A supergene determines highly divergent male reproductive morphs in the ruff

Küpper, Clemens; Stocks, Michael; Risse, Judith; Remedios, Natalie dos; Farrell, Lindsay; McRae, Susan B.; Morgan, Tawna C.; Karlionova, Natalia; Pinchuk, Pavel; Verkuil, Yvonne I.; Kitaysky, Alexander S.; Wingfield, John C.; Piersma, Theunis; Zeng, Kai; Slate, Jon; Blaxter, Mark; Lank, David B.; Burke, Terry

doi:10.1038/ng.3443

Cited by 476 publications

(584 citation statements)

References 69 publications

Supporting

Mentioning

556

Contrasting

Unclassified

Order By: Relevance

“…Mimicry polymorphism in H. numata is controlled by a supergene characterized by distinct chromosomal inversions maintaining the different haplotypes underlying the various wing patterns (14). As documented in an increasing number of cases, inversions may be associated with deleterious effects, either through the disruption of gene regulation by the breakpoints or due to deleterious mutations present within the segment at the time of the inversion, causing reduced fitness in homozygotes (27,(38)(39)(40). By minimizing the frequency of homozygotes for the inversion in offspring, disassortative mating protects from the deleterious effects associated with the inversions.…”

Section: Resultsmentioning

confidence: 99%

Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures

Chouteau

Llaurens

Piron‐Prunier

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

105

View full text Add to dashboard Cite

Explaining the maintenance of adaptive diversity within populations is a long-standing goal in evolutionary biology, with important implications for conservation, medicine, and agriculture. Adaptation often leads to the fixation of beneficial alleles, and therefore it erodes local diversity so that understanding the coexistence of multiple adaptive phenotypes requires deciphering the ecological mechanisms that determine their respective benefits. Here, we show how antagonistic frequency-dependent selection (FDS), generated by natural and sexual selection acting on the same trait, maintains mimicry polymorphism in the toxic butterfly Heliconius numata. Positive FDS imposed by predators on mimetic signals favors the fixation of the most abundant and best-protected wing-pattern morph, thereby limiting polymorphism. However, by using mate-choice experiments, we reveal disassortative mate preferences of the different wing-pattern morphs. The resulting negative FDS on wing-pattern alleles is consistent with the excess of heterozygote genotypes at the supergene locus controlling wing-pattern variation in natural populations of H. numata. The combined effect of positive and negative FDS on visual signals is sufficient to maintain a diversity of morphs displaying accurate mimicry with other local prey, although some of the forms only provide moderate protection against predators. Our findings help understand how alternative adaptive phenotypes can be maintained within populations and emphasize the need to investigate interactions between selective pressures in other cases of puzzling adaptive polymorphism.disassortative mating | selection conflicts | Müllerian mimicry | aposematism | warning signals

show abstract

Section: Resultsmentioning

confidence: 99%

Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures

Chouteau

Llaurens

Piron‐Prunier

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

105

View full text Add to dashboard Cite

show abstract

“…many QTL of small effect) [48]. Recent empirical studies demonstrate that even seemingly complex phenotypes can be controlled by concentrated architecture [49,50]. Life-history strategies for migration timing in salmonids appear to be less extreme than these examples of traits with concentrated genetic architecture, because many loci of both large and small effects have been implicated across chromosomes [35,51].…”

Section: Discussionmentioning

confidence: 99%

Genetic basis of adult migration timing in anadromous steelhead discovered through multivariate association testing

et al. 2016

View full text Add to dashboard Cite

Migration traits are presumed to be complex and to involve interaction among multiple genes. We used both univariate analyses and a multivariate random forest (RF) machine learning algorithm to conduct association mapping of 15 239 single nucleotide polymorphisms (SNPs) for adult migration-timing phenotype in steelhead (Oncorhynchus mykiss). Our study focused on a model natural population of steelhead that exhibits two distinct migration-timing life histories with high levels of admixture in nature. Neutral divergence was limited between fish exhibiting summer-and winter-run migration owing to high levels of interbreeding, but a univariate mixed linear model found three SNPs from a major effect gene to be significantly associated with migration timing ( p , 0.000005) that explained 46% of trait variation. Alignment to the annotated Salmo salar genome provided evidence that all three SNPs localize within a 46 kb region overlapping GREB1-like (an oestrogen target gene) on chromosome Ssa03. Additionally, multivariate analyses with RF identified that these three SNPs plus 15 additional SNPs explained up to 60% of trait variation. These candidate SNPs may provide the ability to predict adult migration timing of steelhead to facilitate conservation management of this species, and this study demonstrates the benefit of multivariate analyses for association studies.

show abstract

“…This has stimulated ongoing research into the underlying mechanisms at the level of the genome (e.g., Küpper et al. 2016; Lamichhaney et al. 2016).…”

Section: Introductionmentioning

confidence: 99%

Born blonde: a recessive loss‐of‐function mutation in the melanocortin 1 receptor is associated with cream coat coloration inAntarctic fur seals

Peters

Humble

Kröcker

et al. 2016

Ecology and Evolution

View full text Add to dashboard Cite

Although the genetic basis of color variation has been extensively studied in humans and domestic animals, the genetic polymorphisms responsible for different color morphs remain to be elucidated in many wild vertebrate species. For example, hypopigmentation has been observed in numerous marine mammal species but the underlying mutations have not been identified. A particularly compelling candidate gene for explaining color polymorphism is the melanocortin 1 receptor (MC1R), which plays a key role in the regulation of pigment production. We therefore used Antarctic fur seals (Arctocephalus gazella) as a highly tractable marine mammal system with which to test for an association between nucleotide variation at the MC1R and melanin‐based coat color phenotypes. By sequencing 70 wild‐type individuals with dark‐colored coats and 26 hypopigmented individuals with cream‐colored coats, we identified a nonsynonymous mutation that results in the substitution of serine with phenylalanine at an evolutionarily highly conserved structural domain. All of the hypopigmented individuals were homozygous for the allele coding for phenylalanine, consistent with a recessive loss‐of‐function allele. In order to test for cryptic population structure, which can generate artefactual associations, and to evaluate whether homozygosity at the MC1R could be indicative of low genome‐wide heterozygosity, we also genotyped all of the individuals at 50 polymorphic microsatellite loci. We were unable to detect any population structure and also found that wild‐type and hypopigmented individuals did not differ significantly in their standardized multilocus heterozygosity. Such a lack of association implies that hypopigmented individuals are unlikely to suffer disproportionately from inbreeding depression, and hence, we have no reason to believe that they are at a selective disadvantage in the wider population.

show abstract

A supergene determines highly divergent male reproductive morphs in the ruff

Cited by 476 publications

References 69 publications

Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures

Polymorphism at a mimicry supergene maintained by opposing frequency-dependent selection pressures

Genetic basis of adult migration timing in anadromous steelhead discovered through multivariate association testing

Born blonde: a recessive loss‐of‐function mutation in the melanocortin 1 receptor is associated with cream coat coloration inAntarctic fur seals

Contact Info

Product

Resources

About