title: Conservatism and novelty in the genetic architecture of adaptation in Heliconius butterflies.
abstract: Understanding the genetic architecture of adaptive traits has been at the centre of modern evolutionary biology since Fisher; however, evaluating how the genetic architecture of ecologically important traits influences their diversification has been hampered by the scarcity of empirical data. Now, high-throughput genomics facilitates the detailed exploration of variation in the genome-to-phenotype map among closely related taxa. Here, we investigate the evolution of wing pattern diversity in Heliconius, a clade of neotropical butterflies that have undergone an adaptive radiation for wing-pattern mimicry and are influenced by distinct selection regimes. Using crosses between natural wing-pattern variants, we used genome-wide restriction site-associated DNA (RAD) genotyping, traditional linkage mapping and multivariate image analysis to study the evolution of the architecture of adaptive variation in two closely related species: Heliconius hecale and H. ismenius. We implemented a new morphometric procedure for the analysis of whole-wing pattern variation, which allows visualising spatial heatmaps of genotype-to-phenotype association for each quantitative trait locus separately. We used the H. melpomene reference genome to fine-map variation for each major wing-patterning region uncovered, evaluated the role of candidate genes and compared genetic architectures across the genus. Our results show that, although the loci responding to mimicry selection are highly conserved between species, their effect size and phenotypic action vary throughout the clade. Multilocus architecture is ancestral and maintained across species under directional selection, whereas the single-locus (supergene) inheritance controlling polymorphism in H. numata appears to have evolved only once. Nevertheless, the conservatism in the wing-patterning toolkit found throughout the genus does not appear to constrain phenotypic evolution towards local adaptive optima.
authors: 1] Institut de Systématique, Evolution, et Biodiversité, UMR 7205 CNRS, Muséum National d'Histoire Naturelle, Paris, France [2] Laboratoire Biologie Intégrative des Populations, Ecole Pratique des Hautes Etudes (EPHE), Paris, France [3] The Smithsonian Tropical Research Institute, Balboa, República de Panamá
authors: B
authors: B
authors: Huber
authors: Institut de Systématique, Evolution, et Biodiversité, UMR 7205 CNRS, Muséum National d'Histoire Naturelle, Paris, France.
authors: A
authors: A
authors: Whibley
authors: Institut de Systématique, Evolution, et Biodiversité, UMR 7205 CNRS, Muséum National d'Histoire Naturelle, Paris, France.
authors: Y L
authors: YL
authors: Poul
authors: 1] Laboratoire PALEVO, Ecole Pratique des Hautes Etudes, Dijon, France [2] UMR uB/CNRS 6282-Biogéosciences, Université de Bourgogne, Dijon, France.
authors: N
authors: 0000000156944201
authors: N
authors: Navarro
authors: Department of Molecular and Cell Biology, University of California, Berkeley, CA, USA.
authors: A
authors: A
authors: Martin
authors: 1] School of Molecular and Biomedical Science, The University of Adelaide, Adelaide, Australia [2] Department of Zoology, University of Cambridge, Cambridge, UK.
authors: S
authors: S
authors: Baxter
authors: 1] Institut de Systématique, Evolution, et Biodiversité, UMR 7205 CNRS, Muséum National d'Histoire Naturelle, Paris, France [2] Department of Animal Behaviour, Universität Bielefeld, Bielefeld, Germany.
authors: A
authors: A
authors: Shah
authors: 1] Institut de Systématique, Evolution, et Biodiversité, UMR 7205 CNRS, Muséum National d'Histoire Naturelle, Paris, France [2] The Smithsonian Tropical Research Institute, Balboa, República de Panamá
authors: B
authors: B
authors: Gilles
authors: 1] Institut de Systématique, Evolution, et Biodiversité, UMR 7205 CNRS, Muséum National d'Histoire Naturelle, Paris, France [2] Laboratoire Biologie Intégrative des Populations, Ecole Pratique des Hautes Etudes (EPHE), Paris, France.
authors: T
authors: T
authors: Wirth
authors: The Smithsonian Tropical Research Institute, Balboa, República de Panamá
authors: W O
authors: WO
authors: McMillan
authors: 1] Institut de Systématique, Evolution, et Biodiversité, UMR 7205 CNRS, Muséum National d'Histoire Naturelle, Paris, France [2] The Smithsonian Tropical Research Institute, Balboa, República de Panamá
authors: M
authors: M
authors: Joron
mesh_terms: D000222:Adaptation, Physiological / Q000235:genetics*; D000818:Animals; D005075:Biological Evolution; D002080:Butterflies / Q000033:anatomy & histology / Q000235:genetics*; D002874:Chromosome Mapping; D003116:Color; D003433:Crosses, Genetic; D005838:Genotype; D010641:Phenotype; D040641:Quantitative Trait Loci; D014921:Wings, Animal / Q000033:anatomy & histology*