skip to main content

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

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.

more » « less
Author(s) / Creator(s):
 ;  ;  ;  ;  ;  ;  ;  ;  ;  
Publisher / Repository:
Date Published:
Journal Name:
Systematic Entomology
Page Range / eLocation ID:
p. 635-652
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. 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. 
    more » « less
  2. Abstract

    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.

    more » « less
  3. Ware, Jessica (Ed.)
    Abstract Broadly distributed species experience divergent abiotic conditions across their ranges that may drive local adaptation. Montane systems where populations are distributed across both latitudinal and elevational gradients are especially likely to produce local adaptation due to spatial variation in multiple abiotic factors, including temperature, oxygen availability, and air density. We use whole-genome resequencing to evaluate the landscape genomics of Bombus vancouverensis Cresson (Hymenoptera: Apidae), a common montane bumble bee that is distributed throughout the western part of North America. Combined statistical approaches revealed several large windows of outlier SNPs with unusual levels of differentiation across the region and indicated that isothermality and elevation were the environmental features most strongly associated with these variants. Genes found within these regions had diverse biological functions, but included neuromuscular function, ion homeostasis, oxidative stress, and hypoxia that could be associated with tolerance of temperature, desiccation, or high elevation conditions. The whole-genome sequencing approach revealed outliers occurred in genome regions with elevated linkage disequilibrium, elevated mean FST, and low intrapopulation nucleotide diversity. Other kinds of structural variations were not widely associated with environmental predictors but did broadly match geographic separation. Results are consistent with other studies suggesting that regions of low recombination may harbor adaptive variation in bumble bees within as well as between species and refine our understanding of candidate genes that could be further investigated as possible targets of selection across the B. vancouverensis range. 
    more » « less
  4. Abstract

    Geographic variation in insect coloration is among the most intriguing examples of rapid phenotypic evolution and provides opportunities to study mechanisms of phenotypic change and diversification in closely related lineages. The bumble beeBombus bifariuscomprises two geographically disparate color groups characterized by red‐banded and black‐banded abdominal pigmentation, but with a range of spatially and phenotypically intermediate populations across western North America. Microsatellite analyses have revealed thatB. bifariusin the USA are structured into two major groups concordant with geography and color pattern, but also suggest ongoing gene flow among regional populations. In this study, we better resolve the relationships among major color groups to better understand evolutionary mechanisms promoting and maintaining such polymorphism. We analyze >90,000 and >25,000 single‐nucleotide polymorphisms derived from transcriptome (RNAseq) and double digest restriction site associatedDNAsequencing (ddRAD), respectively, in representative samples from spatial and color pattern extremes inB. bifariusas well as phenotypic and geographic intermediates. Both ddRADandRNAseq data illustrate substantial genome‐wide differentiation of the red‐banded (eastern) color form from both black‐banded (western) and intermediate (central) phenotypes and negligible differentiation among the latter populations, with no obvious admixture among bees from the two major lineages. Results thus indicate much stronger background differentiation amongB. bifariuslineages than expected, highlighting potential challenges for revealing loci underlying color polymorphism from population genetic data alone. These findings will have significance for resolving taxonomic confusion in this species and in future efforts to investigate color‐pattern evolution inB. bifariusand other polymorphic bumble bee species.

    more » « less
  5. Abstract

    As hybrid zones exhibit selective patterns of gene flow between otherwise distinct lineages, they can be especially valuable for informing processes of microevolution and speciation. The bumble bee,Bombus melanopygus, displays two distinct color forms generated by Müllerian mimicry: a northern “Rocky Mountain'’ color form with ferruginous mid‐abdominal segments (B.m.melanopygus) and a southern “Pacific'’ form with black mid‐abdominal segments (B.m.edwardsii). These morphs meet in a mimetic transition zone in northern California and southern Oregon that is more narrow and transitions further west than comimetic bumble bee species. To understand the historical formation of this mimicry zone, we assessed color distribution data forB.melanopygusfrom the last 100 years. We then examined gene flow among the color forms in the transition zone by comparing sequences from mitochondrial COI barcode sequences, color‐controlling loci, and the rest of the nuclear genome. These data support two geographically distinct mitochondrial haplogroups aligned to the ancestrally ferruginous and black forms that meet within the color transition zone. This clustering is also supported by the nuclear genome, which, while showing strong admixture across individuals, distinguishes individuals most by their mitochondrial haplotype, followed by geography. These data suggest the two lineages most likely were historically isolated, acquired fixed color differences, and then came into secondary contact with ongoing gene flow. The transition zone, however, exhibits asymmetries: mitochondrial haplotypes transition further south than color pattern, and both transition over shorter distances in the south. This system thus demonstrates alternative patterns of gene flow that occur in contact zones, presenting another example of mito‐nuclear discordance. Discordant gene flow is inferred to most likely be driven by a combination of mimetic selection, dominance effects, and assortative mating.

    more » « less