Popovic I et al. (2014), Selection and demographic history shape the mol...

ECB-ART-43476

Ecol Evol 2014 May 01;49:1567-88. doi: 10.1002/ece3.1042.

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Selection and demographic history shape the molecular evolution of the gamete compatibility protein bindin in Pisaster sea stars.

Popovic I , Marko PB , Wares JP , Hart MW .

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Reproductive compatibility proteins have been shown to evolve rapidly under positive selection leading to reproductive isolation, despite the potential homogenizing effects of gene flow. This process has been implicated in both primary divergence among conspecific populations and reinforcement during secondary contact; however, these two selective regimes can be difficult to discriminate from each other. Here, we describe the gene that encodes the gamete compatibility protein bindin for three sea star species in the genus Pisaster. First, we compare the full-length bindin-coding sequence among all three species and analyze the evolutionary relationships between the repetitive domains of the variable second bindin exon. The comparison suggests that concerted evolution of repetitive domains has an effect on bindin divergence among species and bindin variation within species. Second, we characterize population variation in the second bindin exon of two species: We show that positive selection acts on bindin variation in Pisaster ochraceus but not in Pisaster brevispinus, which is consistent with higher polyspermy risk in P. ochraceus. Third, we show that there is no significant genetic differentiation among populations and no apparent effect of sympatry with congeners that would suggest selection based on reinforcement. Fourth, we combine bindin and cytochrome c oxidase 1 data in isolation-with-migration models to estimate gene flow parameter values and explore the historical demographic context of our positive selection results. Our findings suggest that positive selection on bindin divergence among P. ochraceus alleles can be accounted for in part by relatively recent northward population expansions that may be coupled with the potential homogenizing effects of concerted evolution.

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Species referenced: Echinodermata
Genes referenced: bindin LOC100887844 LOC100893907 LOC577219 LOC577694 LOC581070

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	Figure 1. Collection sites for five Pisaster ochraceus and three Pisaster brevispinus populations sampled in this study are shown on the map on the right. Dashed lines represent the northern and southern range boundaries for P. brevispinus. Solid lines represent the range boundaries for P. ochraceus. Refer to Table 1 for exact localities and sample sizes. Bindin haplotype networks for (a) P. ochraceus and (b) P. brevispinus are shown on the left. Each circle represents a unique haplotype; the area of the circle is proportional to the frequency of the haplotype; colors show the proportion of each haplotype from different localities shown on the map. Each line between haplotypes represents one inferred mutational step, slashes indicate an additional mutation, and numbers within lines specify the number of additional mutational steps >3. Isolated haplotypes represent alleles that differed from the rest of the sample by insertionâ€“deletion differences and could not be connected to the rest of the haplotype network by nucleotide substitutions only.
	Figure 2. (a) Pisaster ochraceus bindin gene structure. (b) Inferred amino acid sequence for the full-length P. ochraceus bindin; the N-terminal preprobindin sequence and the C-terminal conserved core region are in boxes, and the furin-type cleavage site (RVRR) is in bold letters. Asterisks indicate splice sites for two introns. (c) Scaled diagram of repetitive domain structure variation in the second bindin exon for all three Pisaster species. Black regions represent nonrepetitive terminal sequences; collagen-like regions are shown in blue; A repeats are shown in dark green; B repeats are shown in light green and are absent in Pisaster giganteus.
	Figure 3. (a) Alignment of repeat domains in the second bindin exon for all three Pisaster species. (b) Consensus Bayesian genealogy of repetitive domains with Bayesian posterior probabilities of partition at branch nodes. â€œAâ€ and â€œBâ€ denote separate clades grouping repeat types A and B. Circles at branch tips are colored corresponding to species (see legend in panel a) and numbered corresponding to repeat number counted in the 5â€² to 3â€² direction.
	Figure 4. Variation in nucleotide diversity per base pair in sliding windows across the coding sequence for the second bindin exon for (a) Pisaster ochraceus and (b) Pisaster brevispinus populations (window length = 100; step size = 25).
	Figure 5. Consensus Bayesian genealogies of bindin alleles for (a) Pisaster ochraceus and (b) Pisaster brevispinus rooted with a single Pisaster giganteus bindin allele. The scale bar shows 0.4% sequence divergence. Numbers above branches represent Bayesian posterior probabilities of partition, and numbers below the branches denote bootstrap support of the maximum likelihood analysis from 1000 replicates. Red branches were inferred to be experiencing episodic diversifying selection with Ï‰ â‰« 1, using the branch-site random effects likelihood method implemented in HyPhy. Also refer to Tables 4 and 5 for additional tests of positive selection.

References [+] :

Biermann, The molecular evolution of sperm bindin in six species of sea urchins (Echinoida: Strongylocentrotidae). 1998, Pubmed, Echinobase