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Genome Biol Evol
2010 Jan 01;2:800-14. doi: 10.1093/gbe/evq063.
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Whole-genome positive selection and habitat-driven evolution in a shallow and a deep-sea urchin.
Oliver TA
,
Garfield DA
,
Manier MK
,
Haygood R
,
Wray GA
,
Palumbi SR
.
Abstract
Comparisons of genomic sequence between divergent species can provide insight into the action of natural selection across many distinct classes of proteins. Here, we examine the extent of positive selection as a function of tissue-specific and stage-specific gene expression in two closely-related sea urchins, the shallow-water Strongylocentrotus purpuratus and the deep-sea Allocentrotus fragilis, which have diverged greatly in their adult but not larval habitats. Genes that are expressed specifically in adult somatic tissue have significantly higher dN/dS ratios than the genome-wide average, whereas those in larvae are indistinguishable from the genome-wide average. Testis-specific genes have the highest dN/dS values, whereas ovary-specific have the lowest. Branch-site models involving the outgroup S. franciscanus indicate greater selection (ω(FG)) along the A. fragilis branch than along the S. purpuratus branch. The A. fragilis branch also shows a higher proportion of genes under positive selection, including those involved in skeletal development, endocytosis, and sulfur metabolism. Both lineages are approximately equal in enrichment for positive selection of genes involved in immunity, development, and cell-cell communication. The branch-site models further suggest that adult-specific genes have experienced greater positive selection than those expressed in larvae and that ovary-specific genes are more conserved (i.e., experienced greater negative selection) than those expressed specifically in adult somatic tissues and testis. Our results chart the patterns of protein change that have occurred after habitat divergence in these two species and show that the developmental or functional context in which a gene acts can play an important role in how divergent species adapt to new environments.
FIG. 1.—. Pairwise Allocentrotus fragilis: Strongylocentrotus purpuratus dN/dS histograms–(A) Per-read analysis, (B) whole-gene analysis. Note both distributions are plotted on a Log2 x axis scale.
FIG. 2.—. Dendrogram of tissue-specific expression. The dendrogram represents similarities in expression profile of a given tissue using cluster analysis after binarizing expression in each tissue.
FIG. 3.—. Venn diagram of four tissue expression categories using dN/dS calculated from per-read alignments. Shading represents median dN/dS ratios for a given expression category. Percentages within each section report the percentage of all expressed genes/alignments that fell into that category. Asterisks (*) denote a category whose dN/dS distribution is significantly different than the whole-genome dN/dS distribution via two-tailed Mann-Whitney test. A single asterisk (*) denote a category that is significant at the α = 0.05 level, while two asterisks (**) denote a category whose significance is robust to Bonferroni correction for 16 tests, giving α = 0.003.
FIG. 4.—. Comparisons of the composition of the data set by expression categories for both all dN/dS values and a set of high dN/dS genes. Asterisks denote categories showing significant changes among sets, by χ2 with alpha corrected for four tests per data set (α = 0.012).
FIG. 5.—. (A) All tissue mean branch-specific ωFG from branch-specific likelihood model. Error bars show the 95% CIs of 1,000 bootstrap replicates of the mean. Asterisks indicate a significant difference in distributions via Mann-Whitney test. (B) Branch-specific proportion of genes showing significant positive selection in the branch-specific likelihood model. Asterisk indicates a significant comparison by χ2.
FIG. 6.—. (A) Mean branch-specific ωFG from branch-specific likelihood model across each tissue-specific expression category. Error bars show the 95% CIs of 1,000 bootstrap replicates of the mean. Asterisks indicate a significant difference between a given tissue-specific distribution and the all tissue distribution via Mann-Whitney test, Bonferroni corrected for eight comparisons. (B) Branch-specific proportion of genes showing significant positive selection in the branch-specific likelihood model across each tissue-specific expression category. Asterisk indicates a significant comparison by χ2, Bonferroni corrected for eight comparisons.
FIG. 7.—. (A) Positive, (B) neutral, and (C) negative selection scores along each branch from the branch-specific likelihood model, across all tissue-specific expression categories. Asterisks indicate a significant difference between a given tissue-specific distribution and the all tissue distribution via Mann-Whitney test, Bonferroni corrected for eight comparisons.
FIG. 8.—. Correlations between Strongylocentrotus purpuratus and Allocentrotus fragilis selection scores for each of 11.115 genes in branch-specific data set. (A) Correlations between negative selection scores (Pearson's r = 0.81); (B) Correlations between neutrality scores (r = 0.76); and (C) Correlations between positive selection scores (r = 0.08).
ALLISON,
Protection afforded by sickle-cell trait against subtertian malareal infection.
1954, Pubmed
ALLISON,
Protection afforded by sickle-cell trait against subtertian malareal infection.
1954,
Pubmed
Altschul,
Basic local alignment search tool.
1990,
Pubmed
Arbiza,
Positive selection, relaxation, and acceleration in the evolution of the human and chimp genome.
2006,
Pubmed
Artieri,
Ontogeny and phylogeny: molecular signatures of selection, constraint, and temporal pleiotropy in the development of Drosophila.
