The phylogeny of extant starfish (Asteroidea: Echinodermata) including Xyloplax, based on comparative transcriptomics

Abstract

A B S T R A C TMulti-locus phylogenetic studies of echinoderms based on Sanger and RNA-seq technologies and the fossil record have provided evidence for the Asterozoa-Echinozoa hypothesis. This hypothesis posits a sister relationship between asterozoan classes (Asteroidea and Ophiuroidea) and a similar relationship between echinozoan classes (Echinoidea and Holothuroidea). Despite this consensus around Asterozoa-Echinozoa, phylogenetic relationships within the class Asteroidea (sea stars or starfish) have been controversial for over a century. Open questions include relationships within asteroids and the status of the enigmatic taxon Xyloplax. Xyloplax is thought by some to represent a newly discovered sixth class of echinoderms -and by others to be an asteroid. To address these questions, we applied a novel workflow to a large RNA-seq dataset that encompassed a broad taxonomic and genomic sample. This study included 15 species sampled from all extant orders and 13 families, plus four ophiuroid species as an outgroup. To expand the taxonomic coverage, the study also incorporated five previously published transcriptomes and one previously published expressed sequence tags (EST) dataset. We developed and applied methods that used a range of alignment parameters with increasing permissiveness in terms of gap characters present within an alignment. This procedure facilitated the selection of phylogenomic data subsets from large amounts of transcriptome data. The results included 19 nested data subsets that ranged from 37 to 4,281 loci. Tree searches on all data subsets reconstructed Xyloplax as a velatid asteroid rather than a new class. This result implies that asteroid morphology remains labile well beyond the establishment of the body plan of the group. In the phylogenetic tree with the highest average asteroid nodal support several monophyletic groups were recovered. In this tree, Forcipulatida and Velatida are monophyletic and form a clade that includes Brisingida as sister to Forcipulatida. Xyloplax is consistently recovered as sister to Pteraster. Paxillosida and Spinulosida are each monophyletic, with Notomyotida as sister to the Paxillosida. Valvatida is recovered as paraphyletic. The results from other data subsets are largely consistent with these results. Our results support the hypothesis that the earliest divergence event among extant asteroids separated Velatida and Forcipulatacea from Valvatacea and Spinulosida.

Functional characterization of a second pedal peptide/orcokinin‐type neuropeptide signaling system in the starfish Asterias rubens

“…Analysis of the genome/transcriptome of the crown‐of‐thorns starfish Acanthaster planci has revealed the presence of genes/transcripts encoding proteins that are orthologs of ArPPLNP1 and ArPPLNP2 (Smith et al, ). Furthermore, based on recent extensive molecular analysis of the phylogenetic relationships of extant Asteroidea (Linchangco et al, ), the occurrence of PPLNP1‐type (SMP‐type) and PPLNP2‐type proteins in A. rubens (order Forcipulatida) and in A. planci (order Valvatida) suggests that both of these PP/OK‐type precursors would have been present in the common ancestor of all extant starfish. Previous studies have shown that PPLN1‐type (SMP‐type) peptides act as muscle relaxants in P. pectinifera (order Valvatida and in A. rubens (order Forcipulatida) and therefore it seems likely, based on asteroid phylogeny (Linchangco et al, ), that PPLN1‐type peptides act as muscle relaxants in all extant starfish.…”

“…Furthermore, based on recent extensive molecular analysis of the phylogenetic relationships of extant Asteroidea (Linchangco et al, ), the occurrence of PPLNP1‐type (SMP‐type) and PPLNP2‐type proteins in A. rubens (order Forcipulatida) and in A. planci (order Valvatida) suggests that both of these PP/OK‐type precursors would have been present in the common ancestor of all extant starfish. Previous studies have shown that PPLN1‐type (SMP‐type) peptides act as muscle relaxants in P. pectinifera (order Valvatida and in A. rubens (order Forcipulatida) and therefore it seems likely, based on asteroid phylogeny (Linchangco et al, ), that PPLN1‐type peptides act as muscle relaxants in all extant starfish. This study is the first to reveal the myorelaxant activity of PPLN2‐type peptides in a starfish species— A. rubens (order Forcipulatida).…”

“…Acanthaster planci has revealed the presence of genes/transcripts encoding proteins that are orthologs of ArPPLNP1 and ArPPLNP2 (Smith et al, 2017). Furthermore, based on recent extensive molecular analysis of the phylogenetic relationships of extant Asteroidea (Linchangco et al, 2017), the occurrence of PPLNP1-type (SMP-type) and PPLNP2-type proteins in A. rubens (order Forcipulatida) and in A. planci (order Valvatida) suggests that both of these PP/OK-type precursors would have been present in the common ancestor of all extant starfish.…”

“…Previous studies have shown that PPLN1-type (SMP-type) peptides act as muscle relaxants in P. pectinifera (order Valvatida and in A. rubens (order Forcipulatida) and therefore it seems likely, based on asteroid phylogeny (Linchangco et al, 2017), that PPLN1-type peptides act as muscle relaxants in all extant starfish. This study is the first to reveal the myorelaxant activity of PPLN2-type peptides in a starfish species-A.…”

The structural and chemical basis of temporary adhesion in the sea star Asterina gibbosa

“…In this paper, we investigated the structural and chemical basis of temporary adhesion in the valvatid species Asterina gibbosa . The most recent molecular phylogeny of the Class Asteroidea supports a tree in which two main groups apparently diverged early in the evolution of sea stars [30]. According to this phylogeny, A. gibbosa and A. rubens could be considered as distantly-related species as they each belong to one of these two main sea star clades.…”