Patterns of divergence across the geographic and genomic landscape of a butterfly hybrid zone associated with a climatic gradient

Authors: Ryan, Sean; FONTAINE, MICHAEL - University Of Groningen; SCRIBER, J - Michigan State University; O'NEIL, SHAWN - Oregon State University; PREFENDER, MICHAEL - University Of Notre Dame; HELLMAN, JESSICA - University Of Notre Dame

Submitted to: Molecular Biology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/15/2017
Publication Date: 7/20/2017
Citation: Ryan, S.F., Fontaine, M.C., Scriber, J.M., O'Neil, S.T., Prefender, M.E., Hellman, J. 2017. Patterns of divergence across the geographic and genomic landscape of a butterfly hybrid zone associated with a climatic gradient. Molecular Biology and Evolution. https://doi.org/10.1111/mec.14236.
DOI: https://doi.org/10.1111/mec.14236

Interpretive Summary: Understanding how climatic (seasonal) variation affects the evolution of insect species is critical to their conservation, management and control. The aim of this study was to explore how climate can influence the geographic and genomic landscape of divergence within a butterfly hybrid zone. Genomic analyses in this study suggest that adaptation to geographic variation in climate can act as a powerful isolating barrier in the face of ongoing gene-flow and lead to highly heterogeneous patterns of introgression across genome. This study is one of few to provide evidence of climate maintaining genome-wide divergence across a hybrid zone and represents a critical first step in elucidating how climate drives and maintains divergence at the genome level. A scientist at the Center for Medical, Agriculture, and Veterinary Entomology, USDA-ARS, Gainesville, Florida carried out this work as part of the dissertation research before joining USDA-ARS.

Technical Abstract: The process of speciation is impacted by the interaction between the genomic architecture of diverging lineages and the environmental context they occupy. Yet, while climate can have a significant impact on this interaction, its role in determining the patterns of geographic and genomic divergence in hybridizing species remains unresolved. A hybrid zone between two species of butterfly–Papilio glaucus and Papilio canadensis–is one of few hybrids zones where variation in climate appears to be the salient factor maintaining divergence. Here we characterized the geographic and genomic landscape of divergence within a climatic gradient and show that divergence varies across the genome (gene flow varies across mtDNA, sex and autosomes). However, the Z (sex) chromosome which is associated with diapause (seasonal dormancy) harbors a disproportionately greater degree of divergence (high FST and low nucleotide diversity) than other chromosomes. Further, there is strong evidence to suggest the hybrid zone is maintained by migration and strong selection against hybrids. More specifically, climate (length of the growing season) appears to driving divergence across the genomes of these hybridizing species and the Z chromosome in particular. Together, these results suggest that climate is capable of driving genome-wide divergence, but may be dependent on the architecture and location of climate-associated genes within the genome.