Hiding in plain sight: unveiling cryptic diversity and patterns in bumble bees

Bumble bee research has a rich history that spans more than three centuries. The distributions and the vibrant color patterns of nearly all species of bumble bees are well mapped and described. In addition, the natural history, colony structure and social behavior of bumble bees are well documented and a well-supported phylogeny of the ~250 species currently recognized within the genus has been constructed. Yet despite the breadth of research that has been conducted on bumble bees, there is still much that is unknown about this charismatic group of social insects. My dissertation focuses on three areas: phylogenetics, population genetics and evolutionary development. In Chapter One I explore the population genetics of the Bombus ephippiatus-Bombus wilmattae species group. The color pattern diversity within this group across a variety of habitats in Mexico and Central America has brought their taxonomic status into question for over 150 years. To resolve the uncertain species status of this group, I collected extensive genetic data from twelve microsatellite loci and a fragment of the cytochrome oxidase I gene to conduct an in-depth population genetic and phylogenetic study of the group across its widespread distribution. I also explore the use of wing geometric morphometrics to delineate species within this taxon. This group exhibits extensive genetic structure across its range, with major barriers to gene flow at the Isthmus of Tehuantepec in southern Mexico and the Nicaraguan Depression in southern Nicaragua. Wing morphometric data support these genetic divisions within the species complex. The differences in wing shape are not sufficiently divergent to be useful as species diagnostic characters, but they provide another line of evidence to support species boundaries. These extensive genetic and morphometric data provide a wealth of evidence for revising the taxonomic status of the B. ephippiatus-B. wilmattae complex. In Chapter Two, I describe two genetically distinct, sympatric species with limited gene flow in Mexico south of the Isthmus of Tehuantepec through Honduras. I revise the species B. wilmattae within this region to include previously unknown queen and worker polymorphisms and describe a new species sympatric with B. wilmattae, B. maya sp. nov. I recognize a single species in Mexico north of the Isthmus of Tehuantepec, with extensive population structure corresponding to the four main mountain ranges of the Mexican highlands. I consider the species B. ephippiatus to extend only from northwest Mexico to the southern state of Oaxaca, just north of the Isthmus of Tehuantepec. There is also a distinct species in Costa Rica, to which I assign the resurrected name B. schneideri. In Chapter Three, I explore trends in variation among the color patterns of Bombus worldwide. The white, yellow, orange, and black contrasting stripes of color on bumble bees have long served as classic examples of aposematic coloration and their convergence upon common patterns across their extensive distribution has served as a classic example of Müllerian mimicry. Yet nothing is known about the developmental regulation of these color patterns. As a first step in exploring the developmental regulation of color, I mapped the color patterns across the body of individual species with high resolution using a grid map. My collaborators and I use this system to look for common elements of pattern across ~95% of the known species of bumble bees. This novel method revealed twelve primary pattern elements across the dorsal thorax and abdomen, with six on the thorax and six on the abdomen. It also revealed five smaller secondary pattern elements that lie medially and laterally on the abdomen. With the exception of three elements on the scutum, these primary elements correspond to segmental boundaries across the body, which suggests that the developmental regulation of color pattern might involve Hox genes, the same genes that control the development of segmental boundaries early in development. This meticulous exploration of color pattern also revealed common trends in the occurrence of certain colors across the body. Black hairs occur in the center of the thorax in up to 77% of the species included in the analysis, and yellow hairs are found predominantly anteriorly and posteriorly along the edges of the thorax and the first two segments of the abdomen. Orange hairs predominate throughout the last segments of the abdomen. The differential patterns of color expression across species suggest that certain colors occur in specific positions on the body to maximize contrast and aposematic signal to predators. My study of the genotypic and phenotypic diversity of the B. ephippiatus-B. wilmattae species group and investigation of the core elements of pattern responsible for generating the diversity of color patterns across Bombus worldwide explore historically well-characterized systems, providing novel insights into long-standing questions within each system using new methods and approaches

Relocation risky for bumblebee colonies

Climate change impacts on bumblebees converge across continentsFil: Lozier, Jeffrey. University of Alabama; Estados UnidosFil: Cameron, Sydney. University of Illinois; Estados UnidosFil: Duennes, Michelle. University of Illinois; Estados UnidosFil: Strange, James. State University of Utah; Estados UnidosFil: Williams, Paul. Natural History Museum; Reino UnidoFil: Goulson, David. University of Sussex; Reino UnidoFil: Brown, Mark. University of London; Reino UnidoFil: Morales, Carolina Laura. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Patagonia Norte. Instituto de Investigaciones en Biodiversidad y Medioambiente. Universidad Nacional del Comahue. Centro Regional Universidad Bariloche. Instituto de Investigaciones en Biodiversidad y Medioambiente; ArgentinaFil: Jepsen, Sarina. Xerces Society; Estados Unido

