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Proc Natl Acad Sci U S A. 2020 Mar 10;117(10):5376-5385. doi: 10.1073/pnas.1918232117. Epub 2020 Feb 25.

Footprints of natural selection at the mannose-6-phosphate isomerase locus in barnacles.

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Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912;
Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02912.
Center for Computational Molecular Biology, Brown University, Providence, RI 02912.
Department of Chemistry and Molecular Biology, Lundberg Laboratory, University of Gothenburg, 405 30 Göteborg, Sweden.


The mannose-6-phosphate isomerase (Mpi) locus in Semibalanus balanoides has been studied as a candidate gene for balancing selection for more than two decades. Previous work has shown that Mpi allozyme genotypes (fast and slow) have different frequencies across Atlantic intertidal zones due to selection on postsettlement survival (i.e., allele zonation). We present the complete gene sequence of the Mpi locus and quantify nucleotide polymorphism in S. balanoides, as well as divergence to its sister taxon Semibalanus cariosus We show that the slow allozyme contains a derived charge-altering amino acid polymorphism, and both allozyme classes correspond to two haplogroups with multiple internal haplotypes. The locus shows several footprints of balancing selection around the fast/slow site: an enrichment of positive Tajima's D for nonsynonymous mutations, an excess of polymorphism, and a spike in the levels of silent polymorphism relative to silent divergence, as well as a site frequency spectrum enriched for midfrequency mutations. We observe other departures from neutrality across the locus in both coding and noncoding regions. These include a nonsynonymous trans-species polymorphism and a recent mutation under selection within the fast haplogroup. The latter suggests ongoing allelic replacement of functionally relevant amino acid variants. Moreover, predicted models of Mpi protein structure provide insight into the functional significance of the putatively selected amino acid polymorphisms. While footprints of selection are widespread across the range of S. balanoides, our data show that intertidal zonation patterns are variable across both spatial and temporal scales. These data provide further evidence for heterogeneous selection on Mpi.


Semibalanus balanoides; balancing selection; barnacles; ecological genomics; population genetics

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