Partially repeatable genetic basis of benthic adaptation in threespine sticklebacks

Erickson, Priscilla A.; Glazer, Andrew M.; Killingbeck, Emily; Agoglia, Rachel M.; Baek, Jiyeon; Carsanaro, Sara M.; Lee, Anthony M.; Cleves, Phillip A.; Schluter, Dolph; Miller, Craig T.

doi:10.1111/evo.12897

Cited by 39 publications

(55 citation statements)

References 88 publications

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“…In a model that somewhat reconciled the theoretical debate, Orr [56] predicted that a few mutations of large effect and many of smaller effect would contribute to the process of adaptation. Previous analyses of the distribution of effect sizes of QTL identified for body shape and skeletal traits in stickleback provide qualitative support for Orr's model [29,33,42,47]. With data on the per cent variance explained (PVE) for 1034 QTL from the 28 published QTL studies in threespine stickleback, we now have a larger sample size to examine this distribution (figure 2).…”

Section: Identification Of Quantitative Trait Loci Revealsmentioning

confidence: 74%

The genetic and molecular architecture of phenotypic diversity in sticklebacks

Peichel

Marques

2017

Phil. Trans. R. Soc. B

169

201

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One contribution of 17 to a theme issue 'Evodevo in the genomics era, and the origins of morphological diversity'. A major goal of evolutionary biology is to identify the genotypes and phenotypes that underlie adaptation to divergent environments. Stickleback fish, including the threespine stickleback (Gasterosteus aculeatus) and the ninespine stickleback (Pungitius pungitius), have been at the forefront of research to uncover the genetic and molecular architecture that underlies phenotypic diversity and adaptation. A wealth of quantitative trait locus (QTL) mapping studies in sticklebacks have provided insight into longstanding questions about the distribution of effect sizes during adaptation as well as the role of genetic linkage in facilitating adaptation. These QTL mapping studies have also provided a basis for the identification of the genes that underlie phenotypic diversity. These data have revealed that mutations in regulatory elements play an important role in the evolution of phenotypic diversity in sticklebacks. Genetic and molecular studies in sticklebacks have also led to new insights on the genetic basis of repeated evolution and suggest that the same loci are involved about half of the time when the same phenotypes evolve independently. When the same locus is involved, selection on standing variation and repeated mutation of the same genes have both contributed to the evolution of similar phenotypes in independent populations. This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

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Section: Identification Of Quantitative Trait Loci Revealsmentioning

confidence: 74%

The genetic and molecular architecture of phenotypic diversity in sticklebacks

Peichel

Marques

2017

Phil. Trans. R. Soc. B

169

201

View full text Add to dashboard Cite

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“…Nevertheless, several studies indicate that adaptation to novel aquatic environments may also involve parts of the genome outside these large target regions (DeFaveri et al 2011; Leinonen et al 2012; Ellis et al 2015; Erickson et al 2016; Ferchaud and Hansen 2016). The QTL underlying physiological adaptations to different aquatic environments in sticklebacks have not been well characterized.…”

Section: Discussionmentioning

confidence: 99%

Regulatory Architecture of Gene Expression Variation in the Threespine Stickleback Gasterosteus aculeatus

Pritchard

Viitaniemi

McCairns

et al. 2017

G3 Genes|Genomes|Genetics

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Much adaptive evolutionary change is underlain by mutational variation in regions of the genome that regulate gene expression rather than in the coding regions of the genes themselves. An understanding of the role of gene expression variation in facilitating local adaptation will be aided by an understanding of underlying regulatory networks. Here, we characterize the genetic architecture of gene expression variation in the threespine stickleback (Gasterosteus aculeatus), an important model in the study of adaptive evolution. We collected transcriptomic and genomic data from 60 half-sib families using an expression microarray and genotyping-by-sequencing, and located expression quantitative trait loci (eQTL) underlying the variation in gene expression in liver tissue using an interval mapping approach. We identified eQTL for several thousand expression traits. Expression was influenced by polymorphism in both cis- and trans-regulatory regions. Trans-eQTL clustered into hotspots. We did not identify master transcriptional regulators in hotspot locations: rather, the presence of hotspots may be driven by complex interactions between multiple transcription factors. One observed hotspot colocated with a QTL recently found to underlie salinity tolerance in the threespine stickleback. However, most other observed hotspots did not colocate with regions of the genome known to be involved in adaptive divergence between marine and freshwater habitats.

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“…We overlaid positional information for genomic islands with those of Ensembl predicted genes (Jones et al 2012b) and with previously identified quantitative trait loci (QTL), candidate genes, expression outliers and outlier regions (Peichel et al 2001;Colosimo et al 2004Colosimo et al , 2005Cresko et al 2004;Shapiro et al 2004;Kimmel et al 2005;Coyle et al 2007;Miller et al 2007Miller et al , 2014Albert et al 2008;Makinen et al 2008a,b;Chan et al 2009Chan et al , 2010Kitano et al 2009Kitano et al , 2010Kitano et al , 2013Hohenlohe et al 2010;DeFaveri et al 2011;Greenwood et al 2011Greenwood et al , 2012Greenwood et al , 2013Greenwood et al , 2015Shimada et al 2011;Deagle et al 2012;Jones et al 2012a,b;Kaeuffer et al 2012;Malek et al 2012;Rogers et al 2012;Wark et al 2012;Arnegard et al 2014;Berner et al 2014;Cleves et al 2014;Erickson et al 2014Erickson et al , 2015Erickson et al , 2016Glazer et al 2014Glazer et al , 2015Liu et al 2014;Terekhanova et al 2014;…”

Section: Population Genomic Analysesmentioning

confidence: 99%

Genomic landscape of early ecological speciation initiated by selection on nuptial colour

et al. 2016

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Ecological speciation is the evolution of reproductive isolation as a consequence of direct divergent natural selection or ecologically mediated divergent sexual selection. While the genomic signature of the former has been extensively studied in recent years, only few examples exist for genomic differentiation where environment-dependent sexual selection has played an important role. Here, we describe a very young (~90 years old) population of threespine sticklebacks exhibiting phenotypic and genomic differentiation between two habitats within the same pond. We show that differentiation among habitats is limited to male throat colour and nest type, traits known to be subject to sexual selection. Divergence in these traits mirrors divergence in much older benthic and limnetic stickleback species pairs from North American west coast lakes, which also occur in sympatry but are strongly reproductively isolated from each other. We demonstrate that in our population, differences in throat colour and breeding have been stable over a decade, but in contrast to North American benthic and limnetic stickleback species, these mating trait differences are not accompanied by divergence in morphology related to feeding, predator defence or swimming performance. Using genomewide SNP data, we find multiple genomic islands with moderate differentiation spread across several chromosomes, whereas the rest of the genome is undifferentiated. The islands contain potential candidate genes involved in visual perception of colour. Our results suggest that phenotypic and multichromosome genomic divergence of these morphs was driven by environment-dependent sexual selection, demonstrating incipient speciation after only a few decades of divergence in sympatry.

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Partially repeatable genetic basis of benthic adaptation in threespine sticklebacks

Cited by 39 publications

References 88 publications

The genetic and molecular architecture of phenotypic diversity in sticklebacks

The genetic and molecular architecture of phenotypic diversity in sticklebacks

Regulatory Architecture of Gene Expression Variation in the Threespine Stickleback Gasterosteus aculeatus

Genomic landscape of early ecological speciation initiated by selection on nuptial colour

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