Geyer LB et al. (2020), Slow evolution under purifying selection in the...

ECB-ART-49779

Sci Rep 2020 Jun 17;101:9834. doi: 10.1038/s41598-020-66390-2.

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Slow evolution under purifying selection in the gamete recognition protein bindin of the sea urchin Diadema.

Geyer LB , Zigler KS , Tiozzo S , Lessios HA .

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Bindin is a sperm protein that mediates attachment and membrane fusion of gametes. The mode of bindin evolution varies across sea urchin genera studied to date. In three genera it evolves under positive selection, in four under mostly purifying selection, and in one, results have been mixed. We studied bindin evolution in the pantropical sea urchin Diadema, which split from other studied genera 250 million years ago. We found that Diadema bindin is structurally similar to that of other genera, but much longer (418 amino acids). In seven species of Diadema, bindin evolves under purifying selection, more slowly than in any other sea urchin genus. Only bindin of the recently rediscovered D. clarki shows evidence of positive selection. As D. clarki is sympatric with D. setosum and D. savignyi, positive selection could arise from avoidance of maladaptive hybridization. However, D. setosum and D. savignyi overlap in the Indo-West Pacific, yet their bindins show no evidence of positive selection, possibly because the two species spawn at different times. Bindin in the East Pacific D. mexicanum, the West Atlantic D. antillarum, the East Atlantic D. africanum, and the Indo-Pacific D. paucispinum also evolves slowly under purifying selection.

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	Figure 1. Gene genealogy of Diadema bindin first exon alleles. The tree was constructed using MrBayes and rooted on an allele of Echinothrix diadema. Numbers above the branches indicate Bayesian confidence estimates. Branches with less than 0.70 support were collapsed. Numbers below the branches indicate bootstrap support from GARLI maximum likelihood analysis; bootstrap support of less than 60% is not shown. Numbers on the terminal branches indicate the individual from which an allele came, then, after the period, the identity of the allele. For homozygous individuals, only one allele is shown. Species codes: D.afr: Diadema africanum, D. ant: D. antillarum, D.p-a: D. paucispinum-a (as in Lessios et al.33), D.p-b: D.paucispinum-b, D.sav: D. savignyi, D.mex: D. mexicanum, D.cla: D. clarki, D.pal: D. palmeri, D.s-a: D. setosum-a (as in Lessios et al.33), D.s-b: D. setosum-b. Transitions between amino acids identified by MEME as being under positive selection are marked along the branches by showing the amino acid positions in their alignment (Supplementary Fig. S1), and the identity of the amino acids.
	Figure 2. Gene genealogy of entire mature bindin alleles of Diadema. The tree was constructed using MrBayes and was rooted on an allele of Echinothrix diadema. Numbers above the branches indicate Bayesian confidence estimates. Branches with less than 0.70 support were collapsed. Numbers below the branches indicate bootstrap support from GARLI maximum likelihood analysis; bootstrap support of less than 60% is not shown. Numbers on the terminal branches indicate the individual from which an allele came, then, after the period, the identity of the allele. For homozygous individuals, only one allele is shown. Species codes: D.afr: Diadema africanum, D.ant: D. antillarum, D.p-a: D. paucispinum-a (as in Lessios et al.33), D.p-b: D.paucispinum-b, D.sav: D. savignyi, D.mex: D. mexicanum, D.cla: D. clarki. Transitions between amino acids about which FEL and FUBAR agree that they are under positive selection are marked along the branches by showing the amino acid position (Supplementary. S2), and the identity of the amino acids.
	Figure 3. Codons under negative (below horizontal line) and positive (above horizontal line) selection in the entire bindin molecule of Diadema based on tests FEL, SLAC, FUBAR and MEME of program HyPhy61 applied to bindin alleles of all species of Diadema. Amino acid positions along the length of the mature protein (Supplementary Fig. S1 & S2) are marked on the horizontal axis. The dotted vertical line marks the position of the intron. The lightly shaded region indicates the position of the conserved core of bindin, and the dark shading indicates the highly conserved B18 region100 of the core.

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