Phylogenetic relationships and the evolution of regulatory gene sequences in the parrotfishes

Abstract

Regulatory genes control the expression of other genes and are key components of developmental processes such as segmentation and embryonic construction of the skull in vertebrates. Here we examine the variability and evolution of three vertebrate regulatory genes, addressing issues of their utility for phylogenetics and comparing the rates of genetic change seen in regulatory loci to the rates seen in other genes in the parrotfishes. The parrotfishes are a diverse group of colorful fishes from coral reefs and seagrasses worldwide and have been placed phylogenetically within the family Labridae. We tested phylogenetic hypotheses among the parrotfishes, with a focus on the genera Chlorurus and Scarus, by analyzing eight gene fragments for 42 parrotfishes and eight outgroup species. We sequenced mitochondrial 12s rRNA (967 bp), 16s rRNA (577 bp), and cytochrome b (477 bp). From the nuclear genome, we sequenced part of the protein-coding genes rag2 (715 bp), tmo4c4 (485 bp), and the developmental regulatory genes otx1 (672 bp), bmp4 (488 bp), and dlx2 (522 bp). Bayesian, likelihood, and parsimony analyses on the resulting 4903 bp of DNA sequence produced similar topologies that confirm the monophyly of the scarines and provide a phylogeny at the species level for portions of the genera Scarus and Chlorurus. Four major clades of Scarus were recovered, with three distributed in the Indo-Pacific and one containing Caribbean/Atlantic taxa. Molecular rates suggest a Miocene origin of the parrotfishes (22 mya) and a recent divergence of species within Scarus and Chlorurus, within the past 5 million years. Developmentally important genes made a significant contribution to phylogenetic structure, and rates of genetic evolution were high in bmp4, similar to other coding nuclear genes, but low in otx1 and the dlx2 exons. Synonymous and nonsynonymous substitution patterns in developmental regulatory genes support the hypothesis of stabilizing selection during the history of these genes, with several phylogenetic regions of accelerated nonsynonymous change detected in the phylogeny.

Interspecific hybridization causes long‐term phylogenetic discordance between nuclear and mitochondrial genomes in freshwater fishes

“…Our measure of concordance was thus for specifically mitochondrial vs. nuclear genome trees, except in one case where we used three nuclear (regulatory) vs. three mitochondrial plus two nuclear (nonregulatory) (Smith et al . ). This approach minimizes error resulting from poorly resolved nuclear gene trees.…”

Phylogenetic relationships of the Cobitoidea (Teleostei: Cypriniformes) inferred from mitochondrial and nuclear genes with analyses of gene evolution

“…For dN and dS, the former is considered to be related mainly to functional constraints (Kawahara and Imanishi, 2007), while the latter by purifying selection (Smith et al, 2008;Toll-Riera et al, 2011). For this reason, the nearly constant dN and significantly lower dS values of ND4 in the balitorid lineage suggests that it was mostly affected by relaxed purifying selection in this lineage.…”

Patterns and processes in the evolutionary history of parrotfishes (Family Labridae)

“…One of the primary exemplars for this model of adaptive radiation was the evolution of parrotfishes, comprising a speciose group of fishes confined largely to coral reefs (Streelman et al ., ; Streelman & Danley, ). As a result, the processes of sequential diversification under this radiation in stages model have been applied to the evolution of reef fish faunas, especially the Labridae (Smith et al ., ; Kazancioğlu et al ., ). However, recent studies suggest that aspects of this model require reconsideration.…”