Phylogeny and color pattern evolution in a New World bumble bee (Hymenoptera: Apidae: Bombus: Pyrobombus) species complex

Bombus ephippiatus is one of the most common and widespread bumble bee species throughout Mexico and Central America. This robust and charismatic species possesses a highly variable color pattern throughout its wide distribution across montane and lowland regions, which raises the question of whether or not it is in fact one species. I examined the molecular phylogeny of B. ephippiatus populations and its sister species, B. wilmattae and B. impatiens, with the aims of resolving the species relationships, distinguishing species boundaries and examining correlations between color pattern and phylogeny. I applied DNA sequences from three genes to resolve the species-level phylogeny and to gain insight into the population structure of B. ephippiatus. The results reveal that B. impatiens is the sister group to B. ephippiatus + B. wilmattae. Results also suggest that B. ephippiatus is paraphyletic with respect to B. wilmattae, as B. wilmattae attaches to the Costa Rican B. ephippiatus clade. The B. ephippiatus + B. wilmattae complex appears to be associated with geography and color pattern, providing new insights into the evolutionary history of this complex

Information of each museum bumble bee specimen screened for Nosema

Table showing details of bees screened for Nosema. Details include specimen ID of bees, institution of origin, notes written on museum label associated with each bee, collection date, geographic origin of bee and number of times a bee was screened for Nosema using PCR

Alignment of representative SSU rRNA sequences (fasta format)

Fasta file of representative SSU rRNA sequences. See file ssurRNA_counts.csv for information on which insect hosts these ssu rRNA sequences are associated with

Data from: A test of the invasive pathogen hypothesis of bumble bee decline in North America

Emergent fungal diseases are critical factors in global biodiversity declines. The fungal pathogen Nosema bombi was recently found to be widespread in declining species of North American bumble bees (Bombus), with circumstantial evidence suggesting an exotic introduction from Europe. This interpretation has been hampered by a lack of knowledge of global genetic variation, geographic origin, and changing prevalence patterns of N. bombi in declining North American populations. Thus, the temporal and spatial emergence of N. bombi and its potential role in bumble bee decline remain speculative. We analyze Nosema prevalence and genetic variation in the United States and Europe from 1980, before an alleged introduction in the early 1990s, to 2011, extracting Nosema DNA from Bombus natural history collection specimens from across this time period. Nosema bombi prevalence increased significantly from low detectable frequency in the 1980s to significantly higher frequency in the mid- to late-1990s, corresponding to a period of reported massive infectious outbreak of N. bombi in commercial bumble bee rearing stocks in North America. Despite the increased frequency, we find no conclusive evidence of an exotic N. bombi origin based on genetic analysis of global Nosema populations; the widespread Nosema strain found currently in declining United States bumble bees was present in the United States before commercial colony trade. Notably, the US N. bombi is not detectably different from that found predominantly throughout Western Europe, with both regions characterized by low genetic diversity compared with high levels of diversity found in Asia, where commercial bee breeding activities are low or nonexistent

Distribution of haplotypes of 6 Nosema genomic loci

Count of Roche 454 pyrosequencing haplotypes (rows) of 6 Nosema genomic loci in 31 bumble bee samples (columns). See Table S4 for geographic origins of these bee samples. Allele frequency data are used to generate Da distances and neighbor joining tree

Nosema genomic loci information

Information of six genomic loci used to genotype Nosema from 31 bumbles from North America and Europe. The top BlastX hit of each locus matches a sequence from another Nosema species.

Distribution of representative SSUrRNA sequences in various insect samples

Table showing how many times each SSU rRNA representative sequence (rows) is found in each insect sample (columns). Samples were from GenBank, or sequenced with Sanger sequencing or pyrosequencing. Each sample name contains sample ID/GenBank accession no. followed by parasite identification and/or host species identification. See Table S3 for other information associated with each insect sample. See Fig. S4 for phylogenetic network with labeled nodes. Representative DNA sequences can be found in fasta format in the file ssurRNA_rep_sequences.fasta