There are ample examples of how natural selection has operated in nature. Yet, we have a long way to go in understanding how evolutionary change happens at the most basic, genetic level. Given the complex interactions between genes, what kinds of genetic changes are most likely to underlie adaptive variation? Adaptive phenotypic radiations offer some of the greatest promise in discovering genes responsible for variation in traits and thus revealing genetic processes underlying evolution, as they provide numerous convergent and divergent replicates and their rapid change results in a genetic signature less confounded by population structure or speciation.

Our lab studies the genetics underlying adaptive variation by focusing on two lineages that have undergone extensive divergence and convergence in color pattern as a result of Müllerian mimicry: the primarily Holearctic bumble bees (genus Bombus) and the neotropical Heliconius butterflies.

The Genetics and Evolution of Mimetic Coloration in Bumble Bees

       The ~250 species of the cold-adapted bumble bees are exceptionally color diverse, comprising >600 different patterns in their setal pile coloration across their body segments. 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 because selection favors shared advertisement of their toxicity (their sting) to predators. Bumble bee color diversity thus provides extensive replicates for understanding how traits evolve rapidly and repeatedly at the genetic level and to understand how ecological factors influence the formation of mimicry complexes over time.

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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:

 The Geographic Distribution of Mimicry

We are mapping the distribution of coloration in North American bumble bees, including both monomorphic and color polymorphic species (e.g., B. melanopygus, B. bifarius, B. flavifrons), to better characterize the extent of mimicry and the factors that may be driving mimetic color distribution (e.g., climate, historical biogeography). This includes examining both spatial and temporal correspondence of color forms and examining historical shifts in the distributions of color pattern hybrid zones. This project is lead by graduate student, Briana Ezray (right). melanodist EzrayScope

 Developmental and Adaptive Properties of Bee Pigmentation


This direction includes several ongoing projects in the lab:

1) We are using a diversity of approaches (e.g., extractability, TLC, UV-Vis, LC-MS-MS, NMR, Raman Spectroscopy, FTIR, and ToF-SIMS) to determine the chemical nature of the pigments that comprise the yellow, orange, black, and white coloration that stripes these bees and the distribution of these pigments across the lineage. In addition to exploring pigmentation in bumble bees we are examining the melanin chemistry in another mimetic Hymenopteran, the mutillids.

2) We are determining the developmental timing and tissue of deposition of pigments in bumble bees as a foundation for understanding underlying genetic mechanisms. We are examining pupal development across species and how the setae bearing these colors develop from origin to point of color deposition. This is utilizing a diversity of microscopy techniques available at the Huck Institute. Project leaders – Li Tian, Istvan Miko, Daniel Snellings.

3) We are studying the role of bee nutrition in color intensity and other factors (body size, colony development). Lab reared bumble bees tend to be a paler yellow than wild bees. By adjusting rearing parameters, we are testing what factors may influence color intensity, and thus we can better understand whether color is a bioindicator of nutritional quality and potentially involved in evolutionary trade-offs. Project leader : undergraduate Daniel Snellings.

4) We are quantifying thermoregulatory properties of bumble bee colors. Research supports correlation between overall color of bumble bees and their habitat preference, with suggestion that white is more common in deserts, black in the tropics, yellow in mid-temperate regions, and red in alpine zones. We are quantifying how much each of the colors impacts thermal properties of the bees and whether climate may influence which mimicry patterns occur where. Project leader: undergraduate Anna Nixon.

 The Genetic Basis of Mimicry in Western US Bumble Bees

A major research focus is in determining the genetic basis of mimetic color transitions in western U.S. bees. In the Western U.S. bees transition from a Pacific coastal color pattern to a Rocky Mountain mimetic pattern. Some species occur in only one of these zones but others cross both regions and converge onto local patterns by switching from black to red coloration. We are determining the genetic loci driving this red-black color switch in two of these species: Bombus melanopygus and Bombus bifarius. We will examine the role of these isolated loci in driving similar color switches across the bumble bee radiation. Postdoc Li Tian is performing gene expression and validation work on targeted loci. Graduate student Sarthok Rahman is performing bioinformatic analyses using GWAS to target and annotate color loci. Collaborators: James Strange, Jeff Lozier.
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Photo Credit: Sam Droege, USGS Survey

 The Genetic Basis of Yellow Pigmentation in Bumble Bees

Photo: J. Cnaani
We are also examining the genes that drive frequent black to yellow color switches in the subgenus Bombus s.s. using inbred laboratory colonies. We are currently testing isolated loci for the role of this gene across this incipient species complex and its function in pigmentation. Collaborator: Jonathan Cnaani.

Bee Pathogens and Pollinator Conservation

Graduate student Briana Ezray is taking a holistic approach to understanding epidemiology of bee pathogens across time and space. For this project we are performing cross-pathogen screens in bumble bees, carpenter bees, and honey bees from early, late, and midsummer collections to understand how pathogens are shared across communities, at what scale they spread, and their seasonality.  Undergraduate Jesse Schneider is screening carpenter bees and Carrie Hill is examining pollen as a representative of the community of pathogens to which these bees are exposed. This project is funded by a NE SARE grant.

Psithyrus Chemical Ecology

   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. To enter nests either they produce little characteristic smell, produce a smell that mimics their hosts, or produce a compound that repels the host species. Most likely a combination of chemical and aggressive tactics maintains this control, although the process of keeping the workers in check is not well known. Postdoc Patrick Lhomme in the lab is studying strategies of chemical and behavioral control in the lesser-known North American Psithyrus, including mechanisms of host evasion, differences in reproductive success by hosts, and potential for host imprinting. We are also studying species delimitation in North American Psithyrus using an integrative approach combining  genitalia morphology, DNA barcoding, and male cephalic gland chemistry, and in collaboration with Pierre Rasmont. psithyrusinvasion

The Genetics and Evolution of Mimetic Coloration in Heliconius butterflies

Heliconius butterflies have diverged and converged onto a patchwork of mimetic color pattern complexes across the neotropics.  Substantial progress has been made in narrowing the regions of the genome driving this mimetic color pattern variation. Recent collaborative work has revealed a gene, optix, that prefigures the location of future red patterning on these butterflies (Reed et al., 2010; Hines et al., 2012). However, we are still seeking answers to how this gene is regulated to create different red patterns. The lab is involved in collaborative projects targeting this regulatory region and revealing the network of genes involved in these phenotypes. Collaborators: W.Owen McMillan, Brian Counterman, Megan Supple, Robert Reed, James Mallet.

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Phylogenomics of Ichneumonoid Wasps

     We are using phylogenomic approaches to obtain a robust backbone phylogeny of the Ichneumonoidea, a lineage of wasps involved in parasitizing developing forms of a diversity of insects. Ichneumonoids comprise 3% of the species on earth and this radiation has made determining their historical relationships difficult. Resolving their relationships these will aid in understanding the evolution of parasitic strategies and understanding the factors promoting their diversification. Our ~450 gene, ~80 taxon dataset will aid resolution of relationships, while also examining the evolution of polydnavirus (PDVs) replication genes in these wasps. Polydnaviruses are co-evolved viruses imbedded into the genomes of some lineages of Ichneumonoidea used as a delivery system for immune-suppression genes into parasitized insect hosts. Collaborators: Barb Sharanowski, Andrew Deans, and Alan and Emily Lemmon. 8462906167_fb78d06b9a_z