Gene expression dynamics during rapid organismal diversification in African cichlid fishes

Abstract

Changes in gene expression play a fundamental role in phenotypic evolution. Transcriptome evolutionary dynamics have so far mainly been compared among distantly related species and remain largely unexplored during rapid organismal diversification, in which gene regulatory changes have been suggested as particularly effective drivers of phenotypic divergence. Here, we studied gene expression evolution in a model system of adaptive radiation, the cichlid fishes of African Lake Tanganyika. By comparing gene expression profiles of six different organs in 74 cichlid species representing all subclades of this radiation, we demonstrate that the rate of gene expression evolution varies among organs, transcriptome parts, and the subclades of the radiation, indicating different strengths of selection. We found that the non-coding part of the transcriptome evolved more rapidly than the coding part, and that the gonadal transcriptomes evolved more rapidly than the somatic ones, with the exception of liver. We further show that the rate of gene-expression change was not constant over the course of the radiation but accelerated at its later phase. Finally, we show that – at the per-gene level – the evolution of expression patterns is dominated by stabilizing selection.

Dynamics of sex chromosome evolution in a rapid radiation of cichlid fishes

“…To identify sex chromosomes in LT cichlids, we screened male and female genomes of 244 taxa ( 24 ) as well as six transcriptomes of each of 66 taxa ( 28 ) for signatures of sex-linked regions, applying three complementary approaches: genome-wide association study (GWAS; on the genomic data, approach 1, see Materials and Methods), identification of sex-specific SNPs in the genomic data (approach 2), and tests of allele frequency differences on the transcriptome data (approach 3). Genomic locations of inferred sex-linked regions refer to linkage groups (LGs) of the used reference genome of a phylogenetically equidistant outgroup to the cichlid species of the LT radiation, the Nile tilapia ( Oreochromis niloticus ).…”

“…Here we report the identification of genomic signatures supportive of sex chromosomes in 79 taxa of cichlid fishes, most of which belonging to the cichlid adaptive radiation of LT, based on the analysis of whole-genome data from virtually all cichlid species of the radiation ( 24 ) and transcriptome data from a representative set of 66 taxa ( 28 ).…”

“…the limited sample size per-species in the currently available data may have left some SD regions undetected, we found it particularly intriguing that we could identify sex-linked regions only in three species across the second-most species-rich tribe, Ectodini (the available transcriptome data are representative in terms of species-richness per tribe(28)). Some species of this tribe display an impressive level of sexual dimorphism, suggesting similar or even more pronounced sexual antagonistic selection compared to tribes such as the Haplochromini/Tropheini, which show relatively strongly differentiated sex chromosomes.…”

“…In this study, we inspected genomic ( 24 ) and transcriptomic ( 28 ) information from 229 Lake Tanganyika cichlid taxa as well as 18 cichlid species belonging to the Haplochromini and Lamprologini lineages phylogenetically nested within the LT radiation ( 24, 29 ) for signatures of sex chromosomes. Based on this nearly complete taxon sampling of the LT radiation and an available phylogenetic hypothesis based on genome-wide data ( 24 ), we estimated the amount and direction of sex chromosome turnovers in this young species flock.…”

Continuouscis-regulatory changes in an advantageous gene are linked with adaptive radiation in cichlid fishes

“…Indeed, such findings for proteins are often exciting but can be counted on one hand, in particular for adaptive radiation [6][7][8] . Instead, emphasizing the roles of gene regulation in adaptive radiation arises frequently, especially with recent advances in genome-wide association studies, in which noncoding regions are often linked with gene expression changes [9][10][11] . However, functional evidence of these noncoding regions in the form of their cis-regulatory roles, especially for small changes such as SNPs, is necessary but sparse (but see the reference 12 ), particularly in the context of whether many loci with small changes or one single locus with large effects can have phenotypic changes 13 .…”