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BACKGROUND: 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. Although the differing isolating mechanisms of vicariance and rapidly evolving gamete recognition proteins have been proposed, a stable and robust phylogeny is unavailable.
RESULTS: We 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.
CONCLUSIONS: Nuclear 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.
Figure 1. The cladogram of the most frequent tree obtained from the Maximum Likelihood analysis of 2301 nuclear genes without evidence of positive selection. Branch support is quantified as the frequency that the node is supported by a gene alignment where the most frequent tree was not rejected or the gene’s ML tree was significantly different from the most frequent tree (see text). The tree is rooted between the two major clades identified in this group.
Figure 2. The 50% majority rule consensus phylogram of the stationary trees obtained from the Bayesian inference analysis of concatenated neutral nuclear genes at four-fold degenerate sites mid-point rooted between the two major clades previously identified. Branch support values are the BI posterior probabilities (PP), MP bootstrap (BSMP) and ML bootstrap (BSML) for genes rejecting evidence of positive selection. Branches leading to deep water species are colored in purple. The branch leading to S. droebachiensis is colored blue, as this species occurs primarily in shallow water but can range to a depth of 300 m. Adult depth range: s, shallow (0-50 m); m, medium (0-200 m); d, deep (0-1600 m). Distributions: West Pacific (WP), East Pacific (EP), holarctic (HA). The cross-section of the ultrastructure of primary spines [59]: rectangular (r), trapezoid (z), triangular (t) or ansiform (a).
Figure 3. The 50% majority rule consensus phylogram of the stationary trees obtained from the Bayesian inference analysis of concatenated mitochondrial genes at all sites. Branch support are the Bayesian Inference posterior probabilities (BI PP), Maximum Parsimony bootstrap (MP BS) and Maximum Likelihood bootstrap (ML BS) for concatenated mitochondrial genes above and four-fold degenerate sites below the branch. Asterisks on the branch labels denote strong support for the method or all methods (BI PP > =99, MP BS > =95, ML BS > =95). Unsupported nodes are indicated with ‘-‘. Single quotation marks next to a taxon name denote the de novo assembled individual from this study of the species. Scale bar, substitutions per site.
Figure 4. The molecular clock enforced dated phylogram from Bayesian Inference (BI) among fourfold degenerate sites from partial alignments of 2,562 nuclear genes without evidence of positive selection calibrated on fossil data. The Bayes Factor test shows no difference with the clock-enforced tree and clock-non-enforced tree. Blue 95% HPD node bars are filled according to posterior probability. Vertical arrows mark the approximate timing of the opening of the Bering Strait [69]. The scale bars denote time based on two dates of calibration based on the fossil record: 13–19 Ma at node A with 12S mitochondrial sequence (Lee, 2003 rate estimate’) [35] and 5–12 Ma at node C (‘Fossil’) [67].
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