Investigating the molecular basis of local adaptation to thermal stress: population differences in gene expression across the transcriptome of the copepod Tigriopus californicus

Anastasia Wolff,Ronald S Burton,Gary W Moy,Sean D Schoville,Felipe S Barreto

doi:10.1186/1471-2148-12-170

Abstract

BackgroundGeographic variation in the thermal environment impacts a broad range of biochemical and physiological processes and can be a major selective force leading to local population adaptation. In the intertidal copepod Tigriopus californicus, populations along the coast of California show differences in thermal tolerance that are consistent with adaptation, i.e., southern populations withstand thermal stresses that are lethal to northern populations. To understand the genetic basis of these physiological differences, we use an RNA-seq approach to compare genome-wide patterns of gene expression in two populations known to differ in thermal tolerance.ResultsObserved differences in gene expression between the southern (San Diego) and the northern (Santa Cruz) populations included both the number of affected loci as well as the identity of these loci. However, the most pronounced differences concerned the amplitude of up-regulation of genes producing heat shock proteins (Hsps) and genes involved in ubiquitination and proteolysis. Among the hsp genes, orthologous pairs show markedly different thermal responses as the amplitude of hsp response was greatly elevated in the San Diego population, most notably in members of the hsp70 gene family. There was no evidence of accelerated evolution at the sequence level for hsp genes. Among other sets of genes, cuticle genes were up-regulated in SD but down-regulated in SC, and mitochondrial genes were down-regulated in both populations.ConclusionsMarked changes in gene expression were observed in response to acute sub-lethal thermal stress in the copepod T. californicus. Although some qualitative differences were observed between populations, the most pronounced differences involved the magnitude of induction of numerous hsp and ubiquitin genes. These differences in gene expression suggest that evolutionary divergence in the regulatory pathway(s) involved in acute temperature stress may offer at least a partial explanation of population differences in thermal tolerance observed in Tigriopus.

Highlights

Geographic variation in the thermal environment impacts a broad range of biochemical and physiological processes and can be a major selective force leading to local population adaptation
We initiate investigations of the genetic mechanisms that underlie population differences in thermal tolerance observed in Tigriopus californicus [32]
78% of the total reads were uniquely mapped in the San Diego (SD) control sample, while ~82% reads were uniquely mapped in the SD heat stress sample

Summary

Introduction

Geographic variation in the thermal environment impacts a broad range of biochemical and physiological processes and can be a major selective force leading to local population adaptation. Several studies have shown that tolerance of intertidal invertebrates to thermal stress is correlated with local temperature regimes; much of this work has focused on the tolerance limits of different species, both among unrelated taxa [3] and among congeners [4,5,6] Results of these studies typically indicate that the geographic and ecological ranges of species are determined by thermal constraints, but the genetic basis for thermal tolerance is often not known and in some cases the observed phenotypic variation is driven by plasticity in traits rather than genetic differences among populations [7,8]. Rates of interpopulation gene flow must remain low, or gene swamping will override the effect of diversifying selection [10]

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