was identical haplotype wasindividual in examined for mutations the Lake Victoria anorange-blotch blotch morph, Victoria Lake alsothe causes (Roberts morphs blotched female of thepattern mimics and exactly melanophores larger and tofewer leads upregulation and leads to precursors crest neural from melanocytes of the development coordinates that factor al. ski1 the QTL near asingle with isassociated polymorphism orange-blotch/plain Malawi 2009; Streelman 2009; gene, and is caused by a cis-regulatory mutation of the of mutation andis acis-regulatory by gene, caused . The location is found 70 kb downstream of the red colour the colour of red kbdownstream isfound 70 location . The Molecular geneticsand developmental basis of colour morphs H. cydno butterflies provide evidence for a direct role of introgression in fuelling the the fuelling in introgression of role a direct for evidence provide butterflies pax7 et al. et upregulation. Studies on zebrafish zebrafish on Studies upregulation. et al. et species clade. Another study on the orange-blotch/plain orange-blotch/plain the on study Another clade. species Regulatory vs protein coding evolution coding evolution vs protein Regulatory 2013; Santos & Salzburger 2012). For example, the Lake Lake the example, For 2012). Salzburger & Santos 2013; 2003). This cis-regulatory mutation affects a transcription a transcription affects mutation cis-regulatory This 2003). et al . (2012) found a location with an almost perfect perfect withanalmost alocation found . (2012) et al etal. H. melpomene Heliconius . (2009) showed that the orange-blotch orange-blotch the that showed (2009) . 2009). To investigate if the same mutation thesame mutation if To investigate 2009). pax7 pax7 example, this spread has most

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Accepted Article associated with mutations in the coding sequence the of sequence inthe coding withassociated mutations often are which 2010), Schöneberg & Hofreiter 2006; (Hoekstra vertebrates tetrapod guppy in(Tezuka the polymorphism colour the melanic is noand there dominant, gold being with locusmodel, two-allele single byaMendelian determined is polymorphism gold The uniformly. progress not does change thiscolour and often visible, become to xanthophores underlying allowing thereby degrade dark juveniles of melanophores when the ismarked change colour ontogenetic of onset The 2012). years(Mattersdorfer several of age at an start can it inothers, but old, months theyare a few when golden colour the displaying with individuals some exists, colouremergence golden of timing in the variation inter-individual Large morphs. gold of consisting population the of <10% with rare, very and linked sex not are above, polymorphism Unlike blotch/plain the differences. colour underlying mechanism a regulatory of example another provide the in cichlids Midas of polymorphisms barred/gold The This article This protectedis by Allcopyright. rights reserved. inducing spatial changes in cell-signalling gradients across the wing (Martin wing the across gradients in cell-signalling spatialinducing changes in divergence pattern black Likewise, variants. cis-regulatory multiple, linked, of tightly the implicating involvement 1989), (Mallet observed been have sometimes elements of expression spatial in the differences generate that variation cis-regulatory by driven are patterns In colour variants. and sympatric geographic In that found was synthesis, it function with melanin in contradictoryits and yet, other teleosts, between synteny coding high revealed analyses conserved amino acid sequence variation in variation sequence acid amino conserved (Reed causal factor et al. (Nadeau region down an to 150 kb narrowed been have differences colour red race Yet another example is the phylogenetically widespread sex-limited the in mimicry sex-limited widespread thephylogenetically is example another Yet (Fan pattern colour in differences to been related yet not have differences but detected, been splicing havesplicing patterns species-specific tissues.In cichlids, in andtarget species the mRNA target of analyses RNA-seq through differences expression study to species polymorphic in colour importance the highlights This will go undetected. variants spliced differently techniques, but with polymorphisms, colour the most usedcommonly DNA-sequencing in the contextof potential hasgreat splicing alternative reasons, For these diversity. overall phenotypic the enhances of genome and capacity totalcoding increases the this, e.g.alternative splicing same retention. gene, or exon by skipping intron With the mRNAs worksfrom different diversity, and by of proteomic producing generation the and bothgene regulation for mechanism isa splicing fundamental Alternative 2012). Heliconius Heliconius 2012) and analyses indicate that the homeobox transcription factor factor transcription homeobox the that indicate analyses and 2012) mc1r butterflies, regulatory changes are causative of colour patterns in some patterns insome colour of causative are changes regulatory butterflies, evolves through cis-regulatory variation of the morphogen themorphogen of variation through cis-regulatory evolves optix was upregulated wasinmorph (Henning the gold upregulated mc1r (Reed sequence polymorphism (Henning et al. et etal. 2011). Gene expression analyses and the highly expression analyses 2011). Gene 2011). Phenotypic recombinants red between pattern recombinants 2011). Phenotypic Alternative splicing splicing Alternative Amphilophus H. melpomene, optix Amphilophus

both suggest that variable red red that variable suggest both Amphilophus Amphilophus et al. et et al. et et al. et morphs colour dark/gold mc1r et al. for example, for 2010). 2010). Thisunlike is 2012; Kocher 2004). 2004). 2012; Kocher when compared to to when compared gene. Comparative gene. Comparative 2011) and many and many 2011) 2010). 2010). species group group species optix

