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1. Local adaptation across a complex bioclimatic landscape in two montane bumble bee species

   https://doi.org/10.1111/mec.15376  

   Jackson, Jason M. ; Pimsler, Meaghan L. ; Oyen, Kennan J. ; Strange, James P. ; Dillon, Michael E. ; Lozier, Jeffrey D. ( February 2020 , Molecular Ecology)

   Understanding evolutionary responses to variation in temperature and precipitation across species ranges is of fundamental interest given ongoing climate change. The importance of temperature and precipitation for multiple aspects of bumble bee (Bombus) biology, combined with large geographic ranges that expose populations to diverse environmental pressures, make these insects well‐suited for studying local adaptation. Here, we analyzed genome‐wide sequence data from two widespread bumble bees,Bombus vosnesenskiiandBombus vancouverensis, using multiple environmental association analysis methods to investigate climate adaptation across latitude and altitude. The strongest signatures of selection were observed inB. vancouverensis, but despite unique responses between species for most loci, we detected several shared responses. Genes relating to neural and neuromuscular function and ion transport were especially evident with respect to temperature variables, while genes relating to cuticle formation, tracheal and respiratory system development, and homeostasis were associated with precipitation variables. Our data thus suggest that adaptive responses for tolerating abiotic variation are likely to be complex, but that several parallels among species can emerge even for these complex traits and landscapes. Results provide the framework for future work into mechanisms of thermal and desiccation tolerance in bumble bees and a set of genomic targets that might be monitored for future conservation efforts.

    

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2. Divergence in Body Mass, Wing Loading, and Population Structure Reveals Species-Specific and Potentially Adaptive Trait Variation Across Elevations in Montane Bumble Bees

   https://doi.org/10.1093/isd/ixab012  

   Lozier, Jeffrey D ; Parsons, Zachary M ; Rachoki, Lois ; Jackson, Jason M ; Pimsler, Meaghan L ; Oyen, Kennan J ; Strange, James ; Dillon, Michael E ( September 2021 , Insect Systematics and Diversity)

   Hines, Heather (Ed.)

   Abstract Biogeographic clines in morphology along environmental gradients can illuminate forces influencing trait evolution within and between species. Latitude has long been studied as a driver of morphological clines, with a focus on body size and temperature. However, counteracting environmental pressures may impose constraints on body size. In montane landscapes, declines in air density with elevation can negatively impact flight performance in volant species, which may contribute to selection for reduced body mass despite declining temperatures. We examine morphology in two bumble bee (Hymenoptera: Apidae: Bombus Latreille) species, Bombus vancouverensis Cresson and Bombus vosnesenskii Radoszkowski, across mountainous regions of California, Oregon, and Washington, United States. We incorporate population genomic data to investigate the relationship between genomic ancestry and morphological divergence. We find that B. vancouverensis, which tends to be more specialized for high elevations, exhibits stronger spatial-environmental variation, being smaller in the southern and higher elevation parts of its range and having reduced wing loading (mass relative to wing area) at high elevations. Bombus vosnesenskii, which is more of an elevational generalist, has substantial trait variation, but spatial-environmental correlations are weak. Population structure is stronger in the smaller B. vancouverensis, and we find a significant association between elevation and wing loading after accounting for genetic structure, suggesting the possibility of local adaptation for this flight performance trait. Our findings suggest that some conflicting results for body size trends may stem from distinct environmental pressures that impact different aspects of bumble bee ecology, and that different species show different morphological clines in the same region. 

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3. Whole genome analyses reveal weak signatures of population structure and environmentally associated local adaptation in an important North American pollinator, the bumble bee Bombus vosnesenskii

   https://doi.org/10.1111/mec.17125  

   Heraghty, Sam D. ; Jackson, Jason M. ; Lozier, Jeffrey D. ( September 2023 , Molecular Ecology)

   Studies of species that experience environmental heterogeneity across their distributions have become an important tool for understanding mechanisms of adaptation and predicting responses to climate change. We examine population structure, demographic history and environmentally associated genomic variation inBombus vosnesenskii, a common bumble bee in the western USA, using whole genome resequencing of populations distributed across a broad range of latitudes and elevations. We find thatB. vosnesenskiiexhibits minimal population structure and weak isolation by distance, confirming results from previous studies using other molecular marker types. Similarly, demographic analyses with Sequentially Markovian Coalescent models suggest that minimal population structure may have persisted since the last interglacial period, with genomes from different parts of the species range showing similar historical effective population size trajectories and relatively small fluctuations through time. Redundancy analysis revealed a small amount of genomic variation explained by bioclimatic variables. Environmental association analysis with latent factor mixed modelling (LFMM2) identified few outlier loci that were sparsely distributed throughout the genome and although a few putative signatures of selective sweeps were identified, none encompassed particularly large numbers of loci. Some outlier loci were in genes with known regulatory relationships, suggesting the possibility of weak selection, although compared with other species examined with similar approaches, evidence for extensive local adaptation signatures in the genome was relatively weak. Overall, results indicateB. vosnesenskiiis an example of a generalist with a high degree of flexibility in its environmental requirements that may ultimately benefit the species under periods of climate change.

