Connecting Genotypes to Phenotypes: Bumble Bees as a New Model System for Pigmentation Genetics
Open Access
- Author:
- Rahman, Sarthok Rasique
- Graduate Program:
- Biology
- Degree:
- Doctor of Philosophy
- Document Type:
- Dissertation
- Date of Defense:
- December 11, 2020
- Committee Members:
- Heather M Hines, Dissertation Advisor/Co-Advisor
Stephen Wade Schaeffer, Committee Chair/Co-Chair
Christina M Grozinger, Committee Member
Istvan Albert, Outside Member
Timothy J Jegla, Program Head/Chair - Keywords:
- Bombus
Bumble bee
evo-devo
Abd-B
Hox
cut
Müllerian mimicry
pigmentation genetics
color genetics
Arthropod genetics
Hymenoptera - Abstract:
- Repeated instances of phenotypic evolution have been particularly advantageous to evolutionary genetics research. These systems not only lead to the discovery of implicated genes behind phenotypes, but they provide a comparative framework to discover underlying “rules of life” through revealing the diversity of genomic routes to a similar phenotypic outcome and the evolutionary trajectory of such variants. Until recently, such research relied heavily on a limited number of model organisms, however, the advent of high-throughput genome sequencing techniques, availability of genomic resources, and computational tools have enabled the exploration of a wide range of non-model systems. In this dissertation, I investigate the genomic basis of color variation in a new non-model organism, bumble bees (Genus: Bombus), which exhibit exceptional segmental color pattern diversity primarily driven by Mullerian mimicry. Their repeated convergence onto local mimetic color patterns provides many natural replicates, making this system ideal for evolutionary genetics. To begin to uncover the genetic underpinnings driving mimetic color variation in bumble bees, in Chapter 2, I utilize a genome-wide association study (GWAS) to identify the locus that controls the red/black mid-abdominal color switch involved in convergence onto western North American mimicry complexes in the bumble bee, B. melanopygus. This was localized to an ~4KB cis-regulatory region that alters the gene expression of a Hox gene driving abdominal segmental fate, Abd-B. This gene was found to be expressed in a location anterior to its normal expression, thus involves a late-developmental homeotic shift to drive this adaptive coloration. In Chapter 3, I used a developmental transcriptomics (RNA-Seq) approach at a key developmental stage to reveal how Abd-B turns on differences in pigmentation in B. melanopygus and build the gene regulatory network for this phenotypic transition. Strong differential expression was found not only in the upstream gene (Abd-B), but also in a likely intermediate developmental gene (nubbin), and in a suite of downstream melanin and redox genes that likely interact to generate distinct color dimorphism. In Chapter 4, I take advantage of the natural replicates of the system through examining the genetic basis of the same red/black color switch in a North American bumble bee co-mimic, B. vancouverensis, using a GWAS approach. This revealed the potential involvement of a 7-bp nearly fixed deletion event that aligns to the location of a color dimorphic deletion event in the established Abd-B color interval of B. melanopygus, indicating that an independent deletion in the same conserved cis-regulatory region of the same gene has been targeted to generate a similar phenotypic outcome in two co-mimicking species. In Chapter 5, using a combination of WGS and RAD-Seq on a lab-generated yellow color variant in bumble bee B. terrestris, I discover an additional upstream developmental player (cut) involved in pigmentation. My dissertation work, more broadly, unravels several novel upstream and downstream genes driving bumble bee pigmentation variation. Some of these upstream developmental transcription factors (e.g., Abd-B, nubbin, cut) were thought to be highly conserved and pleiotropic, however, my research shows how they can be excellent evolutionary targets to regulate novel morphological features. My research also demonstrates the repeated use of a potential genomic hotspot to generate similar but independently evolved genomic routes that can drive phenotypic diversification in bumble bee mimetic radiation. Overall, my dissertation work provides foundational data for a new model system in evolutionary genetics.