Abstract

Heritable phenotypic differences between populations, caused by the selective effects of distinct environmental conditions, are of commonplace occurrence in nature. However, the actual genomic targets of this kind of selection are still poorly understood. We conducted a quantitative trait locus (QTL) mapping study to identify genomic regions responsible for morphometric differentiation between genetically and phenotypically divergent marine and freshwater nine-spined stickleback (Pungitius pungitius) populations. Using a dense panel of SNP-markers obtained by restriction site associated DNA sequencing of an F2 recombinant cross, we found 22 QTL that explained 3.5–12.9% of phenotypic variance in the traits under investigation. We detected one fairly large-effect (PVE = 9.6%) QTL for caudal peduncle length–a trait with a well-established adaptive function showing clear differentiation among marine and freshwater populations. We also identified two large-effect QTL for lateral plate numbers, which are different from the lateral plate QTL reported in earlier studies of this and related species. Hence, apart from identifying several large-effect QTL in shape traits showing adaptive differentiation in response to different environmental conditions, the results suggest intra- and interspecific heterogeneity in the genomic basis of lateral plate number variation.

Highlights

  • Heritable phenotypic differences between populations, caused by the selective effects of distinct environmental conditions, are of commonplace occurrence in nature

  • Adaptive genetic divergence in body shape among fish populations residing in different environments has been repeatedly demonstrated[10,11,12], but the genetic underpinnings of this divergence are still fairly poorly understood[13,14]

  • The three-spined stickleback (Gasterosteus aculeatus) has been proposed as a model to study the evolution of body shape in fish[17]; recently the nine-spined stickleback (Pungitius pungitius)– which diverged from the three-spined stickleback around 13 million years ago18–has been emerging as a model for evolutionary investigations[19]

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Summary

Introduction

Heritable phenotypic differences between populations, caused by the selective effects of distinct environmental conditions, are of commonplace occurrence in nature. We conducted a quantitative trait locus (QTL) mapping study to identify genomic regions responsible for morphometric differentiation between genetically and phenotypically divergent marine and freshwater nine-spined stickleback (Pungitius pungitius) populations. Adaptive genetic divergence in body shape among fish populations residing in different environments has been repeatedly demonstrated[10,11,12], but the genetic underpinnings of this divergence are still fairly poorly understood[13,14] This is not surprising, because body shape is a complex trait, likely to be highly polygenic: large sample sizes, both in terms of number of individuals and markers, are needed to identify the causal loci influencing variation in such traits[15,16]. The power and precision of QTL-mapping critically depends on the experimental design and number of mapped progeny[53], Stange et al.[54] demonstrated that high-density maps can increase the precision of QTL localization and effect sizes, especially for small and medium sized QTL, as well as the power to resolve closely linked QTL

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