Revealing less derived nature of cartilaginous fish genomes with their evolutionary time scale inferred with nuclear genes.

Adina J Renz,Shigehiro Kuraku,Axel Meyer,Hector Escriva

doi:10.1371/journal.pone.0066400

Abstract

Cartilaginous fishes, divided into Holocephali (chimaeras) and Elasmoblanchii (sharks, rays and skates), occupy a key phylogenetic position among extant vertebrates in reconstructing their evolutionary processes. Their accurate evolutionary time scale is indispensable for better understanding of the relationship between phenotypic and molecular evolution of cartilaginous fishes. However, our current knowledge on the time scale of cartilaginous fish evolution largely relies on estimates using mitochondrial DNA sequences. In this study, making the best use of the still partial, but large-scale sequencing data of cartilaginous fish species, we estimate the divergence times between the major cartilaginous fish lineages employing nuclear genes. By rigorous orthology assessment based on available genomic and transcriptomic sequence resources for cartilaginous fishes, we selected 20 protein-coding genes in the nuclear genome, spanning 2973 amino acid residues. Our analysis based on the Bayesian inference resulted in the mean divergence time of 421 Ma, the late Silurian, for the Holocephali-Elasmobranchii split, and 306 Ma, the late Carboniferous, for the split between sharks and rays/skates. By applying these results and other documented divergence times, we measured the relative evolutionary rate of the Hox A cluster sequences in the cartilaginous fish lineages, which resulted in a lower substitution rate with a factor of at least 2.4 in comparison to tetrapod lineages. The obtained time scale enables mapping phenotypic and molecular changes in a quantitative framework. It is of great interest to corroborate the less derived nature of cartilaginous fish at the molecular level as a genome-wide phenomenon.

Highlights

Chondrichthyans occupy a key phylogenetic position among extant vertebrates as one of the earlybranching lineages [1,2,3]
After investigation of the corresponding alignment of each gene, 122 candidate genes were excluded from further analyses, because they yielded spurious blast hits corresponding to sequences expanded into abundant copies (.500) in the chimaera genome
These 122 discarded candidates included genes whose mammalian orthologs are known to be involved in pathogen recognition and signal transduction [e.g. the nod-like receptor (NLR) family, the tripartite motif (TRIM) family and proteins containing WD repeats or FYVE zinc-finger domains] or are predicted hypothetical genes

Summary

Introduction

Chondrichthyans (cartilaginous fishes) occupy a key phylogenetic position among extant vertebrates as one of the earlybranching lineages [1,2,3]. The basal dichotomy between batoids and sharks and monophylies of each of these two groups (Figure 1) have been supported by several molecular phylogenetic studies employing genes in mtDNA [9,14,15,16,17] and the nucleus-encoded recombination activating gene 1 (RAG1) [18]. Based on this phylogenetic relationship, the monophyletic group containing all sharks is designated ‘Selachimorpha’ (Figure 1). This assignment of Synechodontiformes into a monophyletic group which originated at the basal position of living sharks shifts the previously assumed minimum constraint of 190 Ma as the origin of modern sharks [20] back to the Late Permian around 250 Ma [15,19]

Methods

Results

Discussion

Conclusion