Ontogenetic stage‐specific quantitative trait loci contribute to divergence in developmental trajectories of sexually dimorphic fins between medaka populations

Kawajiri, Maiko; Yoshida, Kohta; Fujimoto, Shingo; Mokodongan, Daniel F.; Ravinet, Mark; Kirkpatrick, Mark; Yamahira, Kazunori; Kitano, Jun

doi:10.1111/mec.12933

Cited by 22 publications

(34 citation statements)

References 81 publications

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“…This shift may be a result of steroid‐dependent gene regulation because the hormonal changes associated with sexual maturation provide a mechanism that could have been co‐opted to change the expression of a specific toxin locus (Kawajiri et al . ), and the shift in phenotype appears to be discrete rather than gradual (Jensen et al . ).…”

Section: Resultsmentioning

confidence: 99%

Phenotypic integration in the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus)

et al. 2015

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Selection can vary geographically across environments and temporally over the lifetime of an individual. Unlike geographic contexts, where different selective regimes can act on different alleles, age-specific selection is constrained to act on the same genome by altering age-specific expression. Snake venoms are exceptional traits for studying ontogeny because toxin expression variation directly changes the phenotype; relative amounts of venom components determine, in part, venom efficacy. Phenotypic integration is the dependent relationship between different traits that collectively produce a complex phenotype and, in venomous snakes, may include traits as diverse as venom, head shape and fang length. We examined the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus) across environments and over the lifetime of individuals and used a genotype-phenotype map approach, protein expression data and morphological data to demonstrate that: (i) ontogenetic effects explained more of the variation in toxin expression variation than geographic effects, (ii) both juveniles and adults varied geographically, (iii) toxin expression variation was a result of directional selection and (iv) different venom phenotypes covaried with morphological traits also associated with feeding in temporal (ontogenetic) and geographic (functional) contexts. These data are the first to demonstrate, to our knowledge, phenotypic integration between multiple morphological characters and a biochemical phenotype across populations and age classes. We identified copy number variation as the mechanism driving the difference in the venom phenotype associated with these morphological differences, and the parallel mitochondrial, venom and morphological divergence between northern and southern clades suggests that each clade may warrant classification as a separate evolutionarily significant unit.

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Section: Resultsmentioning

confidence: 99%

Phenotypic integration in the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus)

et al. 2015

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“…; Kawajiri et al . ). The genomewide thresholds of significance of logarithm of the odds ratio (LOD) scores ( P < 0.05) were determined with 1000 bootstrap permutations (genomewide significance threshold of LOD = 3.46).…”

Section: Methodsmentioning

confidence: 97%

“…Reads were trimmed and mapped to the repeat‐masked reference stickleback genome (BROAD S1) using the clc genomic workbench 5.1 with the previously used parameters (Kawajiri et al . , ; Yoshida et al . ) except that the paired‐end distance was set to 10–1000 bp, minimum variant frequency = 0 and required variant count threshold = 3.…”

Section: Methodsmentioning

confidence: 99%

“…All sequence reads are available from DDBJ (DRA004936). Reads were trimmed and mapped to the repeat-masked reference stickleback genome (BROAD S1) using the CLC GENOMIC WORKBENCH 5.1 with the previously used parameters (Kawajiri et al 2014(Kawajiri et al , 2015Yoshida et al 2014) except that the paired-end distance was set to 10-1000 bp, minimum variant frequency = 0 and required variant count threshold = 3. We then selected SNPs that met the following three criteria: (i) 50-bp flanking regions on both sides of the SNP were conserved between populations, (ii) the Illumina designability rank score was 1, (iii) the SNP was located within coding regions if available.…”

Section: Qtl Mappingmentioning

confidence: 99%

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Genetic basis for variation in salinity tolerance between stickleback ecotypes

et al. 2016

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Adaptation to different salinities can drive and maintain divergence between populations of aquatic organisms. Anadromous and stream ecotypes of threespine stickleback (Gasterosteus aculeatus) are an excellent model to explore the genetic mechanisms underlying osmoregulation divergence. Using a parapatric pair of anadromous and stream stickleback ecotypes, we employed an integrated genomic approach to identify candidate genes important for adaptation to different salinity environments. Quantitative trait loci (QTL) mapping of plasma sodium concentrations under a seawater challenge experiment identified a significant QTL on chromosome 16. To identify candidate genes within this QTL, we first conducted RNA-seq and microarray analysis on gill tissue to find ecotypic differences in gene expression that were associated with plasma Na levels. This resulted in the identification of ten candidate genes. Quantitative PCR analysis on gill tissue of additional Japanese stickleback populations revealed that the majority of the candidate genes showed parallel divergence in expression levels. Second, we conducted whole-genome sequencing and found five genes that are predicted to have functionally important amino acid substitutions. Finally, we conducted genome scan analysis and found that eight of these candidate genes were located in genomic islands of high differentiation, suggesting that they may be under divergent selection. The candidate genes included those involved in ATP synthesis and hormonal signalling, whose expression or amino acid changes may underlie the variation in salinity tolerance. Further functional molecular analysis of these genes will reveal the causative genetic and genomic changes underlying divergent adaptation.

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“…A). QTL and GWAS techniques have also identified seemingly modular age‐specific allelic effects in a wide range of organisms . These studies have all reported that the polymorphisms contributing to trait variation are different at different ages.…”

Section: Genetic Modularity Of Life Histories: the Case For Evolutionmentioning

confidence: 99%

Pleiotropy, constraint, and modularity in the evolution of life histories: insights from genomic analyses

Hughes

Leips

2016

Annals of the New York Academy of Sciences

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Multicellular organisms display an enormous range of life history strategies and present an evolutionary conundrum; despite strong natural selection, life history traits are characterized by high levels of genetic variation. To understand the evolution of life histories and the maintenance of this variation, the specific phenotypic effects of segregating alleles and the genetic networks in which they act need to be elucidated. In particular, the extent to which life history evolution is constrained by the pleiotropy of alleles contributing to life history variation is generally unknown. Here we review recent empirical results that shed light on this question, with an emphasis on studies employing genomic analyses. While genome-scale analyses are increasingly practical and affordable, they face limitations of genetic resolution and statistical power. We describe new research approaches that we believe can produce new insights and evaluate their promise and applicability to different kinds of organisms. Two approaches seem particularly promising: experiments that manipulate selection in multiple dimensions and measure phenotypic and genomic response, and analytical approaches that take into account genome-wide associations between markers and phenotypes, rather than applying a traditional marker-by-marker approach.

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Ontogenetic stage‐specific quantitative trait loci contribute to divergence in developmental trajectories of sexually dimorphic fins between medaka populations

Cited by 22 publications

References 81 publications

Phenotypic integration in the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus)

Phenotypic integration in the feeding system of the eastern diamondback rattlesnake (Crotalus adamanteus)

Genetic basis for variation in salinity tolerance between stickleback ecotypes

Pleiotropy, constraint, and modularity in the evolution of life histories: insights from genomic analyses

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