Evolution and genetics of mimetic coloration in bumble bees

       The ~250 species of the cold-adapted bumble bees are exceptionally color diverse. One of the main factors driving such variation is localized selection through Müllerian mimicry – taxonomically diverse species in the same geographic region have convergently evolved a similar color pattern as selection favors shared advertisement of their toxicity (their sting) to predators. Bumble bee color diversity provides extensive replicates for understanding genomic targets of evolution (evolutionary genetics) (Hines and Rahman, 2019), for understanding how ecological factors influence the formation of mimicry complexes over time (evolutionary ecology), and for understanding how developmental genes such as segmentation genes control phenotypic variation (evo-devo).

Through an NSF CAREER project, we are developing the bumble bee system for understanding the genetic regulation of adaptive phenotypic variation. This involves several directions:

  • Documenting mimetic distributions and developing new techniques for quantifying mimicry (Ezray et al., 2019).
  • Determining the genetic basis of mimetic convergence in bumble bees. We have determined that a late developmental homeotic shift in Hox genes induced mimetic color variation in one species (B. melanopygus) (Tian et al., 2019) and are studying whether other species that attain these same patterns do so using similar mechanisms. We will continue to explore mechanisms driving mimetic color diversity in these bees using genomic and developmental genetic approaches.
  • Examining the genes that drive frequent black to yellow color switches in the subgenus Bombus s.s.
  • Understanding pigmentation. We have characterized the pigments in bumble bees (Hines et al., 2017, Hines, 2008) and continue to examine factors influencing their pigmentation with the goal of understanding the genetic links between upstream developmental genes and downstream pigmentation pathways.
  • We are characterizing bumble bee development (Tian et al., 2018) and the functional morphology and development of the bumble bee setal pile. While bumble bee pile is touted for its role in thermoregulation, we are exploring alternative functions of these hairs.

Photo credits: J. Cnaani (upper right), Sam Droege, USGS Survey (upper middle)

Bee pathogens and pollinator conservation

Bumble bee diversity has changed dramatically in the last 20 years and one of the major factors contributing to this is the spread of bee pathogens. We seek to contribute to growing data to help determine the major factors threatening these bees. We are:

  • Modeling bee pathogen epidemiology. We are performing a large scale survey in central PA to understand epidemiology of bee pathogens across time and space. This project involves cross-pathogen screens in bumble bees, carpenter bees, and honey bees across the season to understand how pathogens are shared across communities, at what scale they spread, and the role of different species in pathogen overwintering and maintenance.
  • Understanding bee virus transmission across insect communities. We are studying whether DWV and BQCV, the two most common bee viruses, can be directly transmitted between honey bees, bumble bees, and nest commensals using laboratory experiments.
  • Determining the factors and duration of virus persistence in the environment. We are determining how long bee viruses persist in various conditions to understand the role the timing between bee floral visitors and floral morphology may play in pathogen transmission.
  • Determining how bee virus communities change over time. We are determining changes in bee virus strains and composition in honey bee pollen over the last decade to understand how temporally dynamic these communities can be.
  • Landscape factors impacting bumble bee pathogen loads. Although understanding what pathogens are present is an important part of developing solutions for bee health, finding solutions to reduce pathogen loads is a more difficult task. One solution is preventative, in maintaining healthy bees with less likelihood of succumbing to and spreading pathogens. To address this, as part of a large collaborative grant (funding: Foundation for Food and Agriculture Research), we are comparing the role of a variety of landscape conditions throughout Pennsylvania on the virus load and immune gene upregulation in bumble bee communities. This will help us identify the primary habitats and resources of value to maintatining healthy bees. Primary Collaborators: Christina Grozinger, Margarita Lopez-Uribe, D.J. McNeil

Mechanisms of gall induction by gall wasps

Gall wasps oviposit into developing plant tissues where larvae induce the formation of elaborate and predictable gall morphologies. The ways in which both adults and developing larvae induce this developmental change remain largely unknown. With an NSF funded grant, we are combining comparative phylogenomics, comparative gland morphology, and transcriptomic and metabolomic approaches to explore potential mechanisms of gall induction. These analyses are comparing across species, sexual/asexual generations, and larval/adult generations of gall wasps.

Just a sampling of some of the incredible diversity of gall morphologies induced by gall wasp species. From Left: Wooly catkin gall wasp (Callyrhytis quercusoperator) including both asexual and sexual galling generations, Hedgehog gall (Acraspis erinacei), Honeycomb leaf gall (Callyrhytis favosa), Clustered midrib gall (Andricus dimorphus), Wooly oak gall (Callyrhytis lanata). Images by collaborator Andy Deans, available on iNaturalist.

Role of nectar metabolites in pollinator visitation bias and health

We are examining the role of plant defense compounds in nectar, focusing on milkweed toxins (cardenolides), in bumble bee visitation bias. These data are being used to understand differences in mechanisms of resistance across bumble bees, and how these might translate to differential response to pesticides and pathogens in their environment.

The evolution of social parasitism in bumble bees

Most bumble bees have a life history that starts with nest initiation by a lone queen who then produces several generations of workers that ultimately will rear some of their sisters to become new reproductive queens.  Some bumble bees, those in the subgenus Psithyrus, use a different strategy. They invade the young nests of other species, take over – either through killing or coinhabiting with the resident queen – and coerce the workers of this young colony to rear their reproductive offspring instead. Recent research on European species has revealed some of the strategies by which they manage to evade their hosts. We are seeking to understanding this strategy better by studying:

  • Strategies of chemical and behavioral control in North American Psithyrus, including mechanisms of host evasion, differences in reproductive success by hosts, mechanisms inducing larval feeding, and potential for host imprinting.
  • Species delimitation in North American Psithyrus using an integrative approach combining genitalia morphology, DNA barcoding, and male cephalic gland chemistry.
  • Comparative genomics of host and socially parasitic bumble bees to determine genes under selection potentially related to parasitism.