Linkage of butterfly mate preference and wing color preference cue at the genomic location ofwingless

Abstract

Sexual isolation is a critical form of reproductive isolation in the early stages of animal speciation, yet little is known about the genetic basis of divergent mate preferences and preference cues in young species. Heliconius butterflies, well known for their diversity of wing color patterns, mate assortatively as a result of divergence in male preference for wing patterns. Here we show that the specific cue used by Heliconius cydno and Heliconius pachinus males to recognize conspecific females is the color of patches on the wings. In addition, male mate preference segregates with forewing color in hybrids, indicating a genetic association between the loci responsible for preference and preference cue. Quantitative trait locus mapping places a preference locus coincident with the locus that determines forewing color, which itself is perfectly linked to the wing patterning candidate gene, wingless. Furthermore, yellow-colored males of the polymorphic race H. cydno alithea prefer to court yellow females, indicating that wing color and color preference are controlled by loci that are located in an inversion or are pleiotropic effects of a single locus. Tight genetic associations between preference and preference cue, although rare, make divergence and speciation particularly likely because the effects of natural and sexual selection on one trait are transferred to the other, leading to the coordinated evolution of mate recognition. This effect of linkage on divergence is especially important in Heliconius because differentiation of wing color patterns in the genus has been driven and maintained by natural selection for Mü llerian mimicry.Heliconius ͉ Lepidoptera ͉ sexual isolation ͉ speciation

Development and evolution of insect pigmentation: Genetic mechanisms and the potential consequences of pleiotropy

“…These expression differences could be caused by cis-regulatory changes in the genes examined or by changes in their transcriptional activators. Although specific genetic changes have not yet been identified, studies mapping the genetic basis of variable wing pigmentation are consistent with changes at pleiotropic regulatory genes: Distal-less is associated with quantitative variation in eyespot size in Bicyclus anynana [31], wingless is associated with wing color in hybrids of Heliconius species [32], and engrailed/invected is associated with wing pattern polymorphism in Papilio dardanus [33]. Increased mapping resolution and/or functional analyses are ultimately needed to separate the effects of these candidate genes from linked loci.…”

“…An association with pigmentation has been described for diverse behaviors, including swarming [48], feeding [49], social dominance [50], mate preference [32], and courtship display [51]. The molecular basis for these associations, as well as the data supporting them, are also varied.…”

Quantified reproductive isolation inHeliconiusbutterflies: Implications for introgression and hybrid speciation

“…That is, geographical races of H. melpomene behave as a single biological species, as do geographical races of H. cydno and H. timareta , respectively. Heliconius pachinus appears to be intrinsically isolated from H. cydno, as implied previously (Kronforst, Young, & Gilbert, 2007; Kronforst et al., 2006). In contrast, H. heurippa is only isolated from H. cydno by allopatry, suggesting that these two forms are parts of a single biological species (Brower, 2011).…”

“…Heliconius butterflies have likewise become a model system for studying patterns of speciation in the putative presence of ongoing gene flow (Dasmahapatra et al., 2012; Kronforst et al., 2006, 2013; Nadeau et al., 2013). Most Heliconius species are Müllerian mimics of one another, as well as other unpalatable taxa, displaying shared, aposematic wing patterns that are maintained by positive numerically dependent selection.…”

Relationships among pest flour beetles of the genus Tribolium (Tenebrionidae) inferred from multiple molecular markers

“…Such comparative studies have revealed the evolutionary flexibility of developmental mechanisms at the species level (e.g. Raff et al, 1999;Kopp et al, 2000;Gompel and Carroll, 2003;Hoekstra and Nachman, 2003;Voss and Smith, 2005;Kronforst et al, 2006;Protas et al, 2006), allowing insights into the evolution of novel phenotypes (e.g. Wittkopp et al, 2002) as well as the conservation of ontogenetic functions (e.g.…”