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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].
Addison,
Multiple gene genealogies reveal asymmetrical hybridization and introgression among strongylocentrotid sea urchins.
2009, Pubmed,
Echinobase
Addison,
Multiple gene genealogies reveal asymmetrical hybridization and introgression among strongylocentrotid sea urchins.
2009,
Pubmed
,
Echinobase
Andrew Cameron,
A basal deuterostome genome viewed as a natural experiment.
2007,
Pubmed
,
Echinobase
Avise,
Phylogenetics and the origin of species.
1997,
Pubmed
Berkes,
Ecology. Globalization, roving bandits, and marine resources.
2006,
Pubmed
,
Echinobase
Bernardi,
Vicariance and dispersal across Baja California in disjunct marine fish populations.
2003,
Pubmed
Biermann,
Phylogeny and development of marine model species: strongylocentrotid sea urchins.
2003,
Pubmed
,
Echinobase
Biermann,
The molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae).
1998,
Pubmed
,
Echinobase
Bininda-Emonds,
transAlign: using amino acids to facilitate the multiple alignment of protein-coding DNA sequences.
2005,
Pubmed
Boore,
Animal mitochondrial genomes.
1999,
Pubmed
Briggs,
In the beginning...animal fertilization and sea urchin development.
2006,
Pubmed
,
Echinobase
Britten,
Rates of DNA sequence evolution differ between taxonomic groups.
1986,
Pubmed
,
Echinobase
Britten,
Gene regulation for higher cells: a theory.
1969,
Pubmed
Britten,
Repeated sequences in DNA. Hundreds of thousands of copies of DNA sequences have been incorporated into the genomes of higher organisms.
1968,
Pubmed
Cameron,
SpBase: the sea urchin genome database and web site.
2009,
Pubmed
,
Echinobase
Castresana,
Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis.
2000,
Pubmed
Davidson,
The sea urchin genome: where will it lead us?
2006,
Pubmed
,
Echinobase
Erpenbeck,
Phylogenetic analyses under secondary structure-specific substitution models outperform traditional approaches: case studies with diploblast LSU.
2007,
Pubmed
Gowri-Shankar,
On the correlation between composition and site-specific evolutionary rate: implications for phylogenetic inference.
2006,
Pubmed
Guindon,
New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0.
2010,
Pubmed
Haq,
Chronology of fluctuating sea levels since the triassic.
1987,
Pubmed
Hofacker,
Automatic detection of conserved base pairing patterns in RNA virus genomes.
1999,
Pubmed
Howard-Ashby,
High regulatory gene use in sea urchin embryogenesis: Implications for bilaterian development and evolution.
2006,
Pubmed
,
Echinobase
Huang,
CAP3: A DNA sequence assembly program.
1999,
Pubmed
Hudelot,
RNA-based phylogenetic methods: application to mammalian mitochondrial RNA sequences.
2003,
Pubmed
Iken,
Large-scale spatial distribution patterns of echinoderms in nearshore rocky habitats.
2010,
Pubmed
,
Echinobase
Janies,
Echinoderm phylogeny including Xyloplax, a progenetic asteroid.
2011,
Pubmed
,
Echinobase
Junier,
The Newick utilities: high-throughput phylogenetic tree processing in the UNIX shell.
2010,
Pubmed
Karolchik,
The UCSC Genome Browser Database: 2008 update.
2008,
Pubmed
Kent,
BLAT--the BLAST-like alignment tool.
2002,
Pubmed
Kent,
The human genome browser at UCSC.
2002,
Pubmed
Knudson,
Of sea urchins and worms: development and cancer.
2004,
Pubmed
,
Echinobase
Kumar,
Statistics and truth in phylogenomics.
2012,
Pubmed
Larkin,
Clustal W and Clustal X version 2.0.
2007,
Pubmed
Lee,
Molecular phylogenies and divergence times of sea urchin species of Strongylocentrotidae, Echinoida.
2003,
Pubmed
,
Echinobase
Lessios,
Phylogeography and bindin evolution in Arbacia, a sea urchin genus with an unusual distribution.
2012,
Pubmed
,
Echinobase
Lessios,
Speciation genes in free-spawning marine invertebrates.
2011,
Pubmed
,
Echinobase
Littlewood,
A combined morphological and molecular phylogeny for sea urchins (Echinoidea: Echinodermata).