    

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4. Substantial genetic divergence and lack of recent gene flow support cryptic speciation in a colour polymorphic bumble bee ( Bombus bifarius ) species complex

   https://doi.org/10.1111/syen.12419  

   Ghisbain, Guillaume ; Lozier, Jeffrey D. ; Rahman, Sarthok Rasique ; Ezray, Briana D. ; Tian, Li ; Ulmer, Jonah M. ; Heraghty, Sam D. ; Strange, James P. ; Rasmont, Pierre ; Hines, Heather M. ( January 2020 , Systematic Entomology)

   Phenotypic polymorphism can constitute an inherent challenge for species delimitation. This issue is exemplified in bumble bees (Bombus), where species can exhibit high colour variation across their range, but otherwise exhibit little morphological variation to distinguish them from close relatives. We examine the species status of one of the most abundant North American bumble bees,Bombus bifariusCresson, which historically comprised two major taxa,bifariuss.s. andnearcticus. These lineages are recognized primarily by red and black variation in their mid‐abdominal coloration; however, a continuum from black (nearcticus) to red (bifariuss.s.) variation has led to their historic synonymization. Integrating mitochondrial and nuclear data and whole‐genome sequencing, we reveal a high level of both mitochondrial and nuclear divergence delimiting two morphologically cryptic species – the redbifariuss.s. and the colour‐variable (black to red)nearcticus. Population genomic analysis supports an absence of recent genomic admixture and a strong population structure between the two clades, even in sympatry. Species distribution models predict partially differentiated niches between the genetically inferred clades with annual precipitation being a leading differentiating variable. Thebifariuss.s. lineage also occupies significantly higher elevations, with regions of sympatry being among the highest elevations innearcticus. Our data also support a subspecies‐level divergence between the broadly distributednearcticusand the island populationvancouverensis. In this paper, we formally recognize the two species,Bombus bifariusCresson andBombus vancouverensisCresson, the latter including the subspeciesB. vancouverensis vancouverensiscomb.n.andB. vancouverensis nearcticuscomb.n., withvancouverensisthe name bearer due to year priority.

    

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5. Whole genome resequencing identifies local adaptation associated with environmental variation for redband trout

   https://doi.org/10.1111/mec.16810  

   Andrews, Kimberly R. ; Seaborn, Travis ; Egan, Joshua P. ; Fagnan, Matthew W. ; New, Daniel D. ; Chen, Zhongqi ; Hohenlohe, Paul A. ; Waits, Lisette P. ; Caudill, Christopher C. ; Narum, Shawn R. ( December 2022 , Molecular Ecology)

   Aquatic ectotherms are predicted to harbour genomic signals of local adaptation resulting from selective pressures driven by the strong influence of climate conditions on body temperature. We investigated local adaptation in redband trout (Oncorhynchus mykiss gairdneri) using genome scans for 547 samples from 11 populations across a wide range of habitats and thermal gradients in the interior Columbia River. We estimated allele frequencies for millions of single nucleotide polymorphism loci (SNPs) across populations using low‐coverage whole genome resequencing, and used population structure outlier analyses to identify genomic regions under divergent selection between populations. Twelve genomic regions showed signatures of local adaptation, including two regions associated with genes known to influence migration and developmental timing in salmonids (GREB1L,ROCK1,SIX6). Genotype–environment association analyses indicated that diurnal temperature variation was a strong driver of local adaptation, with signatures of selection driven primarily by divergence of two populations in the northern extreme of the subspecies range. We also found evidence for adaptive differences between high‐elevation desert vs. montane habitats at a smaller geographical scale. Finally, we estimated vulnerability of redband trout to future climate change using ecological niche modelling and genetic offset analyses under two climate change scenarios. These analyses predicted substantial habitat loss and strong genetic shifts necessary for adaptation to future habitats, with the greatest vulnerability predicted for high‐elevation desert populations. Our results provide new insight into the complexity of local adaptation in salmonids, and important predictions regarding future responses of redband trout to climate change.

    

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