Utility of sequenced genomes for microsatellite marker development in non-model organisms: a case study of functionally important genes in nine-spined sticklebacks (Pungitius pungitius)

Shikano, Takahito; Ramadevi, J.; Shimada, Yukinori; Merilä, Juha

doi:10.1186/1471-2164-11-334

Cited by 33 publications

(45 citation statements)

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“…Because the two species diverged 13 Mya [22], we anticipated that the genetic differences would be considerable despite the highly ecological, phenotypic, and genetic similarities between the species [23, 43]. The rate of sequence substitution is of central importance to understand mechanisms underlying molecular evolution.…”

Section: Discussionmentioning

confidence: 99%

Genomic divergence between nine- and three-spined sticklebacks

et al. 2013

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BackgroundComparative genomics approaches help to shed light on evolutionary processes that shape differentiation between lineages. The nine-spined stickleback (Pungitius pungitius) is a closely related species of the ecological ‘supermodel’ three-spined stickleback (Gasterosteus aculeatus). It is an emerging model system for evolutionary biology research but has garnered less attention and lacks extensive genomic resources. To expand on these resources and aid the study of sticklebacks in a phylogenetic framework, we characterized nine-spined stickleback transcriptomes from brain and liver using deep sequencing.ResultsWe obtained nearly eight thousand assembled transcripts, of which 3,091 were assigned as putative one-to-one orthologs to genes found in the three-spined stickleback. These sequences were used for evaluating overall differentiation and substitution rates between nine- and three-spined sticklebacks, and to identify genes that are putatively evolving under positive selection. The synonymous substitution rate was estimated to be 7.1 × 10-9 per site per year between the two species, and a total of 165 genes showed patterns of adaptive evolution in one or both species. A few nine-spined stickleback contigs lacked an obvious ortholog in three-spined sticklebacks but were found to match genes in other fish species, suggesting several gene losses within 13 million years since the divergence of the two stickleback species. We identified 47 SNPs in 25 different genes that differentiate pond and marine ecotypes. We also identified 468 microsatellites that could be further developed as genetic markers in nine-spined sticklebacks.ConclusionWith deep sequencing of nine-spined stickleback cDNA libraries, our study provides a significant increase in the number of gene sequences and microsatellite markers for this species, and identifies a number of genes showing patterns of adaptive evolution between nine- and three-spined sticklebacks. We also report several candidate genes that might be involved in differential adaptation between marine and freshwater nine-spined sticklebacks. This study provides a valuable resource for future studies aiming to identify candidate genes underlying ecological adaptation in this and other stickleback species.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-14-756) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Genomic divergence between nine- and three-spined sticklebacks

et al. 2013

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“…All the F 2 offspring ( N = 283) and their parents and grandparents ( N = 4) were genotyped for 235 microsatellite markers (Largiadèr et al 1999; Peichel et al 2001; Heckel et al 2002; Colosimo et al 2004; Miller et al 2007; Mäkinen et al 2008; Shapiro et al 2009; Shikano et al 2010b, 2011; Shimada et al 2011; Laine et al 2012; Supporting Information, Table S1). Out of the 235 markers, 46 were developed for specific genes with known biological functions in fish (Shapiro et al 2009; Shikano et al 2010b; Shimada et al 2011; Laine et al 2012). Polymerase chain reactions (PCRs) for all markers except Ppbig were performed in a 10-μl volume containing 1× Qiagen Multiplex PCR Master Mix (Qiagen), 0.5× Q-Solution, 2 pmol of each primer, and 10–20 ng of template DNA.…”

Section: Methodsmentioning

confidence: 99%

Genetic Architecture of Parallel Pelvic Reduction in Ninespine Sticklebacks

Shikano

Laine

Herczeg

et al. 2013

G3 Genes|Genomes|Genetics

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Teleost fish genomes are known to be evolving faster than those of other vertebrate taxa. Thus, fish are suited to address the extent to which the same vs. different genes are responsible for similar phenotypic changes in rapidly evolving genomes of evolutionary independent lineages. To gain insights into the genetic basis and evolutionary processes behind parallel phenotypic changes within and between species, we identified the genomic regions involved in pelvic reduction in Northern European ninespine sticklebacks (Pungitius pungitius) and compared them to those of North American ninespine and threespine sticklebacks (Gasterosteus aculeatus). To this end, we conducted quantitative trait locus (QTL) mapping using 283 F2 progeny from an interpopulation cross. Phenotypic analyses indicated that pelvic reduction is a recessive trait and is inherited in a simple Mendelian fashion. Significant QTL for pelvic spine and girdle lengths were identified in the region of the Pituitary homeobox transcription factor 1 (Pitx1) gene, also responsible for pelvic reduction in threespine sticklebacks. The fact that no QTL was observed in the region identified in the mapping study of North American ninespine sticklebacks suggests that an alternative QTL for pelvic reduction has emerged in this species within the past 1.6 million years after the split between Northern European and North American populations. In general, our study provides empirical support for the view that alternative genetic mechanisms that lead to similar phenotypes can evolve over short evolutionary time scales.

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“…Comparative genomic analyses have revealed the evolutionary history of the 7SL RNA-derived SINEs including the Alu within the Supraprimates (Kriegs et al, 2007). Genome-wide surveys of REs also make it possible to identify microsatellite sequences of various lengths among eukaryotic species and will help to identify molecular landmarks for evolutionary, population genetic and conservation studies (Csencsics et al, 2010;Saarinen and Austin, 2010;Shikano et al, 2010). Thus, RE variations in genomes of animals provide useful insight for genome structure evolution.…”

Section: Introductionmentioning

confidence: 96%