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written by: Jenan El-Hifnawi We all know the bumble bee - their black and yellow bodies are a staple of landscapes across Maryland. If we stumbled upon a bumble bee in Turkey, however, many of us would be surprised that they don’t fit our black and yellow mold. Globally, bumble bees (Bombus) have over 400 known color patterns - far more than the 265 Bombus species. They range from mostly frosty white to entirely jet black or yellow, and they span almost every possible color pattern in between. Dr. Heather Hines, Professor of Entomology and Biology at Penn State University, investigates the genetic basis of these color patterns. Bumble bees' diverse coloration is often the result of Müllerian mimicry: a phenomenon in which multiple co-distributed toxic species converge on a single phenotype to strengthen the deterrent effect of their warning signal. In bumble bees, distantly related species that coexist in the same region will converge on the same color pattern, creating more opportunities for predators to learn their lesson through a sting. In Turkey for example, eight bumble bee species from distant lineages converged upon black and white coloration. There are many of these “mimicry complexes” across the globe, with bumble bees’ phenotypes often clustering geographically rather than along species lines.  Eight bumble bee species converged on similar color patterning, codistributed in Turkey Photo Credit: Bombus of Turkey, Atlas Hymenoptera Mimicry complexes frequently overlap spatially, creating a continuum of many intermediate phenotypes. In addition to creating phenotypic diversity, mimetic complexes increase genetic diversity within species, as local mimicry complexes drive populations in different parts of the species range to diverge as they assimilate to their local color pattern. This is called mimetic radiation - something well studied in Heliconius butterflies. High diversity isn't the only thing making Bombus mimetic radiation such an exciting research opportunity. Convergent evolution of different lineages to the same color pattern provides the perfect opportunity to explore evolutionary development. Each lineage converging on the same phenotype is like a replicate of evolution. This allows Dr. Hines to ask if the same genetic mechanism is responsible for generating this phenotype every time, or if different lineages took different routes to the same color pattern. Dr. Hines approached this question using a Genome Wide Association Test (GWAS). The GWAS identified regions in the genome responsible for phenotypic variation by identifying regions where genetic variation correlates with phenotypic variation. In other words, in a species which has both red-tailed bees and black-tailed bees, Dr. Hines found where black tailed individuals had one version of that gene (allele), and red-tailed individuals have a different version. Prior to completing GWAS, however, she needed to complete population genetic analyses to confirm that each species she investigated was truly a single species. This proved necessary as she discovered B. bifarius is actually 2 species: the true B. bifarius, and B. vancouverensis. B. bifarius is only red, while B. vancouverensis has red, black, and intermediate forms, making the two species difficult to separate morphologically. Once she confirmed the species status of each taxon, she completed GWAS in B. melanopygus and B. vancouverensis. Both occur in the Western US and exhibit both black and red forms, participating in overlapping mimicry complexes near the Rockies and Pacific coast. While they’re in mimetic complexes together, each species has its own story. The intermediate forms present in B. vancouverensis suggest its color depends on more than one gene. B. melanopygus, on the other hand, only has two discrete forms - black or red. This suggests a single gene is responsible. In B. melanopygus, the GWAS identified a single gene where black forms have 75 base pair deletion, and red forms don’t. B. vancouverensis had a similar result: black forms had a 7 base pair deletion in the same gene! While located in the same region, the deletions are notably different. They result from different evolutionary events targeting the same “evolutionary hotspot”, not a single mutation shared between species.  The gene in question regulates Hox abdominal genes A and B (AbdA and AbdB). Hox genes help determine the body plan of an organism, with AbdA and AbdB responsible for the anterior region of the abdomen (towards the head), and the posterior region respectively. They’re famous for their ability to cause drastic “homeotic” mutations in which body segments are moved, multiplied, or otherwise transformed when Hox genes are expressed in different parts of the body than usual.
Through comparative transcriptomics, Dr. Hines established that AbdB is expressed more in red individuals than black individuals in multiple Bombus species. AbdB seems to “turn on” red pigment genes in posterior abdominal segments. Interestingly, AbdB is also expressed in anterior regions of the abdomen in red individuals - somewhere it typically is not expressed. The unusual expression caused red pigment production in anterior segments, showing the ability of Hox genes to change color patterns by being expressed in different body segments. No drastic homeotic mutations are caused because the relocated expression occurs very late in development - body segment structure has already been established. The ability of Hox genes to readily change color patterns underscores the importance or relying on characters beyond color for identification and classification. These findings also highlight the importance of mutation in driving the generation of diversity. Among closely related species, different bumble bees independently targeted the same gene in similar ways. These conclusions only scratch the surface of Dr. Hines’ work. For more information, check out the Hines Lab website. Learn more about Dr. Heather Hines’ work through some of her related publications: Rahman, S. R., T. Terranova, L. Tian, & H.M. Hines. 2021. Developmental transcriptomics reveals a gene network driving mimetic color variation in a bumble bee. Genome Biology and Evolution. evab080, https://doi.org/10.1093/gbe/evab080 Wanhu Yang, Jixiang Cui, Yuxin Chen, Chao Wang, Yuanzhi Yin, Wei Zhang, Shanlin Liu, Cheng Sun, Hu Li, Yuange Duan, Fan Song, Wanzhi Cai, Heather M Hines, Li Tian. Genetic modification of a Hox locus drives mimetic color pattern variation in a highly polymorphic bumble bee, Molecular Biology and Evolution, 2023, msad261, https://doi.org/10.1093/molbev/msad261 Ezray BD, Wham DC, Hill CE, Hines HM. Unsupervised machine learning reveals mimicry complexes in bumblebees occur along a perceptual continuum. Proc Biol Sci. 2019 Sep 11;286(1910):20191501. doi: 10.1098/rspb.2019.1501. Epub 2019 Sep 11. PMID: 31506052; PMCID: PMC6742998. Jenan El-Hifnawi is a third-year Masters student in the Espíndola Lab. Her research seeks to explore the impacts of Ice Age glaciations on the diversification and range of several South Andean bee species using comparative phylogeographic methods. Comments are closed.
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