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Accepted Article (Svensson damselflies 1996), Lively & (Sinervo lizard side-blotched of morphs on colour studies are field exceptions Notable goal. and difficult this challenging achieved studies have empirical few To date, orboth. temporally either spatially, change, frequencies as predictably morph colour of varies morphs ordering rank and fitnesses the thattherelative in frequencies) differ morph local that demes and/or subpopulations multiple from data fitness (using demonstrated be itneeds to NFDS, of the case In 1953). (Levene polymorphisms genetic of the maintenance for prerequisite genetic a population is which conditions, environmental changing to response varies in fitness specific morph of ordering rank the that show to needs one Rather, existence. itsof is proof this pattern that argue to erroneous be would it selection, balancing with isconsistent within of multiple populations local morphs presence the Although outcome. default is the monomorphism hence and selection and/or local drift genetic by time over morphs several or one will lose populations locally, operates (Svensson or NFDS advantage) (heterozygote of overdominance form inthe of balancing either selection, form some to require thought is usually within populations colour polymorphisms Maintaining genus This article This protectedis by Allcopyright. rights reserved. be more might morphs male colour some is variable, environment the lightning Forinstance, if or such environments. visual as temperature factors, environmental with abiotic interact can interactions and mating systems by causedmating factors intrinsic even that likely, and possible,is it However, damselflies). (e.g. conflict side-blotched lizards) or frequency-dependent male matingharassment and sexual (e.g. competition male-male and selection intrasexual toeither due social reasons, and intrinsic purely arise might for NFDS how exemplify above thestudies of Some NFDS. about inference astrong make wants to one if to frequency in relation changes morphs fitness how show to explicitly needs One loads orbehaviours. parasite such as fecundity, components, or fitness phenotypic inor traits oneseveral morphs colour between differences demonstrate to notenough is it NFDS, case of the that in taxa.Note of range awider of will question that studies open require is an traits and other in colour polymorphisms important than overdominant selection in maintaining sexually selected sexually (Johnston selected character) (Gratten character) selected (anon-sexually polymorphism coatcolour both on overdominance through selection islandSoay of population sheep an on study recent a NFDS, through selection balancing demonstrated which studies guppy(Hughes the in advantages mating male supergene mimicry in in mimicry supergene polymorphisms. geneticcolour of evolution inthe splicing alternative of role the understand to needed are More studies role. a have also between differences functional the to contributed iso-forms) spliced (specific differences expression that isoform DNA controls when where and Papilio et al. et described above (Kunte described 2005; Takahashi & Watanabe 2010) and a recent study on rare- on study a recent and 2010) Watanabe & Takahashi 2005; P. polytesP. Box 2: Polymorphism maintenance et al. et dsx dsx et al. Ovis aries and there is evidence that noncoding, regulatory regulatory noncoding, that is and there evidence 2008) and horn polymorphism (a non-colour but (anon-colour polymorphism horn and 2008) is expressed. Indeed, Kunte Kunte isIndeed, expressed. alleles, and that protein sequence evolution may evolution sequence protein and that alleles, 2009, Figure 2). If no balancing selection selection nobalancing 2). If Figure 2009, et al. et et al. et instead provided evidence of balancing balancing of evidence provided instead 2014). 2014). gene The 2013). Whether isNFDS 2013).more Whether etal.

