Crossing fitness valleys: empirical estimation of a fitness landscape associated with polymorphic mimicry.
Characterizing fitness landscapes associated with polymorphic adaptive traits enables investigation of mechanisms allowing transitions between fitness peaks. Here, we explore how natural selection can promote genetic mechanisms preventing heterozygous phenotypes from falling into non-adaptive valleys. Polymorphic mimicry is an ideal system to investigate such fitness landscapes, because the direction of selection acting on complex mimetic colour patterns can be predicted by the local mimetic community composition. Using more than 5000 artificial butterflies displaying colour patterns exhibited by the polymorphic Müllerian mimic Heliconius numata, we directly tested the role of wild predators in shaping fitness landscapes. We compared predation rates on mimetic phenotypes (homozygotes at the supergene controlling colour pattern), intermediate phenotypes (heterozygotes), exotic morphs (absent from the local community) and palatable cryptic phenotypes. Exotic morphs were significantly more attacked than local morphs, highlighting predators' discriminatory capacities. Overall, intermediates were attacked twice as much as local homozygotes, suggesting the existence of deep fitness valleys promoting strict dominance and reduced recombination between supergene alleles. By including information on predators' colour perception, we also showed that protection on intermediates strongly depends on their phenotypic similarity to homozygous phenotypes and that ridges exist between similar phenotypes, which may facilitate divergence in colour patterns.
Institut Systématique, Evolution, Biodiversité, UMR 7205 MNHN-CNRS-EPHE-UPMC- Sorbonne universités, Muséum National d'Histoire Naturelle, Bâtiment d'entomologie, CP050, 57, rue Cuvier, 75005 Paris, France UMR CNRS 7179, CNRS-MNHN MECADEV, Muséum National d'Histoire Naturelle, 1, avenue du petit château, 91800 Brunoy, France moarias@gmail.com.
Mónica
M
Arias
Institut Systématique, Evolution, Biodiversité, UMR 7205 MNHN-CNRS-EPHE-UPMC- Sorbonne universités, Muséum National d'Histoire Naturelle, Bâtiment d'entomologie, CP050, 57, rue Cuvier, 75005 Paris, France.
Yann
Y
le Poul
Institut Systématique, Evolution, Biodiversité, UMR 7205 MNHN-CNRS-EPHE-UPMC- Sorbonne universités, Muséum National d'Histoire Naturelle, Bâtiment d'entomologie, CP050, 57, rue Cuvier, 75005 Paris, France.
Mathieu
M
Chouteau
Institut Systématique, Evolution, Biodiversité, UMR 7205 MNHN-CNRS-EPHE-UPMC- Sorbonne universités, Muséum National d'Histoire Naturelle, Bâtiment d'entomologie, CP050, 57, rue Cuvier, 75005 Paris, France Département de Biologie, Ecole Normale supérieure, 75 005 Paris, France.
Romain
0000-0003-4317-1064
R
Boisseau
Department of Biology, University of York, Wentworth Way, York YO10 5DD, UK.
Neil
N
Rosser
UMR CNRS 7179, CNRS-MNHN MECADEV, Muséum National d'Histoire Naturelle, 1, avenue du petit château, 91800 Brunoy, France.
Marc
M
Théry
Institut Systématique, Evolution, Biodiversité, UMR 7205 MNHN-CNRS-EPHE-UPMC- Sorbonne universités, Muséum National d'Histoire Naturelle, Bâtiment d'entomologie, CP050, 57, rue Cuvier, 75005 Paris, France.
Violaine
V
Llaurens
D000220:Adaptation, Biological; D000818:Animals; D000067558:Biological Mimicry / Q000235:genetics* / Q000502:physiology*; D002080:Butterflies / Q000235:genetics* / Q000502:physiology*; D003118:Color Perception; D056084:Genetic Fitness; D008954:Models, Biological; D010641:Phenotype; D010858:Pigmentation / Q000235:genetics / Q000502:physiology; D011110:Polymorphism, Genetic; D011235:Predatory Behavior; D012641:Selection, Genetic
aposematism; dominance; generalization; heterozygote; linkage disequilibrium; passion-vine butterfly