Phylogeography and population genetics of pine butterflies: sky islands increase genetic divergence

Authors: Halbritter, Dale; KAWAHARA, AKITO - Florida Museum Of Natural History; STORER, CAROLINE - Florida Museum Of Natural History; DANIELS, JARET - Florida Museum Of Natural History

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/7/2019
Publication Date: 11/7/2019
Citation: Halbritter, D.A., Kawahara, A., Storer, C., Daniels, J. 2019. Phylogeography and population genetics of pine butterflies: sky islands increase genetic divergence. Ecology and Evolution. 9(23):13389-13401. https://doi.org/10.1002/ece3.5793.
DOI: https://doi.org/10.1002/ece3.5793

Interpretive Summary: Forested mountain habitats in arid regions, much like oceanic islands in shallow seas, are known to change in both area and connectivity over time due to historical climate changes and geological processes. Here, the dispersal capabilities and recent evolutionary history of two species of butterflies residing in isolated mountain habitats were inferred from the careful analysis of thousands of DNA sequences sampled from across the genome of each species. Results indicate the geographic distance between the sky island mountains of southeastern Arizona, with the closest mountains being 56 km apart, is sufficient to maintain genetic isolation between populations of Neophasia terlooii residing on each mountain. In contrast, the largely connected habitat in northern Arizona in which Neophasia menapia resides facilitates genetic mixing. Thus N. menapia are able to disperse and breed within their range in northern Arizona, while N. terlooii rarely, if ever, travel between mountains. Genetic relationships among N. terlooii indicate populations on near mountains are more closely related to each other than populations on far mountains, suggesting some dispersal had occurred recently on an evolutionary time scale. During the last ice age, for example, mountain habitats were likely more connected, thereby allowing dispersal to occur. Studies such as this contribute to a better understanding of evolution of organisms in isolated habitats during times of change.

Technical Abstract: Aim The sky islands of southeastern Arizona (AZ) are considered a neglected biodiversity hotspot, as they mark a major transition zone between tropical and temperate biota. Our aim was to investigate the population structure and phylogeography of two pine-feeding pierid butterflies restricted to these "islands" at this transition zone: the pine white (Neophasia menapia) and the Mexican pine white (N. terlooii). Given their dependence on pine as the larval host in AZ, we hypothesized that habitat connectivity will affect population structure and is at least partly responsible for their allopatry. Location Seventeen sites within pine forests on the Kaibab Plateau, Mogollon Rim, White Mountains, and sky islands of AZ Methods Genomic DNA was extracted from freshly collected butterflies and a ddRADSeq library was created for each barcoded individual. Up to 15,399 SNPs were discovered and used in population genetic and phylogenetic analyses. We utilized both Stacks and pyRAD pipelines for locus discovery and genotyping, and several downstream analytical techniques to gather multiple lines of evidence. Results Most evidence suggests N. menapia is panmictic. There is some support for individuals north of the Grand Canyon being genetically distinct from individuals on the Mogollon Rim. There is strong evidence for population structure within N. terlooii. Each sky island likely contains a population, and clustering is hierarchical, with populations on proximal mountains being more related to each other. Main conclusions The connected N. menapia habitat facilitates panmixia while the sky islands, separated by as little as 56 km, create distinct population structure for N. terlooii. Both loci discovery and genotype calling pipelines, despite only sharing up to 17.9 % of loci, allowed us to reach the same conclusions. The historical climate-driven fluxes in forest habitat connectivity have implications for understanding the biodiversity of fragmented habitats.