2013). In contrast to these tothese Incontrast 2013). et al dsx . (2014) showed showed . (2014) controls the the controls Accepted Article traits of correlational selection (Roff & Fairbairn 2012). In either scenario and under under and scenario either In 2012). Fairbairn & (Roff selection correlational of traits both impact target which mutations pleiotropic thespread of can selection favour correlational chronic Alternatively, 2002). Svensson & (Sinervo disequilibrium linkage theytraits, evenloci, the sets through governed of if of by formation are separate disparate between genetic buildsup correlations selection that chronic correlational is for this sign. One explanation and of magnitude in terms correlations the genetic with concordant are gradients selection correlational system, same the in estimated are correlations and genetic interactions) fitness pair-wise as estimated usually selection when showed correlational that (2012) Fairbairn & Roff meta-analysis, a Using 2012). Fairbairn & (Roff confirmed was of this hypothesis the generality that was it notuntil recently but fitness, maximum of direction the in surface adaptive the with aligned become to expected be would traits between correlations genetic that suggested (1984) Cheverud adaptation. phenotypic and evolves how it may constrain architecture the genetic how explored date have to few studies Relatively of covariances. sign the traits and between and covariances variances genetic of wellas as the such magnitudes loci, size the of affecting loci traits, effect of the number includes architecture genetic The Linking architecture genetic and selection sexual sexual selection. dependent with frequency negative concert operate in needs to environments the variable but selection, natural frequency-independent by polymorphisms colour maintain unlikely to alone, and itself is,in environment Gray (e.g. successof suchlocally morphs visible inhigher mating resulting others, visible than This article This protectedis by Allcopyright. rights reserved. 2002; Svensson Svensson & (Sinervo lizards and side-blotched 1992) III Brodie 1989; III (Brodie snakes garter such as reptiles, of studies field mainly from come this supporting examples Empirical (1996). and Altenberg by Wagner theoretically suggested been as has by selection, beshaped can architecture genetic that the suggesting correlations, adaptiveof genetic the formation is result the mechanisms, both polymorphisms. More specifically, researchers could reconstruct the evolutionary specifically, could reconstruct More researchers polymorphisms. these of history evolutionary on the studies genomic future in research of wethenwould have avenue anew toNFDS, subjected systems polymorphic colour is to it applicable if and general is thisscenario If time. QTLover effect large single, when asymmetric the trait wasby targeted NFDS and that trait evolvedthe into a more become can architecture genetic the that demonstrated (2006) Hermisson Kopp and small effect, of each one multiple loci, of architecture apolygenic from Starting 2006). Hermisson & (Kopp NFDS chronic under evolve can supergenes) loci effect QTLs or that major (i.e. suggested architecture onselection genetic frequency-dependent of effects on the model genetic population A architecture. sizesan initially haveeffect evolved from polygenic polymorphic systems colour in and of their loci the number if is question unexplored and empirically interesting An et al. 2003). 2003). et al. et etal. 2008). However, theory suggests that such a varying abiotic abiotic avarying that such suggests theory However, 2008). 2009), and a few laboratory studies, such as guppies guppies (Blows as such studies, laboratory anda 2009), few (selection for combinations of characters, of characters, (selection for combinations

Accepted Article polymorphism may emerge (Rueffler emerge may polymorphism a and stable disadvantage heterozygote ameliorate would alleles recessive of This masking homozygotes. to similar more phenotypically heterozygotes by making of allelic evolution dominance the promote also mayselection ora QTLs.Sexual one few by are governed the morphs of that architectures genetic oligogenic with up ending and traits polygenic of form the in states character with ancestral starting polymorphisms, colour of architecture of the genetic history This article This protectedis by Allcopyright. rights reserved. fish (Table 1), such as in the polymorphism of the damselfly of the damselfly inthe polymorphism as 1), such (Table fish expression, which is in gene the evolution common colour of and sex-limited insects such as behaviours, physiology and developmental rates as correlated responses. as responses. rates correlated and developmental suchas physiology behaviours, traits, phenotypic other change also could but population, local the in frequencies and on one only would advantage selection consistent morph alter not morph fitness a Hence, 2010). Pierotti McKinnon & in (reviewed cases in several demonstrated has been which with colour, are correlated traits fitness-related multipleother if particularly polymorphisms, including colour traits, selected sexually to beextended can models These and response by-product. asa correlated isolation reproductive traitresults in ecological on the selection sothat isolation, and reproductive models postulate a pleiotropic link an between ecological trait conferring adaptation (Gavrilets 2004; Magalhaes traits 'magic' termed been have traits these and pleiotropy, synergistic through isolation inreproductive traits involved between recombination reduce or eliminate that either byarchitectures genomic is favoured speciation is that accumulating Indeed, evidence natural (e.g. in guppies). of effects selection and sexual synergistic by the governed evolution is show that systems polymorphic many colour on Studies hierarchy (Sánchez-Guillén morphs colour andanallelic by both females-limited characterized dominance and an ecologically important (Summers colour trait important and anecologically mating non-random association between an demonstrating morph, torespect colour with inat assortative is species, mating least some Interestingly, Cummings 2012). warning of toxicity(Joron signal orunpalatability aposematic dart are which brightly frogs, warning is and colouration to coloured, bethought an (Rosenthal functions physiological with other or antioxidants and immuno-stimulants as with use their trade off may ornamentation in deposition carotenoid since pigments, carotenoid containing those than quality of individual indicators to belesslikely are thought colours plumage melanin-based birds, in example For content. information signal the determining in important be colourmay of origin metabolic The 2004). Roulin (e.g. effort reproductive toprevious load, mutation deleterious immuno-competence, performance, ecological from ranging traits varied indicate may and quality, individual for asignal as performs also taxa,colour of range wide 1). Ina (Table cichlids Midas in morphs barred/gold the goose or snow lesser finches, suchas inGouldian demonstrated, been has mating assortative where polymorphisms are here particular colour interest Of example of this might be provided by beprovided this might of example One selection. sexual and bothnatural by couldbe favoured morphs colour different for instance, colour of polymorphisms, 2011). In the case (Maan & Seehausen et al. (e.g. Gray shown as often been other, has each bein to opposition notalways might selection natural sexualand that awareness is agrowing magic traits of discovery 2008), but could work in the same direction and favour similar trait values values trait similar and favour direction work inthe same but could 2008), etal. et al. et 2005). 2005). 2010; Servedio 2010; etal. Heliconius 2006). Similar arguments could apply apply couldto Similar arguments 2006). etal. butterflies and and butterflies et al. et 2012). Closely connected tothe connected Closely 2012).

