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

Journal article
Authors J. C. B. Nunez
P. A. Flight
K. B. Neil
S. Rong
Leif A Eriksson
D. A. Ferranti
Magnus Alm Rosenblad
Anders Blomberg
D. M. Rand
Published in Proceedings of the National Academy of Sciences of the United States of America
Volume 117
Issue 10
Pages 5376-5385
ISSN 0027-8424
Publication year 2020
Published at Department of Chemistry and Molecular Biology
Pages 5376-5385
Language en
Links dx.doi.org/10.1073/pnas.1918232117
Keywords population genetics, ecological genomics, balancing selection, barnacles, Semibalanus balanoides, northern acorn barnacle, balancing selection, semibalanus-balanoides, drosophila-melanogaster, physiological stress, genetic-structure, local, adaptation, spatial scale, polymorphism, mpi, Science & Technology - Other Topics
Subject categories Ecology, Genetics

Abstract

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 fre-quencies across Atlantic intertidal zones due to selection on post-settlement survival (i.e., allele zonation). We present the complete gene sequence of the Mpi locus and quantify nucleotide polymor-phism 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 allo-zyme classes correspond to two haplogroups with multiple internal haplotypes. The locus shows several footprints of balancing selec-tion 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 diver-gence, as well as a site frequency spectrum enriched for midfre-quency mutations. We observe other departures from neutrality across the locus in both coding and noncoding regions. These in-clude 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 heteroge-neous selection on Mpi.

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