Abstract

BackgroundStrongylocentrotid sea urchins have a long tradition as model organisms for studying many fundamental processes in biology including fertilization, embryology, development and genome regulation but the phylogenetic relationships of the group remain largely unresolved. Although the differing isolating mechanisms of vicariance and rapidly evolving gamete recognition proteins have been proposed, a stable and robust phylogeny is unavailable.ResultsWe used a phylogenomic approach with mitochondrial and nuclear genes taking advantage of the whole-genome sequencing of nine species in the group to establish a stable (i.e. concordance in tree topology among multiple lies of evidence) and robust (i.e. high nodal support) phylogenetic hypothesis for the family Strongylocentrotidae. We generated eight draft mitochondrial genome assemblies and obtained 13 complete mitochondrial genes for each species. Consistent with previous studies, mitochondrial sequences failed to provide a reliable phylogeny. In contrast, we obtained a very well-supported phylogeny from 2301 nuclear genes without evidence of positive Darwinian selection both from the majority of most-likely gene trees and the concatenated fourfold degenerate sites: ((P. depressus, (M. nudus, M. franciscanus), (H. pulcherrimus, (S. purpuratus, (S. fragilis, (S. pallidus, (S. droebachiensis, S. intermedius)). This phylogeny was consistent with a single invasion of deep-water environments followed by a holarctic expansion by Strongylocentrotus. Divergence times for each species estimated with reference to the divergence times between the two major clades of the group suggest a correspondence in the timing with the opening of the Bering Strait and the invasion of the holarctic regions.ConclusionsNuclear genome data contains phylogenetic signal informative for understanding the evolutionary history of this group. However, mitochondrial genome data does not. Vicariance can explain major patterns observed in the phylogeny. Other isolating mechanisms are appropriate to explore in this system to help explain divergence patterns not well supported by vicariance, such as the effects of rapidly evolving gamete recognition proteins on isolating populations. Our findings of a stable and robust phylogeny, with the increase in mitochondrial and nuclear comparative genomic data, provide a system in which we can enhance our understanding of molecular evolution and adaptation in this group of sea urchins.

Highlights

  • Strongylocentrotid sea urchins have a long tradition as model organisms for studying many fundamental processes in biology including fertilization, embryology, development and genome regulation but the phylogenetic relationships of the group remain largely unresolved

  • Incomplete lineage sorting and natural selection may all contribute to gene tree histories that do not represent the true species tree [42], resulting in gene trees that do not necessarily reflect species trees [50]., In this group of sea urchins, introgression has been documented between some taxa [37], and of the primary mechanisms of horizontal gene transfer (HGT), the possibility of HGT by viral transfer exists but is likely to be extremely rare

  • Recent phylogenomic work has demonstrated the potential poor performance of standard phylogenetic methods due to among-site rate variation, causing shifts in the phylogenetic positions of terminal taxa in well-supported trees generated from different models of nucleotide substitution or by different methods [56]. Our analyses evaluated both the gene level supportbased evidence and a concatenated site approach including the implicit model of nucleotide evolution in Maximum Parsimony (MP), an explicit model of GTR + I + G with Bayesian Inference (BI) and a mixture model allowing for rate variation among sites under Maximum Likelihood (ML)

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Summary

Introduction

Strongylocentrotid sea urchins have a long tradition as model organisms for studying many fundamental processes in biology including fertilization, embryology, development and genome regulation but the phylogenetic relationships of the group remain largely unresolved. Sea urchins are a primary research model for embryology [5], fertilization [6], bilaterian development [7], genomic regulatory systems [8,9] and our basic understanding of fundamental properties of genomes [10,11] They provide broadly useful natural systems in which we investigate central evolutionary questions of natural selection [12,13], reproductive isolation [14] and speciation [15,16,17] and ecological questions of population responses to disease [18] and global scale habitat distribution patterns [19]. Our first coherent view of cancer was provided by studying embryonic development in sea urchins [20] and origins of the phagocytic theory, a key process in the idea of an immune system, were based on observations of the movement and engulfing of foreign particles in echinoderm tissue [21]

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