etal. 2011). In short, magic trait- magic short, In 2011). 1999). Another example is is example Another 1999). et al. et Dendrobates Dendrobates I. elegans, elegans, I. 2011; Maan 2011; & which is is which poison poison

Accepted Article reported between several colour polymorphic polymorphic colour several between reported been has hybridisation ongoing and intense Interestingly, 2005). Svensson & (Abbott fecundity) and time development (e.g. traits related fitness manyother affects (Sánchez-Guillén fashion Mendelian a simple in segregate found to the be for example, could, systems these of One locus. aMendelian to similar afashion in segregate but that 2010), Pierotti (McKinnon & traits and fitness-related phenotypic with other correlated genetically are that phenotypes colour multivariate will be relationships these to study candidates system study Good rise. to likely are genes colour of bearers be to found are and inversions QTLs large caseswhere supergenes, of thenumbers techniques, genomic of development the continuing 1). With (Table phenotypes colour adaptive control several to been shown have that structures supergene and inversions of case in as the such traits, other with colourloci of clustering a tight towards point colourgenes of examples prominent selection. Several of targets the molecular with about knowledge polymorphisms on studies colour selection sexual to integrate opportunity the offer These studies polymorphisms. colour genetic of underpinnings genomic the describe been made to has progress Over lastyears, significant the Conclusions andfuture directions (Hughes advantage mating rare-male and through selection sexual through (Olendorf predation less of NFDS in terms by favoured apparently are morphs colour male where rare guppies, by provided This article This protectedis by Allcopyright. rights reserved. Sánchez-Guillén 2013a; of colour genes (Sánchez-Guillén to system adaptive study introgression stages. life reproductive the only not affect and is to be strong likely on architecture expected pressure the genetic evolutionary the workingconcordantly, are selection naturalwere and sexual Incases 2013). supergenes and inversions lead to reduced recombination between colour and other other and colour between recombination reduced to lead inversions and supergenes both orinversions. clusters supergene with of species While colour future fate the concerns attention little received far so has that aspect interesting An selection. and sexual natural to inrelation evolve may phenotypes colour and when how help elucidate can networks) complexity geneexpression of and regulation type of disequilibrium, linkage history, (e.g.mutational factors correlated of and the suite polymorphisms of colour properties genetic functional the Deciphering approaches. comparative phylogenetic using possible is reconstruction historical a where 1), and (Table damselflies cichlids and as butterflies, such loci, colour harbour also that regions ingenomic genes linked tightly carry, likely or carry, that species related closely will be events and traits such explore to groups Suitable events. evolutionary of the sequence clarify further will and supergenes clusters gene within changes of order temporal the about knowledge that we foresee Further, be overcome. can hopefully hurdles these mapping, and technologies sequencing improved With selection them. acting upon of the consequence understanding for be valuable would see 1), dominant, Table found to be are often genes (which including the colour clusters, such genes in of patterns the dominance deciphering Moreover, function. to genes tomap difficult it makes clusters within tightlinkage the since phenotypes, of novelcolour generation the are for clusters causative within these residing thegenes of which be todetermine will genetics developmental in studies future et al. et 2011b; Sánchez-Guillén 2011b; Ischnura Ischnura et al. Ischnura 2006), but also in terms of NFDS NFDS of in terms but also 2006), damselfly system, whereis colour system, damselfly

et al. et species, making this a making this also species, 2012). A challenge for for A challenge 2012). et al. et 2005), but et al. et et al. et

