Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures

Abstract

Explaining the maintenance of adaptive diversity within populations is a long-standing goal in evolutionary biology, with important implications for conservation, medicine, and agriculture. Adaptation often leads to the fixation of beneficial alleles, and therefore it erodes local diversity so that understanding the coexistence of multiple adaptive phenotypes requires deciphering the ecological mechanisms that determine their respective benefits. Here, we show how antagonistic frequency-dependent selection (FDS), generated by natural and sexual selection acting on the same trait, maintains mimicry polymorphism in the toxic butterfly Heliconius numata. Positive FDS imposed by predators on mimetic signals favors the fixation of the most abundant and best-protected wing-pattern morph, thereby limiting polymorphism. However, by using mate-choice experiments, we reveal disassortative mate preferences of the different wing-pattern morphs. The resulting negative FDS on wing-pattern alleles is consistent with the excess of heterozygote genotypes at the supergene locus controlling wing-pattern variation in natural populations of H. numata. The combined effect of positive and negative FDS on visual signals is sufficient to maintain a diversity of morphs displaying accurate mimicry with other local prey, although some of the forms only provide moderate protection against predators. Our findings help understand how alternative adaptive phenotypes can be maintained within populations and emphasize the need to investigate interactions between selective pressures in other cases of puzzling adaptive polymorphism.disassortative mating | selection conflicts | Müllerian mimicry | aposematism | warning signals

Female mate choice is a reproductive isolating barrier in Heliconius butterflies

“…In intraspecific trials, "close wings" behaviour was positively correlated with the outcome of the experiment, suggesting that wing closing indicates female acceptance of a courting male (coefficient = 14.3, SE of coefficient = 5.1, p = 0.0088). The other three behaviours were not significantly correlated with outcome, though all had negative coefficients and are considered rejection behaviours by other authors (Figure 2; Table 3; Chouteau et al, 2017;Jiggins, 2016…”

“…Unlike in many taxa, male choice has been much more commonly studied than female choice in Heliconius, because male choice is easier to test with model females as stimuli and because male choice is the first step in mating interactions. Female choice studies have almost exclusively documented mate preference for variation (natural or experimentally induced) in conspecific males (Chouteau, Llaurens, Piron-Prunier, & Joron, 2017;Darragh et al, 2017;Finkbeiner, Fishman, Osorio, & Briscoe, 2017). However, males still regularly court heterospecific females when they have the opportunity (Merrill, Gompert, et al, 2011) and researchers have generally found stronger assortative mating between species when there is the potential for female choice in the experimental design (Mérot, Salazar, Merrill, Jiggins, & Joron, 2017).…”

Diversity in warning coloration: selective paradox or the norm?

“…For example, multiple morphs of the same species are frequently found existing in the same locality (e.g. Brown & Benson, ; Borer et al, ), often at low densities and/or low frequencies within a population (Chouteau et al, ). Furthermore, the idea that such polymorphisms are likely to be transient and unstable has also been empirically challenged; for example, polymorphism in the poison frog Oophaga pumilio has been persistent on Bastimentos Island in Panama (Richards‐Zawacki, Yeager & Bart, ) and relaxed selection resulting from a decrease in predators produces a vastly reduced predation rate even on novel or intermediate forms (Chouteau & Angers, ).…”

Supergene evolution triggered by the introgression of a chromosomal inversion

“…Balancing selection, mediated by negative assortative mating among inversion genotypes, prevents the fixation of the inversion, as reflected by a deficit of homozygotes for the introgressed haplotype in the wild 31 . Supergene evolution is therefore consistent with the introgressed inversion having a strong advantage under mimicry selection but being maintained in a polymorphism with ancestral haplotypes by negative frequency-dependence.…”