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A combined RAD-Seq and WGS approach reveals the genomic basis of yellow color variation in bumble bee Bombus terrestris.

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 bee Bombus 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 to B. 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 factor cut. 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. Cut is 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.

SUBMITTER: Rahman SR

PROVIDER: S-EPMC8042027 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND: The impact of social parasites on their hosts' fitness is a strong selective pressure that can lead to the evolution of adapted defence strategies. Guarding the nest to prevent the intrusion of parasites is a widespread response of host species. If absolute rejection of strangers provides the best protection against parasites, more fine-tuned strategies can prove more adaptive. Guarding is indeed costly and not all strangers constitute a real threat. That is particularly true for worker reproductive parasitism in social insects since only a fraction of non-nestmate visitors, the fertile ones, can readily engage in parasitic reproduction. Guards should thus be more restrictive towards fertile than sterile non-nestmate workers. We here tested this hypothesis by examining the reaction of nest-entrance guards towards nestmate and non-nestmate workers with varying fertility levels in the bumble bee Bombus terrestris. Because social recognition in social insects mainly relies on cuticular lipids (CLs), chemical analysis was also conducted to examine whether workers' CLs could convey the relevant information upon which guards could base their decision. We thus aimed to determine whether an adapted defensive strategy to worker reproductive parasitism has evolved in B. terrestris colonies. RESULTS: Chemical analysis revealed that the cuticular chemical profiles of workers encode information about both their colony membership and their current fertility, therefore providing potential recognition cues for a suitable adjustment of the guards' defensive decisions. We found that guards were similarly tolerant towards sterile non-nestmate workers than towards nestmate workers. However, as predicted, guards responded more aggressively towards fertile non-nestmates. CONCLUSION: Our results show that B. terrestris guards discriminate non-nestmates that differ in their reproductive potential and respond more strongly to the individuals that are a greatest threat for the colony. Cuticular hydrocarbons are the probable cues underlying the specific recognition of reproductive parasites, with the specific profile of highly fertile bees eliciting the agonistic response when combined with non-colony membership information. Our study therefore provides a first piece of empirical evidence supporting the hypothesis that an adapted defensive strategy against worker reproductive parasitism exists in B. terrestris colonies.

Project description: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 for B. melanopygus from 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.

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A combined RAD-Seq and WGS approach reveals the genomic basis of yellow color variation in bumble bee Bombus terrestris.

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