Convergent evolution of gene expression in two high-toothed stickleback populations

Abstract

25Changes in developmental gene regulatory networks enable evolved changes in morphology. 26These changes can be in cis regulatory elements that act in an allele-specific manner, or 27 changes to the overall trans regulatory environment that interacts with cis regulatory 28 sequences. Here we address several questions about the evolution of gene expression 29 accompanying a convergently evolved constructive morphological trait, increases in tooth 30 number in two independently derived freshwater populations of threespine stickleback fish 31 (Gasterosteus aculeatus). Are convergently evolved cis and/or trans changes in gene 32 expression associated with convergently evolved morphological evolution? Do cis or trans 33 regulatory changes contribute more to the evolutionary gain of a morphological trait? 34Transcriptome data from dental tissue of ancestral low-toothed and two independently derived 35 high-toothed stickleback populations revealed significantly shared gene expression changes 36 that have convergently evolved in the two high-toothed populations. Comparing cis and trans 37 regulatory changes using phased gene expression data from F1 hybrids, we found that trans 38 regulatory changes were predominant and more likely to be shared among both high-toothed 39 populations. In contrast, while cis regulatory changes have evolved in both high-toothed 40 populations, overall these changes were distinct and not shared among high-toothed 41 populations. Together these data suggest that a convergently evolved trait can occur through 42 genetically distinct regulatory changes that converge on similar trans regulatory 43

Parallel transcriptome evolution in stream threespine sticklebacks

“…If we assume that the majority of the eQTLs on the same chromosomes are putatively cis ‐regulatory mutations, as reported in a previous study (Ponsuksili, Murani, Schwerin, Schellander, & Wimmers, ), our data suggest that cis ‐regulatory mutations contribute more to the transcriptome evolution between ecotypes than trans ‐regulatory mutations. This contrasts with a previous work on the stickleback dental tissues, indicating that the contribution of trans ‐regulatory mutations is larger than cis ‐regulatory mutations to parallel gene expression changes (Hart et al., ). Further analysis on tissues other than brains and dental tissues would help to understand whether different tissues have different mechanisms underlying parallel transcriptome evolution.…”

“…If the contribution of the parallel evolution of gene expression to phenotypic convergence is prevalent, we can predict that many genes would be repeatedly up‐ or down‐regulated in one ecotype compared to another in independent lineages. Consistent with this prediction, some of the previous transcriptome studies showed parallel transcriptome evolution between the low‐ and the high‐latitude populations of Drosophila melanogaster and D. simulans and between the marine and freshwater ecotypes of stickleback (Hart, Ellis, Eisen, & Miller, ; Zhao, Wit, Svetec, & Begun, ). However, other studies failed to show significant parallel patterns between the wild and weedy populations of Helianthus annuus (Lai, Kane, Zou, & Rieseberg, ) or revealed not only parallel, but also antiparallel patterns (i.e., ecotypes in different lineages showed opposite direction of differential expression) between the normal and dwarf morphs of whitefish (Derome, Duchesne, & Bernatchez, ) and between the lake and stream ecotypes of stickleback (Hanson, Hu, Hendry, & Barrett, ).…”

“…Therefore, even if parallelism is observed in the expression of many genes, it is not certain whether they are caused by many cis ‐regulatory mutations across the genome or a few pleiotropic trans ‐regulatory mutations. Although a previous study indicated that trans ‐regulatory changes contribute more to parallel evolution than cis ‐regulatory changes (Hart et al., ), we do not know how general this pattern is.…”

“…Two previous studies examined the parallel patterns of genome‐wide transcriptome evolution in sticklebacks. The transcriptome analysis of dental tissues in marine and freshwater populations showed parallel transcriptome evolution (Hart et al., ). In contrast, another study on the livers of lake–stream sticklebacks showed not only parallel patterns, but also antiparallel patterns (Hanson et al., ).…”

Population transcriptomics reveals weak parallel genetic basis in repeated marine and freshwater divergence in nine‐spined sticklebacks

“…(2015) demonstrated substantial heritability of genome‐wide gene expression variation in a three‐spined stickleback population from the Baltic Sea. Likewise, the genetic basis of gene expression variation has been recently uncovered in several three‐spined stickleback populations (Hart, Ellis, Eisen, & Miller, 2018; Pritchard et al., 2017). Notably, trans ‐regulatory changes are predominant and more likely to be shared among convergently evolved populations, whereas different cis ‐regulatory changes are more frequent in convergently evolved populations (Hart et al., 2018).…”