A problem for understanding bumblebee biogeography is that if bumblebees dispersed from Asia through North America to South America, if they are poor at long-distance dispersal with establishment over sea, and if the land bridge between North and South America was not established until c. 3 Ma BP, then there is an apparent conflict with the divergence among currently endemic South American lineages having been dated as early as 15–17 Ma. Using the first complete phylogenetic trees for all known and accepted extant species of the groups involved, we show how this conflict could be resolved. We suggest that characterizing bumblebees as being associated generally with temperate flower-rich meadows conflates divergent habitat specializations between two early lineages, associated with northern lowland grasslands and with southern montane grasslands respectively, which may have driven divergences in behaviour and in biogeographic processes. First, for most of the lowland grassland group of bumblebees, estimated dates of divergence are consistent with dispersal to South America via the land-bridge corridor that opened at c. 3 Ma, followed by extant endemic lineages diverging in situ within South America. In contrast, for the second group that occupies montane grassland habitats (and for a few montane lineages of the ‘lowland’ group), we suggest that dispersal to South America at c. 3 Ma could be consistent with older divergence for currently endemic species if: (1) many of the extant South American lineages had already diverged outside the region before 3 Ma in neighbouring Mesoamerica; and (2) they had been constrained within the high mountains there, dispersing southwards into South America only once the isthmus corridor had become established; and (3) some of those ancestral montane lineages had become extirpated from Mesoamerica during subsequent warm climatic fluctuations. This interpretation re-emphasizes that biogeographic studies need to consider habitat-specific dispersal models that change through time.

When did bumblebees reach South America? Unexpectedly old montane species may be explained by Mexican stopover (Hymenoptera: Apidae)

The mountain bumblebees of the subgenus Alpigenobombus Skorikov, 1914, are uniquely distinctive because the females have enlarged mandibles with six large, evenly spaced teeth, which they use to bite holes in long-corolla flowers for nectar robbing. Recognition of species in this subgenus has been uncertain, with names used in various combinations. To revise the species, we examined COI-like barcodes for evidence of species’ gene coalescents using MrBayes and PTP and we compare the coalescent groups with morphological variation for integrative assessment. While we seek to include only orthologous barcodes (the ‘good’) and exclude all of the more strongly divergent barcode-like numts (the ‘bad’), for some nominal taxa only low-divergence numts could be obtained (the ‘ugly’). For taxa with no orthologous sequences available, using a minimum number of the lowest divergence numts did yield coalescent candidates for species that were consistent with morphologically diagnosable groups. These results agree in recognising 11 species within this subgenus, supporting: (1) recognising the widespread European Bombus mastrucatus Gerstaecker, 1869 stat. rev. as a species separate from the west Asian B. wurflenii Radoszkowski, 1860 s. str.; (2) the recently recognised B. rainai Williams, 2022, as a species separate from B. kashmirensis Friese, 1909, within the western Himalaya; (3) the recognition once again of B. sikkimi Friese, 1918 stat. rev. and B. validus Friese, 1905 stat. rev. as species separate from B. nobilis Friese, 1905 s. str. within the eastern Himalaya and Hengduan regions; (4) confirming the recognition of B. angustus Chiu, 1948, B. breviceps Smith, 1852 s. lat., B. genalis Friese, 1918, and B. grahami (Frison, 1933) as separate species within the Himalaya, China, and Southeast Asia; (5) recognising the conspecificity of the nominal taxa (not species) channicus Gribodo, 1892 (Southeast Asia) and dentatus Handlirsch, 1888 (Himalaya) as parts of the species B. breviceps s. lat. (southern and eastern China); and (6) recognising the conspecificity of the rare taxon beresovskii (Skorikov, 1933) syn. n. as part of the species B. grahami within China. Nectar robbing by bumblebees is reviewed briefly and prospects for future research discussed. 

Bumblebees with big teeth: revising the subgenus Alpigenobombus with the good, the bad and the ugly of numts (Hymenoptera: Apidae)

An important goal of evolutionary genomics is to identify genomic regions whose substitution rates differ among lineages. For example, genomic regions experiencing accelerated molecular evolution in some lineages may provide insight into links between genotype to phenotype. Several comparative genomics methods have been developed to identify genomic accelerations between species, including a Bayesian method called PhyloAcc, which models shifts in substitution rate in multiple target lineages on a phylogeny. However, few methods consider the possibility of discordance between the trees of individual loci and the species tree due to incomplete lineage sorting, which might cause false positives. Here we present PhyloAcc-GT, which extends PhyloAcc by modeling gene tree heterogeneity to detect rate shifts across genomic regions. Given a species tree, we adopt the multispecies coalescent model as the prior distribution of gene trees, use Markov chain Monte Carlo (MCMC) for inference, and design novel MCMC moves to sample gene trees efficiently. Through extensive simulations, we show that PhyloAcc-GT outperforms PhyloAcc and other methods in identifying target-lineage-specific accelerations and detecting complex patterns of rate shifts, and is robust to specification of population size parameters. We apply PhyloAcc-GT to two examples of convergent evolution: flightlessness in ratites and marine mammal adaptations. PhyloAcc-GT is usually more conservative than PhyloAcc in calling convergent rate shifts because it identifies more accelerations on ancestral than on terminal branches. In summary, PhyloAcc-GT is a useful tool to identify shifts in substitution rate associated with specific target lineages while accounting for incomplete lineage sorting.

