Integrating ecological genomics and eco-evo-devo reveals multiple adaptive peaks in ant populations of the Arizona Sky Islands

Abstract

Uncovering the genetic basis of adaptation is a great challenge facing evolutionary biologists. We ask where is the locus of adaptation from the perspective of ecological genomics (ecogen) and evolutionary developmental biology (evodevo). Ecogen focuses on identifying loci under selection between populations in different environments by scanning genome-wide patterns of genetic divergence, while evodevo focuses on candidate developmental regulatory genes and networks underlying phenotypic differences between species and higher taxa. We attempt to reconcile these different perspectives by studying the response of ant populations to past climate change on the Arizona Sky Islands - high elevation mountain ranges that represent a replicated natural experiment. We previously used an evodevo approach to show that adaptation to climatic changes in the Arizona Sky Islands in the ant species Monomorium emersoni occurred through repeated changes within the gene network underlying the development of alternative dispersal phenotypes: winged and wingless queens. Here, using an ecogen approach we uncovered several loci under positive selection that associate with habitat temperature. These temperatureassociated loci show a repeated increase in frequency following climatic changes on each of the Sky Islands. Surprisingly, gene flow between locations within a Sky Island is restricted by temperature adaptation along the ecological gradient and not by dispersal phenotype. This finding suggests that determination of winged and wingless queens may be developmentally plastic, and this plasticity may facilitate jumps between adaptive peaks on a fitness landscape. Integration of evodevo and ecogen reveals multiple adaptive peaks and predictability at multiple biological levels within a single species.