Accepted Article & Cáceres 2013). Lledó (Lucas improved being progress this in presently is although field approaches, withto detect NGS difficult they more are generally approaches, cytogenetic and karyotypic with visualised can be inversions while large Moreover, genome. whileevidence for atrans-regulatory change potentially implicates the entire function, divergent the with gene the close to belocated must change regulatory cis- acausal because is This changes. trans-regulatory than rather regulatory a cis- will bias detecting be positive towards there approaches genomic current (e.g. in sequences protein certain towards findings will bias approaches gene candidate Moreover, areas. in such markers having of likelihood increased to the due areas genomic large detecting towards the findings skew e.g. will approaches (NGS) Sequencing Generation Next applied commonly the with others over genetic mechanisms of types certain detect to potential The bias. a methodological partly is probably clusters gene and/or loci effect large by caused are traits colour many that finding the that though, would liketocaution We dead-ends. evolutionary to lead eventually can this together and affected, area genomic the also increase will but process, only will facilitate this not selected clusters around hitchhiking speciation. Genetic and divergence constrain species evolutionary andfor long may survival term disadvantageous be could linkage tight or pleiotropy traitsthrough of the coupling for sense,selection this isIn minimal. recombination since change evolutionary cause efficiently cannot clusters within these loci only selected on acting selection cluster, actasonetight both and supergenes inversions Because potential. evolutionary restricted to lead can clusters such then change, regimes selection if phenotypes, intermediate preventing by likelyadaptive shortterm are the in and loci, linked This article This protectedis by Allcopyright. rights reserved. (Roberts hybridization and/or polymorphism ancestral an of sorting by either flock, Malawi cichlid the of genera four across species multiple into been incorporated subsequently has and this occurred has loci with sexdetermination theorange-blotch of tight linkage Here, cichlids. incompatibilities are coupled on the Zchromosome in and intrinsic postzygotic preferences mating colour, plumage for the loci Likewise, or sex loci mate between of colour colour preferences and linkage In loci. a linkage show studies is several that for research avenue new interesting Another (Forsman 2013; 2013; Forsman (Forsman species and ultimately, populations morphs, onindividual acting consequences ecological tothe and connected be unravelled can selection of targets the molecular where phase new an exciting studies areentering think We that polymorphism colour of allele orange-blotch in the determination insex involved loci and loci between colour linkage favoured have also to appears selection antagonistic Sexually 2010). (Pryke finches and Gouldian 2008) & Bailey (Qvarnstrom (Kronforst region genomic same the by controlled white is versus yellow for and the preference pattern switch colour yellow/white a pattern,that such colour controlling those with associated genetically are genes preference mate butterflies, et al. et 2008). We predict that this field will flourish over the the over will flourish field this predict that 2008). We et al. 2009) 2009)

mc1r ). withIn addition, most Ficedula Ficedula pax7 etal. in Malawi Malawi in flycatchers Heliconius 2006). 2006).

Accepted Article Research Council, the Crafoord foundation and Carl Tryggers Stiftelse (CTS). (CTS). Stiftelse CarlTryggers and foundation Crafoord Council, the Research the Swedish grants from by were supported Theauthors togenomes’. ecology from polymorphisms: colour heritable of and maintenance evolution ‘The entitled wouldBH likeacknowledge to theXIV ESEB meetinghelp forhost to a symposium and MW thisof manuscript. version anearlier on comments Maan for Martine and Heliconius numata Heliconius of photographs morph colour providing Corlfor and Amon Mathieu Joron Tuttle, Elaina Maan, thankMartine We Acknowledgements heritable colour polymorphisms. on selection sexual of consequences genetic the about be made to inferences will approach unify help and ecological wouldmolecular studies, allowand for research anintegrative Such traits. other and morphs colour on operates selection how of understanding enhanced and traits correlated of decoupling the experiments, whichschemes oreven genetic engineering), in will turn allow for controlled crossing treatments, hormone through (e.g. manipulations phenotype of design the facilitate may then genetics, functional molecular and the about knowledge detailed with addition in studies, Such selection. sexual of the effectiveness on constraints genetic possible and reveal pressures, selection different exposed to whichbe may colour thegenes genes, of insights intheinto vicinity increased provide to aim also studies should Future molecular colour. of underpinnings thewith selection molecular on morphs studies on of causes behavioural and ecological and on fitness the effects colour evaluating studies rigorous integrate ideally should approaches combined Such genetics. with ecology combine explicitly studies that will from only come polymorphisms on colour selection sexual of ourunderstanding progress in that would to emphasize like years, but next This article This protectedis by Allcopyright. rights reserved. and evolution Integration (2005) PC Yelick TD, Kocher JT, RC,Streelman Albertson and inemergence and genetic variation (2005) Phenotypic EI J, Svensson Abbott References Barlow G (1983) The benefits of being gold: behavioral consequences of of consequences behavioral gold: being of benefits The G(1983) Barlow America of of of States ofthe United National Sciences Academy the Proceedings strategies. alternate feeding of basis The molecular cichlid the mandible: of 18 damselfly. a of trimorphic time development Biology of Fishes of Biology cichlid, midas the in polychromatism , 1464-1470. 1464-1470. ,

