A homeotic shift late in development drives mimetic color variation in a bumble bee

Authors: TIAN, LI - Pennsylvania State University; RAHMAN, SARTHOK - Pennsylvania State University; EZRAY, BRIANA - Pennsylvania State University; FRANZINI, LUCA - Pennsylvania State University; Strange, James; LHOMME, PATRICK - International Center For Agricultural Research In The Dry Areas (ICARDA)

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 4/5/2019
Publication Date: 5/1/2019
Citation: Tian, L., Rahman, S., Ezray, B., Franzini, L., Strange, J.P., Lhomme, P. 2019. A homeotic shift late in development drives mimetic color variation in a bumble bee. Proceedings of the National Academy of Sciences. 116(24):11857-11865. https://doi.org/10.1073/pnas.1900365116.
DOI: https://doi.org/10.1073/pnas.1900365116

Interpretive Summary: Changes in genetics of organisms that occur during species evolution result in changes in physical traits. This study observes the changes in hair color of bumble bees and the underlying changes to the genome that cause color change. Bumble bees are excellent study organisms due to high level of color variation they have in nature. The genetic mechanism that determines color variation in the Black-tailed Bumble Bee were discovered and we found that this mechanism is not universally involved in color determination in bumble bees.

Technical Abstract: Natural phenotypic radiations, with their high diversity and convergence, are opportune for informing how genomic changes translate to natural phenotypic variation. New genomic tools enable discovery in such traditionally non-model systems. Here, we characterize the genomic basis of color pattern variation in bumble bees (Hymenoptera, Apidae, Bombus), a group that has undergone rampant convergence of setal color patterns as a result of Müllerian mimicry. In western North America, multiple species converge on local mimicry patterns through parallel shifts of mid-abdominal segments from red to black. Using genome-wide association we establish that a cis-regulatory locus between the abdominal fate-determining Hox genes, abd-A and Abd-B, controls the red-black color switch in a western species, Bombus melanopygus. Genomic modifications at this locus generate distinct shifts in Abd-B aligned with the duration of setal pigmentation at the pupal-adult transition. This results in atypical anterior Abd-B expression, a late developmental homeotic shift. Changing expression of Hox genes is unexpected given their important role across segmental phenotypes, however, the late timing reduces this pleiotropy, making Hox genes suitable targets. Analysis of this locus across mimics and relatives reveals that other species follow independent genetic routes to obtain the same phenotypes.