2009,
Pubmed
Babbitt,
Both noncoding and protein-coding RNAs contribute to gene expression evolution in the primate brain.
2010,
Pubmed
Bakewell,
More genes underwent positive selection in chimpanzee evolution than in human evolution.
2007,
Pubmed
Begun,
Population genomics: whole-genome analysis of polymorphism and divergence in Drosophila simulans.
2007,
Pubmed
Biermann,
Phylogeny and development of marine model species: strongylocentrotid sea urchins.
2003,
Pubmed
,
Echinobase
Blanchette,
Aligning multiple genomic sequences with the threaded blockset aligner.
2004,
Pubmed
Blekhman,
Gene regulation in primates evolves under tissue-specific selection pressures.
2008,
Pubmed
Bustamante,
Natural selection on protein-coding genes in the human genome.
2005,
Pubmed
Castillo-Davis,
Genome evolution and developmental constraint in Caenorhabditis elegans.
2002,
Pubmed
Chimpanzee Sequencing and Analysis Consortium,
Initial sequence of the chimpanzee genome and comparison with the human genome.
2005,
Pubmed
Clark,
Positive selection in the human genome inferred from human-chimp-mouse orthologous gene alignments.
2003,
Pubmed
Cobbett,
Phytochelatins and metallothioneins: roles in heavy metal detoxification and homeostasis.
2002,
Pubmed
Davidson,
Gene regulatory networks and the evolution of animal body plans.
2006,
Pubmed
Davis,
Protein evolution in the context of Drosophila development.
2005,
Pubmed
Ellegren,
Sequencing goes 454 and takes large-scale genomics into the wild.
2008,
Pubmed
Elsik,
Creating a honey bee consensus gene set.
2007,
Pubmed
Emlet,
DEVELOPMENTAL MODE AND SPECIES GEOGRAPHIC RANGE IN REGULAR SEA URCHINS (ECHINODERMATA: ECHINOIDEA).
1995,
Pubmed
,
Echinobase
Fitch,
Positive Darwinian evolution in human influenza A viruses.
1991,
Pubmed
Galau,
A measurement of the sequence complexity of polysomal messenger RNA in sea urchin embryos.
1974,
Pubmed
,
Echinobase
Garfield,
Comparative embryology without a microscope: using genomic approaches to understand the evolution of development.
2009,
Pubmed
Gibbs,
Evolutionary and biomedical insights from the rhesus macaque genome.
2007,
Pubmed
Hoyle,
Making sense of microarray data distributions.
2002,
Pubmed
Hughes,
Pattern of nucleotide substitution at major histocompatibility complex class I loci reveals overdominant selection.
1988,
Pubmed
Huse,
Accuracy and quality of massively parallel DNA pyrosequencing.
2007,
Pubmed
Kent,
BLAT--the BLAST-like alignment tool.
2002,
Pubmed
Kosiol,
Patterns of positive selection in six Mammalian genomes.
2008,
Pubmed
Lee,
Molecular phylogenies and divergence times of sea urchin species of Strongylocentrotidae, Echinoida.
2003,
Pubmed
,
Echinobase
Li,
CHST1 and CHST2 sulfotransferases expressed by human vascular endothelial cells: cDNA cloning, expression, and chromosomal localization.
1999,
Pubmed
Nei,
Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions.
1986,
Pubmed
Nielsen,
A scan for positively selected genes in the genomes of humans and chimpanzees.
2005,
Pubmed
Palumbi,
Strong reproductive isolation between closely related tropical sea urchins (genus Echinometra).
1991,
Pubmed
,
Echinobase
Pond,
HyPhy: hypothesis testing using phylogenies.
2005,
Pubmed
Roux,
Developmental constraints on vertebrate genome evolution.
2008,
Pubmed
Sabeti,
Genome-wide detection and characterization of positive selection in human populations.
2007,
Pubmed
Samanta,
The transcriptome of the sea urchin embryo.
2006,
Pubmed
,
Echinobase
Smyth,
Linear models and empirical bayes methods for assessing differential expression in microarray experiments.
2004,
Pubmed
Sodergren,
The genome of the sea urchin Strongylocentrotus purpuratus.
2006,
Pubmed
,
Echinobase
Sutter,
A single IGF1 allele is a major determinant of small size in dogs.
2007,
Pubmed
Swanson,
The rapid evolution of reproductive proteins.
2002,
Pubmed
Thomas,
PANTHER: a library of protein families and subfamilies indexed by function.
2003,
Pubmed
Uddin,
Sister grouping of chimpanzees and humans as revealed by genome-wide phylogenetic analysis of brain gene expression profiles.
2004,
Pubmed
Wei,
A database of mRNA expression patterns for the sea urchin embryo.
2006,
Pubmed
,
Echinobase
Wray,
The evolution of embryonic patterning mechanisms in animals.
2000,
Pubmed
Yang,
PAML: a program package for phylogenetic analysis by maximum likelihood.
1997,
Pubmed
Zhang,
Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level.
2005,
Pubmed