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Accepted Article Tuttle EM (2003) Alternative reproductive strategies in the white-throated sparrow: sparrow: white-throated the in strategies reproductive Alternative (2003) EM Tuttle Sánchez-Guillén RA, Wellenreuther M, Cordero-Rivera A, Hansson B (2011b) (2011b) Hansson B A, M,Cordero-Rivera RA, Wellenreuther Sánchez-Guillén This article This protectedis by Allcopyright. rights reserved. Wagner GP, Altenberg L (1996) Perspective: Complex adaptations and the evolution the evolution and adaptations Complex L(1996) Perspective: Altenberg GP, Wagner The A (2008) C¢rdoba-Aguilar A, Cordero-Rivera TN, H, Sherratt Van Gossum Sánchez-Guillén RA, Wellenreuther M, Cordero-Rivera AS (2012) Strong asymmetry asymmetry Strong (2012) AS M, Cordero-Rivera Wellenreuther RA, Sánchez-Guillén Seehausen, Mayhew, Alphen JJMV (1999a) Evolution of colour patterns in East East in patterns colour of Evolution (1999a) JJMV Alphen Mayhew, Seehausen, Phenotypes. Complex and Supergenes L (2014) R, Keller T,Libbrecht Schwander Diversify. Cichlids (2012) How W ME, Salzburger Santos Sinervo B, Lively CM (1996) The rock-paper-scissors game and the evolution of theevolution and game rock-paper-scissors The (1996) CM Lively B, Sinervo ratio sex and polymorphism Color R(1999b) Lande JJM, Alphen Van O, Seehausen Servedio MR, Van Doorn GS, Kopp M, Frame AM, Nosil P (2011) Magic traits in traits Magic Nosil (2011) AM, P Kopp M, Frame GS, MR, Doorn Van Servedio Sinervo B, Svensson E (2002) Correlational selection and the evolution of genomic genomic of and the evolution selection (2002) E SvenssonCorrelational B, Sinervo Streelman JT, Albertson RC, Kocher TD (2003) Genome mapping of the orange orange the of mapping Genome (2003) TD RC,Kocher Albertson JT, Streelman spatial nest of effects isolation, the Partitioning DI Bolnick (2012) LK, Snowberg Tezuka A, Yamamoto H, Yokoyama J, van Oosterhout C, Kawata M (2011) The The Kawata M C, (2011) van Oosterhout J, H,Yokoyama Yamamoto A, Tezuka is affected by success Mreproductive Y, Female (2010) Takahashi Watanabe frequency polymorphism, J, Female Hardling R (2005) Abbott Svensson E, SummersK, Symula R, Clough M, CroninT (1999) Visual matechoice in poison Svensson E, Abbott J, Gosden T, Coreau A (2009) Female polymorphisms, sexual sexual polymorphisms, J,GosdenT,Coreau (2009) Female A Abbott Svensson E, behavioral and genetic and behavioral genetic evidence. Evolutionary Biology Evolutionary damselflies. insympatric turnover species rapid and Introgression of evolvability. evolvability. of University Oxford, Press. ecologicalModel and organisms research evolutionary for In: sex-limited polymorphism. of evolution colour damselfly sister species. species. sister damselfly two between postzygotic barriers and in of prezygotic strengths the relative African cichlid fish. Biology Current alternative male strategies. strategies. male alternative sexual selection. by speciation sympatric in stage as anincipient fish a cichlid in distortion speciation: 'magic' butnot 'magic' speciation: rare? architecture. architecture. blotch colour pattern in cichlid fishes. cichlid fishes. in pattern colour blotch stickleback. threespine diethabitat, and in individual causing assortative mating within a of population polymorphisms. polymorphisms. MC1R gene in the guppy ( guppy the in gene MC1R Behavior in harassment selective damselfly male the Naturalist American indynamics natural populations. evolutionary andrapid dependence, 23 Sciences frogs. conflict and limits to speciation processes in animals. in processes to speciation limits and conflict , 93-108. Proceedings of the Royal Society of London. Series B: Biological Biological B: Series London. of the Royal Society of Proceedings

