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Characterizing molecular underpinnings of plastic traits and balanced polymorphisms represent two important goals of evolutionary biology. Fire ant gynes (pre-reproductive queens) provide an ideal system to study potential links between these phenomena because they exhibit both supergene-mediated polymorphism and nutritional plasticity in weight and colony-founding behavior. Gynes with the inversion supergene haplotype are lightweight and depend on existing workers to initiate reproduction. Gynes with only the ancestral, non-inverted gene arrangement accumulate more nutrient reserves as adults and, in a distinct colony-founding behavior, initiate reproduction without help from workers. However, when such gynes overwinter in the natal nest they develop an environmentally induced lightweight phenotype and colony-founding behavior, similar to gynes with the inversion haplotype that have not overwintered. To evaluate the extent of shared mechanisms between plasticity and balanced polymorphism in fire ant gyne traits, we assessed whether genes with expression variation linked to overwintering plasticity may be affected by evolutionary divergence between supergene haplotypes. To do so, we first compared transcriptional profiles of brains and ovaries from overwintered and non-overwintered gynes to identify plasticity-associated genes. These genes were enriched for metabolic and behavioral functions. Next, we compared plasticity-associated genes to those differentially expressed by supergene genotype, revealing a significant overlap of the two sets in ovarian tissues. We also identified sequence substitutions between supergene variants of multiple plasticity-associated genes, consistent with a scenario in which an ancestrally plastic phenotype responsive to an environmental condition became increasingly genetically regulated.
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Incomplete recombination suppression fuels extensive haplotype diversity in a butterfly colour pattern supergene
Supergenes can evolve when recombination-suppressing mechanisms like inversions promote co-inheritance of alleles at two or more polymorphic loci that affect a complex trait. Theory shows that such genetic architectures can be favoured under balancing selection or local adaptation in the face of gene flow, but they can also bring costs associated with reduced opportunities for recombination. These costs may in turn be offset by rare ‘gene flux’ between inverted and ancestral haplotypes, with a range of possible outcomes. We aimed to shed light on these processes by investigating the ‘BC supergene’, a large genomic region comprising multiple rearrangements associated with three distinct wing colour morphs inDanaus chrysippus, a butterfly known as the African monarch, African queen and plain tiger. Using whole-genome resequencing data from 174 individuals, we first confirm the effects of BC on wing colour pattern: background melanism is associated with SNPs in the promoter region ofyellow, within an inverted subregion of the supergene, while forewing tip pattern is most likely associated with copy-number variation in a separate subregion of the supergene. We then show that haplotype diversity within the supergene is surprisingly extensive: there are at least six divergent haplotype groups that experience suppressed recombination with respect to each other. Despite high divergence between these haplotype groups, we identify an unexpectedly large number of natural recombinant haplotypes. Several of the inferred crossovers occurred between adjacent inversion ‘modules’, while others occurred within inversions. Furthermore, we show that new haplotype groups have arisen through recombination between two pre-existing ones. Specifically, an allele for dark colouration in the promoter ofyellowhas recombined into distinct haplotype backgrounds on at least two separate occasions. Overall, our findings paint a picture of dynamic evolution of supergene haplotypes, fuelled by incomplete recombination suppression.
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- Award ID(s):
- 2311366
- PAR ID:
- 10655954
- Editor(s):
- Khila, Abderrahman
- Publisher / Repository:
- PLOS
- Date Published:
- Journal Name:
- PLOS Biology
- Volume:
- 23
- Issue:
- 2
- ISSN:
- 1545-7885
- Page Range / eLocation ID:
- e3003043
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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- Free Publicly Accessible Full Text
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Accepted Manuscript
- Journal Article:
- https://doi.org/10.1371/journal.pbio.3003043