1995,
Pubmed
,
Echinobase
Maddison,
Inferring phylogeny despite incomplete lineage sorting.
2006,
Pubmed
Materna,
The S. purpuratus genome: a comparative perspective.
2006,
Pubmed
,
Echinobase
Ning,
SSAHA: a fast search method for large DNA databases.
2001,
Pubmed
Oliver,
Whole-genome positive selection and habitat-driven evolution in a shallow and a deep-sea urchin.
2010,
Pubmed
,
Echinobase
Palumbi,
All males are not created equal: fertility differences depend on gamete recognition polymorphisms in sea urchins.
1999,
Pubmed
,
Echinobase
Palumbi,
Evolutionary animation: how do molecular phylogenies compare to Mayr's reconstruction of speciation patterns in the sea?
2005,
Pubmed
,
Echinobase
Palumbi,
Marine speciation on a small planet.
1992,
Pubmed
Palumbi,
SPECIATION AND POPULATION GENETIC STRUCTURE IN TROPICAL PACIFIC SEA URCHINS.
1997,
Pubmed
,
Echinobase
Pamilo,
Relationships between gene trees and species trees.
1988,
Pubmed
Pearse,
Ecological role of purple sea urchins.
2006,
Pubmed
,
Echinobase
Pearson,
Modulating Hox gene functions during animal body patterning.
2005,
Pubmed
Pederson,
The sea urchin's siren.
2006,
Pubmed
,
Echinobase
Perseke,
Mitochondrial genome evolution in Ophiuroidea, Echinoidea, and Holothuroidea: insights in phylogenetic relationships of Echinodermata.
2010,
Pubmed
,
Echinobase
Perseke,
Evolution of mitochondrial gene orders in echinoderms.
2008,
Pubmed
,
Echinobase
Pujolar,
Positive Darwinian selection in gamete recognition proteins of Strongylocentrotus sea urchins.
2011,
Pubmed
,
Echinobase
Quinlan,
BEDTools: a flexible suite of utilities for comparing genomic features.
2010,
Pubmed
Rannala,
Phylogenetic inference using whole genomes.
2008,
Pubmed
Rast,
Marine invertebrate genome sequences and our evolving understanding of animal immunity.
2008,
Pubmed
,
Echinobase
Rice,
EMBOSS: the European Molecular Biology Open Software Suite.
2000,
Pubmed
Ronquist,
MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space.
2012,
Pubmed
Savill,
RNA sequence evolution with secondary structure constraints: comparison of substitution rate models using maximum-likelihood methods.
2001,
Pubmed
Shaw,
Conflict between nuclear and mitochondrial DNA phylogenies of a recent species radiation: what mtDNA reveals and conceals about modes of speciation in Hawaiian crickets.
2002,
Pubmed
Smith,
Testing the molecular clock: molecular and paleontological estimates of divergence times in the Echinoidea (Echinodermata).
2006,
Pubmed
,
Echinobase
Sodergren,
The genome of the sea urchin Strongylocentrotus purpuratus.
2006,
Pubmed
,
Echinobase
Takahata,
Genealogy of neutral genes in two partially isolated populations.
1990,
Pubmed
Telford,
Consideration of RNA secondary structure significantly improves likelihood-based estimates of phylogeny: examples from the bilateria.
2005,
Pubmed
Tillier,
High apparent rate of simultaneous compensatory base-pair substitutions in ribosomal RNA.
1998,
Pubmed
Yang,
PAML 4: phylogenetic analysis by maximum likelihood.
2007,
Pubmed
Yang,
Among-site rate variation and its impact on phylogenetic analyses.
1996,
Pubmed
Yang,
Molecular phylogenetics: principles and practice.
2012,
Pubmed
Zerbino,
Velvet: algorithms for de novo short read assembly using de Bruijn graphs.
2008,
Pubmed
Zerbino,
Using the Velvet de novo assembler for short-read sequencing technologies.
2010,
Pubmed
Zigler,
Speciation on the coasts of the new world: phylogeography and the evolution of bindin in the sea urchin genus Lytechinus.
2004,
Pubmed
,
Echinobase
Zigler,
Sea urchin bindin divergence predicts gamete compatibility.
2005,
Pubmed
,
Echinobase