Sunday JM and Hart MW (2013), Sea star populations diverge by positive select...

ECB-ART-42805

Ecol Evol 2013 Mar 01;33:640-54. doi: 10.1002/ece3.487.

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Sea star populations diverge by positive selection at a sperm-egg compatibility locus.

Sunday JM , Hart MW .

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Fertilization proteins of marine broadcast spawning species often show signals of positive selection. Among geographically isolated populations, positive selection within populations can lead to differences between them, and may result in reproductive isolation upon secondary contact. Here, we test for positive selection in the reproductive compatibility locus, bindin, in two populations of a sea star on either side of a phylogeographic break. We find evidence for positive selection at codon sites in both populations, which are under neutral or purifying selection in the reciprocal population. The signal of positive selection is stronger and more robust in the population where effective population size is larger and bindin diversity is greater. In addition, we find high variation in coding sequence length caused by large indels at two repetitive domains within the gene, with greater length diversity in the larger population. These findings provide evidence of population-divergent positive selection in a fertilization compatibility locus, and suggest that sexual selection can lead to reproductive divergence between conspecific marine populations.

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Species referenced: Echinodermata
Genes referenced: bindin LOC100887844 LOC115925415 LOC577694

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	Figure 1. (a) Schematic diagram of bindin gene organization and coding sequence structure. (a) Main diagram (above) shows the 914-amino acid haplotype with the modal number of collagen-like copies and tandem repeats. Insets below show the extra collagen-like copy with 3' flanking region, and the extra tandem repeat, each found only once in our sample. Rectangles with solid black and grey borders show tandem repeat copies that are present in all alleles, dashed rectangles show tandem repeats that vary in copy number among alleles. Asterisk shows location of the single recombination site at codon site 855, black triangle denotes the 1285 bp intron at codon site 856, and solid black rectangle denotes the 135 bp invariant core. Colors in sequence are the default colors used in Se-al (v.2.0) (cyan = H, R, K; magenta = G, P, T, A, S; black = E, Q, D, N; green = L, V, M, I; blue = Y). (b) Map of study region and location of two main population samples. Dashed gray line represents location of phylogeographic break identified by Keever et al. (2009).
	Figure 2. Summary of bindin diversity across sampled populations.
	Figure 3. Consensus Bayesian gene tree and gene alignment for the first recombinant region of the bindin gene in Patiria miniata. The gene tree is annotated with the 11 codon sites under positive selection. Circled numbers refer to codon sites described in Table 1. Gray circles represent reversals. Two other differences are also annotated on the tree – the addition of two 18 bp inserts, which distinguishes the paraphyletic groups 1 and 2, and a single, but common synonymous transversion, which most members of haplotype group b share. Uncircled numbers above major clades denote Bayesian posterior probability of partition. Gaps in the gene alignment shows variation in repeat units, gray tone in sequences represents amino acid identity (light gray = H, R, K, G, P, T, A, S; dark gray = E, Q, D, N, L, V, M, I, Y), and letters a–d to the right indicate repeat-number variants that occurred multiple times (and are emphasized in the main text).
	Figure 4. Neighbor-joining gene trees from alignments of (a) collagen-like copies and (b) tandem repeats across 44 individuals. In both, clades of repeat units match their location in the gene by number and color. In the collagen-like copy alignment (a), the location of repeat unit 2b is noted with a pink arrowhead, and the two copies of repeat unit 2 from Bamfield that show conversion with other copies (BA-2) are highlighted. In (b) the three tandem repeats that show partial or full gene conversion are highlighted (two from Alaska: AK-9; one from Bamfield: BA-1).
	Figure 5. Site-by-site probability of positive selection, and location of indels, in the first exon of bindin in Patiria miniata. Peaks show for each codon the Bayes-empirical-Bayes estimate of the posterior probability of belonging to the positively selected class of sites (with ω > 1) and high rates of amino acid substitution along the foreground branches from the maximum-likelihood analysis. (a) Results with the Bamfield population in the foreground, (b) results with the Sandspit population in the foreground, both using the most visited tree from the posterior distribution of most likely gene trees generated by the MrBayes analysis (for results from other gene trees, see Fig. S1). Height of the curve shows the probability dN/dS >1 for each site along the length (x-axis) of the first recombinant region. Gray bands show the 95% probability range. Numbered peaks indicate sites with >95% probability dN/dS >1. (c) Distribution of indels.

References [+] :

Biermann, Geographic divergence of gamete recognition systems in two species in the sea urchin genus Strongylocentrotus. 2000, Pubmed, Echinobase