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Accepted Article cydno alithea, Heliconius longwing Numata numata, Heliconius underlying geneticsofcolour in thissystem. inthiscolour species knowledge geneticsabout listthe while the selectionSexual summarises the evi variation,described thecolour (F=female and M=male) the column colour polymorphism incommon name, sex denotes the polymorphic sex thatspecies seem traceable. theand column scientific The species shows systems the where molecular targ list ofpolymorphicn is species genetic basisof colour has been sexual both polymorphism where of Representative examples Table 1: This article This protectedis by Allcopyright. rights reserved. Great mormon memnon, Papilio damselfly tailed elegans, Blue- Ischnura Longwing Cydno Species Sex Colour Colour Sex Species F Large Large F diversity Green, blue and F F M F, morphs (2). yellow wing and White morphs (10). wing black and brown/orange, Yellow, forewing forewing basal the of colour and pattern in wing (3). patterning colour and body pink polymorphism Arthropod Unknown Unknown preference. no show males white females, but yellow prefer males Yellow Unknown Unknown spatially. temporally and that vary fitness costs and rates morph mating dependent frequency- Negative selection on Sexual Sexual colour and number of morphs in brackets. in brackets. morphs of and number on exhaustivehighlightssome but investigatedextent.This tosome ets ofsexualselection oncolour selection on colour andtheselection oncolour dence forsexual selection on speciesgenetic colourwith Single supergene colour/preference/wg. colour/preference/wg. including (5.5-cM) caused by an inversion likely Linkage wg. gene developmental the at same the location of preference colour male wing colour linked to Autosomal supergene specific wing pattern. a to corresponding each one supergene locus P, the for rearrangements possible three create that inversions nested two of consisting locus switch W, F, E, and B. B. E, F, and W, T, supergene: mimicry At least five lociin the species. related in exist patterns inheritance morph fecundity. Similar and time development with Linked hierarchy. dominance in a alleleslocusthree with Mendelian Autosomal

eeiso oor References Genetics ofcolour 2011) 2011) (Jones 2005) Guillén Sánchez- 2011a; Guillén Sánchez- 2008; & Svensson Gosden 2009; & Svensson Gosden 2005; Svensson (Abbott & (Joron 2001) 2001) (Naisbit al. et Joron 2011; 2006) et et al. et et al. et al. et al. et

et al. et

Accepted Article stansburiana, stansburiana, Uta frog poison Strawberry pumilio, Dendrobates mormon Common polytes, Papilio This article This protectedis by Allcopyright. rights reserved. cichlids Midas citrinellus Amphilophus lizards blotched side- Common ,

F M, F M, F M, One F male abdomen (>20). and triangle sexes (2). (2). sexes both in morph gold arare and (~90%) morph dark Barred (3). males) mainly in (blue colours throat blue and yellow Orange, spots (>15). with melanised some patterns, colour and Many body (4). swallowtails Pachliopta patterns of toxic and colours that mimic three morphs mimic, and

Amphibians Reptiles Fish ones, and on foreign over colours male native prefer females level, population inter- colour.an On their own of males prefer generally Females Unknown markers markers neutral divergence of genetic and assortatively mate normal fish and Gold males. same coloured preferences for female that overrides competition male male- Strong males. bright for selection sexual directional level, exhibit population an intra-

yellow. yellow. dominancered of over complete with locus, is controlled by a single patterning dorsal Dark mimicry. controls supergene gene The dominant. being gold with model, locus single two-allele a by determined pattern inheritance Mendelian throats. allele developyellow o an lacking those while orange-throated, are the dominant o allele bb. In females, all with blue-throated males: yy yb, and males: or yellow-throated oy, or ob, oo, males: throated Orange- y allele. the to is recessive allele b the dominant allele,while is the allele o the males, In alleles. three with factor Mendelian a like segregates and heritable is colour Throat between between functional differences contribute to the differences expression alleles.