PhyloAcc-GT: A Bayesian method for inferring patterns of substitution rate shifts and associations with binary traits under gene tree discordance

Background: Sociality has many rewards, but can also be dangerous, as high population density and low genetic
diversity, common in social insects, is ideal for parasite transmission. Despite this risk, honeybees and other
sequenced social insects have far fewer canonical immune genes relative to solitary insects. Social protection from
infection, including behavioral responses, may explain this depauperate immune repertoire. Here, based on full
genome sequences, we describe the immune repertoire of two ecologically and commercially important
bumblebee species that diverged approximately 18 million years ago, the North American Bombus impatiens and
European Bombus terrestris.
Results: We find that the immune systems of these bumblebees, two species of honeybee, and a solitary
leafcutting bee, are strikingly similar. Transcriptional assays confirm the expression of many of these genes in an
immunological context and more strongly in young queens than males, affirming Bateman’s principle of greater
investment in female immunity. We find evidence of positive selection in genes encoding antiviral responses,
components of the Toll and JAK/STAT pathways, and serine protease inhibitors in both social and solitary bees.
Finally, we detect many genes across pathways that differ in selection between bumblebees and honeybees, or
between the social and solitary clades.
Conclusions: The similarity in immune complement across a gradient of sociality suggests that a reduced immune
repertoire predates the evolution of sociality in bees. The differences in selection on immune genes likely reflect
divergent pressures exerted by parasites across social contexts

A depauperate immune repertoire precedesevolution of sociality in bees

Bumblebees (Bombus Latreille, 1802), because of their large body size, bright colours and activity at times and places that coincide with biologists, are an example of a group of insects that is particularly well represented in museum collections. This is important if taxonomic revisions are to achieve greater comparability among species. Bumblebees have also attracted particular attention because they are especially ecologically and economically valuable for pollination in north temperate regions, where they are now becoming increasingly threatened. I argue that the what, the where, and the how of effective conservation management may be informed by understanding the divergent characteristics that have affected their biogeographical past: by helping us to see ‘the woods’, not just ‘the trees’, of their habitat needs. Identifying suitable habitat should be part of reconstructing historical biogeography within taxonomic revisions. For bumblebees, for example, biogeographical analysis associates major taxonomic groups either with flower-rich lowland grasslands or with flower-rich montane grasslands, highlighting their contrasting requirements for: nest sites, flowers of different depths, pollen-plant families, and especially the differing importance of early spring and late summer flowers for breeding success. This broad view of species groups helps filter the less important idiosyncrasies from local case studies in order to focus conservation actions. 

pdf/can-biogeography-help-bumblebee-conservation-3e5rp2cr0r.pdf

Can biogeography help bumblebee conservation?

Bumblebees are a diverse group of globally important pollinators in natural ecosystems and for agricultural food production. With both eusocial and solitary lifecycle phases, and some social parasite species, they are especially interesting models to understand social evolution, behavior, and ecology. Reports of many species in decline point to pathogen transmission, habitat loss, pesticide usage, and global climate change, as interconnected causes. These threats to bumblebee diversity make our reliance on a handful of well-studied species for agricultural pollination particularly precarious. To broadly sample bumblebee genomic and phenotypic diversity, we de novo sequenced and assembled the genomes of 17 species, representing all 15 subgenera, producing the first genus-wide quantification of genetic and genomic variation potentially underlying key ecological and behavioral traits. The species phylogeny resolves subgenera relationships while incomplete lineage sorting likely drives high levels of gene tree discordance. Five chromosome-level assemblies show a stable 18-chromosome karyotype, with major rearrangements creating 25 chromosomes in social parasites. Differential transposable element activity drives changes in genome sizes, with putative domestications of repetitive sequences influencing gene coding and regulatory potential. Dynamically evolving gene families and signatures of positive selection point to genus-wide variation in processes linked to foraging, diet and metabolism, immunity and detoxification, as well as adaptations for life at high altitudes. These high-quality genomic resources capture natural genetic and phenotypic variation across bumblebees, offering new opportunities to advance our understanding of their remarkable ecological success and to identify and manage current and future threats.

https://biorxiv.org/content/10.1101/2020.05.29.122879v1.full.pdf

Genus-wide characterization of bumblebee genomes reveals variation associated with key ecological and behavioral traits of pollinators

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Genus-wide characterization of bumblebee genomes reveals variation associated with key ecological and behavioral traits of pollinators