The diversification of<i>Heliconius</i>butterflies: what have we learned in 150 years?

Merrill, Richard M.; Dasmahapatra, Kanchon K.; Davey, John W.; Dell’Aglio, Denise Dalbosco; Hanly, Joseph J.; Huber, Bárbara; Jiggins, Chris D.; Joron, Mathieu; Kozak, Krzysztof M.; Llaurens, Violaine; Martin, Simon H.; Montgomery, Stephen H.; Morris, Jeffrey J.; Nadeau, Nicola J.; Pinharanda, Ana; Rosser, Neil; Thompson, Mark; Vanjari, Sohini; Wallbank, Richard W. R.; Yu, Qiuhan

doi:10.1111/jeb.12672

Cited by 158 publications

(185 citation statements)

References 236 publications

(351 reference statements)

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“…In the mimicry radiation of Heliconius, preference for a similar mate (positive assortative mating) may evolve in response to the poor mimicry of heterozygous genotypes at mimicry loci (42), and it operates as a key driver of speciation along the entire continuum of differentiation, from the early stages of ecological divergence (10) to the maintenance and strengthening of species differences (42). Our results contrast with this general trend and may drive drastically different adaptive dynamics in H. numata.…”

Section: Resultscontrasting

confidence: 56%

“…In several adaptive radiations, selection on differentiated color phenotypes is thought to precipitate speciation through its roles in mate choice and premating reproductive isolation (23,41,42). In the mimicry radiation of Heliconius, preference for a similar mate (positive assortative mating) may evolve in response to the poor mimicry of heterozygous genotypes at mimicry loci (42), and it operates as a key driver of speciation along the entire continuum of differentiation, from the early stages of ecological divergence (10) to the maintenance and strengthening of species differences (42).…”

Section: Resultsmentioning

confidence: 99%

“…All behavioral experiments were conducted with unrelated sexually mature virgin males (10-18 d old) and receptive females (3-5 d old) in outdoor insectaries in Tarapoto (42). To control for relatedness and to maximize the genetic diversity of the butterflies tested, each sex was drawn from the captive raised progeny of two distinct H. numata colonies.…”

Section: Methodsmentioning

confidence: 99%

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

Chouteau

Llaurens

Piron‐Prunier

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

105

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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

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Section: Resultscontrasting

confidence: 56%

Section: Resultsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

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

Chouteau

Llaurens

Piron‐Prunier

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

105

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“…2015; Merrill et al. 2015). Chromosomal inversions are known to play an important role in the maintenance of a complex color pattern polymorphism in Heliconius numata (Joron et al.…”

Section: Introductionmentioning

confidence: 99%

No evidence for maintenance of a sympatricHeliconiusspecies barrier by chromosomal inversions

et al. 2017

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Mechanisms that suppress recombination are known to help maintain species barriers by preventing the breakup of coadapted gene combinations. The sympatric butterfly species Heliconius melpomene and Heliconius cydno are separated by many strong barriers, but the species still hybridize infrequently in the wild, and around 40% of the genome is influenced by introgression. We tested the hypothesis that genetic barriers between the species are maintained by inversions or other mechanisms that reduce between‐species recombination rate. We constructed fine‐scale recombination maps for Panamanian populations of both species and their hybrids to directly measure recombination rate within and between species, and generated long sequence reads to detect inversions. We find no evidence for a systematic reduction in recombination rates in F1 hybrids, and also no evidence for inversions longer than 50 kb that might be involved in generating or maintaining species barriers. This suggests that mechanisms leading to global or local reduction in recombination do not play a significant role in the maintenance of species barriers between H. melpomene and H. cydno.

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“…This largely involves evolutionary diversification in gene regulation, providing a promising system for dissecting the process of cis-regulatory evolution [11,12]. The patterns have arisen recently enough that it is feasible to identify the exact DNA changes that produce different patterns.…”

Section: Introductionmentioning

confidence: 99%

Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

Jiggins¹,

Wallbank²,

Hanly³

2017

Phil. Trans. R. Soc. B

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One contribution of 17 to a theme issue 'Evo-devo in the genomics era, and the origins of morphological diversity'. A major challenge is to understand how conserved gene regulatory networks control the wonderful diversity of form that we see among animals and plants. Butterfly wing patterns are an excellent example of this diversity. Butterfly wings form as imaginal discs in the caterpillar and are constructed by a gene regulatory network, much of which is conserved across the holometabolous insects. Recent work in Heliconius butterflies takes advantage of genomic approaches and offers insights into how the diversification of wing patterns is overlaid onto this conserved network. WntA is a patterning morphogen that alters spatial information in the wing. Optix is a transcription factor that acts later in development to paint specific wing regions red. Both of these loci fit the paradigm of conserved protein-coding loci with diverse regulatory elements and developmental roles that have taken on novel derived functions in patterning wings. These discoveries offer insights into the 'Nymphalid Ground Plan', which offers a unifying hypothesis for pattern formation across nymphalid butterflies. These loci also represent 'hotspots' for morphological change that have been targeted repeatedly during evolution. Both convergent and divergent evolution of a great diversity of patterns is controlled by complex alleles at just a few genes. We suggest that evolutionary change has become focused on one or a few genetic loci for two reasons. First, pre-existing complex cis-regulatory loci that already interact with potentially relevant transcription factors are more likely to acquire novel functions in wing patterning. Second, the shape of wing regulatory networks may constrain evolutionary change to one or a few loci. Overall, genomic approaches that have identified wing patterning loci in these butterflies offer broad insight into how gene regulatory networks evolve to produce diversity.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

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The diversification ofHeliconiusbutterflies: what have we learned in 150 years?

Cited by 158 publications

References 236 publications

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

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

No evidence for maintenance of a sympatricHeliconiusspecies barrier by chromosomal inversions

Waiting in the wings: what can we learn about gene co-option from the diversification of butterfly wing patterns?

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