Parallel transcriptome evolution in stream threespine sticklebacks

Abstract

Natural selection can cause similar phenotypic evolution in phylogenetically independent lineages inhabiting similar environments. Compared to morphological, behavioral, and physiological traits, little is known about the parallel evolution of transcriptome. Furthermore, the relative contribution of cis‐ and trans‐regulatory changes to parallel transcriptome evolution largely remains unclear. The threespine stickleback fish (Gasterosteus aculeatus) is a great model for studying parallel evolution because its ancestral marine populations independently colonized freshwater habitats in multiple geographical regions, resulting in independent pairs of marine and freshwater ecotypes in each region. Here, we investigated transcriptomic parallelism among the marine and stream ecotypes of Japanese and Canadian threespine sticklebacks by conducting common garden experiments and microarray analysis of the brain, which controls several physiological and behavioral traits differing between these ecotypes. We found parallel expression differences in 103 genes, including those encoding the enzymes involved in taurine synthesis and glycoprotein hydrolysis. The number of genes differentially expressed in parallel was significantly larger than the number of genes showing an antiparallel pattern (71 genes). To investigate the genetic architecture underlying transcriptome divergence, we re‐analyzed the previous expression quantitative trait locus (eQTL) data and found that most eQTLs were located on the same chromosome as the transcripts, possibly in cis‐regulatory regions. Furthermore, the effect sizes of the eQTLs on the same chromosomes were larger than those on different chromosomes. Thus, we found that divergence in the brain transcriptome between the ecotypes shows parallelism and is mainly caused by genetic changes occurring on the same chromosome as the target genes.

Unique signals of clinal and seasonal allele frequency change at eQTLs in Drosophila melanogaster

“…The levels of enrichment of clinal polymorphisms observed here are larger than those observed for other functional categories in Drosophila (Machado et al 2016) and other species (Ye et al 2013;Mack et al 2018), suggesting that SNPs underlying clinal adaptation are more likely to be eQTLs than other categories. This finding agrees with growing literature showing evidence that spatial differentiation at eQTLs contributes to local adaptation across various taxa (Fraser 2013;Gould et al 2017;Kitano et al 2018;Mack et al 2018;Phifer-Rixey et al 2018;Colicchio et al 2020).…”

Parallel and Population-specific Gene Regulatory Evolution in Cold-Adapted Fly Populations

“…The level of parallelism for gene expression abundance changes varies across study systems. In some taxa and natural conditions, significantly more genes show parallel changes (repeatedly up- or down-regulated in one ecotype relative to the other among independent population pairs) than anti-directional changes (Zhao et al 2015; Hart et al 2018; Kitano et al 2018; McGirr and Martin. 2018).…”

Genome Survey of Chromatin-Modifying Enzymes in Threespine Stickleback: A Crucial Epigenetic Toolkit for Adaptation?

“…An ecologically important fish species of interest for epigenetic studies in wild populations is threespine stickleback (Gasterosteus aculeatus), as it has been widely used as a model system to investigate the genetic and non-genetic basis of adaptation to novels environments (Shama and Wegner, 2014;Shama et al, 2016;Shama, 2017;Heckwolf et al, 2018;Metzger and Schulte, 2018;Kitano et al, 2019). After the last glaciation, marine stickleback colonized freshwater habitats of the north temperate zone, leading to local adaptation of populations that exhibit different phenotypes based on, for example, behavior, armor plate number, body shape, and gene expression plasticity (Kitano et al, 2019). Furthermore, whole genome sequence comparisons between freshwater and marine individuals revealed that differential gene expression contributed more to adaptive evolution than protein sequence evolution (Kitano et al, 2019).…”

“…After the last glaciation, marine stickleback colonized freshwater habitats of the north temperate zone, leading to local adaptation of populations that exhibit different phenotypes based on, for example, behavior, armor plate number, body shape, and gene expression plasticity (Kitano et al, 2019). Furthermore, whole genome sequence comparisons between freshwater and marine individuals revealed that differential gene expression contributed more to adaptive evolution than protein sequence evolution (Kitano et al, 2019). This, in combination with the ability to study the evolution of sex chromosome systems make stickleback an ideal candidate to elucidate the role of epigenetic mechanisms in reproduction, development, and adaptation in fishes (Figure 1).…”