Isoform Isoform dsx doublesex mimicry mimicry

2009) 2009) Cummings & (Maan et al. et Mattersdorfer 2010; Henning 1973; (Barlow 1996) Lively & Sinervo Sinervo 2007; (Bleay & 2014) 2014) (Kunte 2012) et al. et

et al. et

Accepted Article Lesser snow snow Lesser caerulescens, c. Anser guppy Millionfish reticulata, Poecilia cichlid Victoria Lake omnicaeruleus, Neochromis This article This protectedis by Allcopyright. rights reserved. Gouldian finch gouldiae, Erythrura Buzzard Common Buteo buteo, goose F M, F M, F M, M Males display a F M, females (3). (3). females in malesand colour patterns head black and yellow Red, white (3) Pale,and dark more) or (3 blue/grey intermediate, White, (>10). green and orange, yellow red- white, including black, colours, ofvarious spots of diversity (3). rare Intermediates morphs. white blotched or as orange or plain occur Females are Birds two morphs. the between occurs by rare-male NFDS caused many pairs. in matching phenotype prevents likely nature in morphs blotched Scarcity of experiments. mate choice laboratory and wild the frequencies in morph from mating assortative colour Evidence for intermorph- fitness of low causing genes the and expression colour preferences, mating for genes harbours likely chromosome Z morph. own mates of their strongly prefer morphs red and black Both advantage. heterozygote morph to due maladaptive possibly mating, Assortative colour. parental on imprinting mating, Assortative female choice. for basis a is also spots orange male Extent of advantage. mating QTL analyses showed showed analyses QTL and mapping Linkage genes. opsin cone three of array tandem a and shape tooth for quantitative trait locus a to proximity close in gene. Thesegenes lie pax7 of the mutation cis-regulatory a and c-ski1 proto-oncogene tightly associatedski to is and of cM, 30 group linkage a to mapped Blotch phenotype indistinguishable. phenotypically homozygous redmales heterozygous and ZRZr (red),with orheterozygous (red), ZRZR (black), ZrZr can behomozygous Males red). ZR black, matches genotype (Zr phenotype birds, in sex heterogametic allele. In females, the (Zr) black recessive dominant red(ZR) and a with locus Z-linked comm.) pers. Kruger, (O. substitutions of mc1r acid Amino gene. in mc1r variation with Melanism associated autosomes. including geneson genes, multiple by controlled are traits colour male most that

2013; Tezuka 2013; (Hughes al. Seehausen al. et Pierotti 2013; & Sefc (Maan Griffith 2006) 2006) Griffith & Pryke 2010; (Pryke al. et Mundy 2001; (Krüger Ducrest 2013) & (Roulin al. et 1999a) 1999a) 2009; 2004) 2011)

et al. et et et al. et et

Accepted Article population of (middle) and yellow (right) homozy polymorphic (A) species. Throat colo 1:Colour Figure plate of some sparrow throated albicollis, White Zonotrichia skua Arctic parasiticus, Stercorarius Ruff pugnax, Philomachus This article This protectedis by Allcopyright. rights reserved. of Neochromis omnicaeruleus Neochromis morph of its juvenile phase (rufescens). (C) Whit androchrome (top right) and infuscan tarapotensis (bottom left) an thebicoloratus(middl topright, numata (bottomright female and plain (top left), white-blotched (WB) (bottom left), plain male (top right) Ischnura elegans the with numata arcuella morph on the top left, onaurora Zonotrichia albicollis F M, F M, Black, M brown, Uta stansburiana. females (2). (2). females in malesand morphs striped white and Tan (3) dark intermediate, Pale, (3) white morphs : infuscans(top left), . Female d timaeus (bottom right). hybrids. morphs. morphs. opposite comprise pairs of allbreeding >96% which in pattern mating disassortative Strong mating. assortative and/or dark males preference for Female strategies. mating assortative Morph (B) The three female colour morphs morphs colour female (B) The three . (D) Blotched and plain morphs of. (D)Blotched andplain ). (E) Colour morphs of representative examplesofcolour e left),silvana (middle right), gous males from a trimorphic froma gous males

orange-blotched s-obsoleta morph (bottom) in e e (left) andtan(right) striped urs of orange (left), blue blue (left), orange of urs mating preferences. preferences. mating and behaviour Affects two. chromosome of 90% almost span that ZAL2m) inversions (ZAL2and paracentric two Supergene regulatedby gene. in mc1r variation with Melanism associated alleles. two one-locus, Autosomal,

male-mimicking

(OB) morph Heliconius 1995) 1995) 2003) 2003) Tuttle 2011, (Huynh 2004) (Mundy (Lank etal. et al. et et al. et

Accepted Article This article This protectedis by Allcopyright. rights reserved.

Accepted Article phenotypic and genotypic evolution ofcolour polymorphisms. Figure 2: Schematicsummary This article This protectedis by Allcopyright. rights reserved. of affectingmain processes