Population genomics of divergence among extreme and intermediate color forms in a polymorphic insect

Authors: LOZIER, JEFFREY - University Of Alabama; JACKSON, JASON - University Of Alabama; DILLON, MICHAEL - University Of Wyoming; Strange, James

Submitted to: Ecology and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 12/9/2015
Publication Date: 2/22/2016
Citation: Lozier, J.D., Jackson, J.M., Dillon, M.E., Strange, J.P. 2016. Population genomics of divergence among extreme and intermediate color forms in a polymorphic insect. Ecology and Evolution. 6(4):1075-1091.

Interpretive Summary: The two-formed bumble bee is a common and broadly distributed bee in western North America. It is an important pollinator of both crops and wild land plants. In the southern and eastern parts of the species geographic range, the bee is generally red and yellow in color, but in the northern and western parts of the species range, the red is substituted for black coloration. Between these two extremes lies a broad band of bees that have an intermediate coloration. We used next generation sequencing techniques to try to understand if the intermediate coloration was from genetic hybrids of the two extremes, or represented a third, distinct lineage. Our results show that there is very little hybridization between the southeastern group and the rest of the species, indicating that the black form and the intermediate form are much more closely related to each other than they are to the red form. These results have implications for species conservation and our understanding of bumble bee evolution in North America.

Technical Abstract: Geographic variation in insect coloration is among the most intriguing examples of rapid phenotypic evolution and provides ideal opportunities to study the mechanisms of phenotypic change and diversification in closely related lineages. The bumble bee Bombus bifarius comprises two geographically disparate color groups characterized by red-banded and black-banded abdominal pigmentation, but with a range of spatially and phenotypically intermediate populations across western North America. Microsatellite analyses have revealed that B. bifarius in the contiguous U.S.A. are structured into two major groups concordant with geography and color pattern, but also suggest ongoing gene flow among regional populations. In this study, we better resolve the relationships among major color groups to facilitate a more complete understanding of evolutionary mechanisms promoting and maintaining such polymorphism. We analyze >90,000 and >25,000 single nucleotide polymorphisms derived from transcriptome (RNAseq) and double digest restriction site associated DNA sequencing (ddRAD), respectively, in representative samples from spatial and color pattern extremes in B. bifarius as well as phenotypic and geographic intermediates. Both ddRAD and RNAseq data illustrate substantial genome-wide differentiation of the red-banded (eastern) color form from both black-banded (western) and intermediate (central) phenotypes and negligible differentiation among the latter populations, with no obvious admixture among bees from the two major lineages. Results thus indicate much stronger background differentiation among B. bifarius lineages than previously suggested, highlighting potential challenges for revealing loci underlying color polymorphism from population genetic data alone. These findings will have significance for resolving taxonomic confusion in this species and in future efforts to investigate color-pattern evolution in B. bifarius as and other polymorphic bumble bee species.