skip to main content

Title: Mito‐nuclear discordance at a mimicry color transition zone in bumble bee Bombus melanopygus

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
Author(s) / Creator(s):
 ;  ;  ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
Ecology and Evolution
Medium: X Size: p. 18151-18168
["p. 18151-18168"]
Sponsoring Org:
National Science Foundation
More Like this
  1. 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
  2. Abstract

    Bumble bees exhibit exceptional diversity in their segmental body coloration largely as a result of mimicry. In this study we sought to discover genes involved in this variation through studying a lab-generated mutant in bumble beeBombus terrestris,in which the typical black coloration of the pleuron, scutellum, and first metasomal tergite is replaced by yellow, a color variant also found in sister lineages toB. terrestris. Utilizing a combination of RAD-Seq and whole-genome re-sequencing, we localized the color-generating variant to a single SNP in the protein-coding sequence of transcription factorcut. This mutation generates an amino acid change that modifies the conformation of a coiled-coil structure outside DNA-binding domains. We found that all sequenced Hymenoptera, including sister lineages, possess the non-mutant allele, indicating different mechanisms are involved in the same color transition in nature.Cutis important for multiple facets of development, yet this mutation generated no noticeable external phenotypic effects outside of setal characteristics. Reproductive capacity was reduced, however, as queens were less likely to mate and produce female offspring, exhibiting behavior similar to that of workers. Our research implicates a novel developmental player in pigmentation, and potentially caste, thus contributing to a better understanding of the evolution of diversity in both of these processes.

    more » « less
  3. Abstract

    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
  4. Abstract

    Hybrid zones can be studied by modeling clines of trait variation (e.g., morphology, genetics) over a linear transect. Yet, hybrid zones can also be spatially complex, can shift over time, and can even lead to the formation of hybrid lineages with the right combination of dispersal and vicariance. We reassessed Sibley’s (1950) gradient between Collared Towhee (Pipilo ocai) and Spotted Towhee (Pipilo maculatus) in Central Mexico to test whether it conformed to a typical tension-zone cline model. By comparing historical and modern data, we found that cline centers for genetic and phenotypic traits have not shifted over the course of 70 years. This equilibrium suggests that secondary contact between these species, which originally diverged over 2 million years ago, likely dates to the Pleistocene. Given the amount of mtDNA divergence, parental ends of the cline have very low autosomal nuclear differentiation (FST = 0.12). Dramatic and coincident cline shifts in mtDNA and throat color suggest the possibility of sexual selection as a factor in differential introgression, while a contrasting cline shift in green back color hints at a role for natural selection. Supporting the idea of a continuum between clinal variation and hybrid lineage formation, the towhee gradient can be analyzed as one population under isolation-by-distance, as a two-population cline, and as three lineages experiencing divergence with gene flow. In the middle of the gradient, a hybrid lineage has become partly isolated, likely due to forested habitat shrinking and fragmenting as it moved upslope after the last glacial maximum and a stark environmental transition. This towhee system offers a window into the potential outcomes of hybridization across a dynamic landscape including the creation of novel genomic and phenotypic combinations and incipient hybrid lineages.

    more » « less
  5. Abstract

    The arrival to theUnitedStates of theAfricanized honey bee, a hybrid betweenEuropean subspecies and theAfrican subspeciesApis mellifera scutellata, is a remarkable model for the study of biological invasions. This immigration has created an opportunity to study the dynamics of secondary contact of honey bee subspecies fromAfrican andEuropean lineages in a feral population inSouthTexas. An 11‐year survey of this population (1991–2001) showed that mitochondrial haplotype frequencies changed drastically over time from a resident population of eastern and western European maternal ancestry, to a population dominated by theAfrican haplotype. A subsequent study of the nuclear genome showed that theAfricanization process included bidirectional gene flow between European and Africanized honey bees, giving rise to a new panmictic mixture ofA. m. scutellata‐and European‐derived genes. In this study, we examined gene flow patterns in the same population 23 years after the first hybridization event occurred. We found 28 active colonies inhabiting 92 tree cavities surveyed in a 5.14 km2area, resulting in a colony density of 5.4 colonies/km2. Of these 28 colonies, 25 were ofA. m. scutellatamaternal ancestry, and three were of western European maternal ancestry. No colonies of eastern European maternal ancestry were detected, although they were present in the earlier samples. NuclearDNArevealed little change in the introgression ofA. m. scutellata‐derived genes into the population compared to previous surveys. Our results suggest this feral population remains an admixed swarm with continued low levels of European ancestry and a greater presence of African‐derived mitochondrial genetic composition.

    more » « less