Abstract
The marine copepod Tigriopus californicus lives in intertidal rock pools along the Pacific coast, where it exhibits strong, temporally stable population genetic structure. Previous allozyme surveys have found high frequency private alleles among neighboring subpopulations, indicating that there is limited genetic exchange between populations. Here we evaluate the factors responsible for the diversification and maintenance of alleles at the phosphoglucose isomerase (Pgi) locus by evaluating patterns of nucleotide variation underlying previously identified allozyme polymorphism. Copepods were sampled from eleven sites throughout California and Baja California, revealing deep genetic structure among populations as well as genetic variability within populations. Evidence of recombination is limited to the sample from Pescadero and there is no support for linkage disequilibrium across the Pgi locus. Neutrality tests and codon-based models of substitution suggest the action of natural selection due to elevated non-synonymous substitutions at a small number of sites in Pgi. Two sites are identified as the charge-changing residues underlying allozyme polymorphisms in T. californicus. A reanalysis of allozyme variation at several focal populations, spanning a period of 26 years and over 200 generations, shows that Pgi alleles are maintained without notable frequency changes. Our data suggest that diversifying selection accounted for the origin of Pgi allozymes, while McDonald-Kreitman tests and the temporal stability of private allozyme alleles suggests that balancing selection may be involved in the maintenance of amino acid polymorphisms within populations.
Highlights
There is considerable interest in quantifying adaptive variation among naturally occurring populations [1] and using this information in the management of populations [2], prospecting for adaptive variation in unknown genomes often requires considerable resources [3] or long-term experimental studies [4]
We investigate whether (1) natural selection has contributed to the origin of genetic polymorphism among divergent lineages, and (2) what processes are maintaining genetic variation at the phosphoglucose isomerase (Pgi) locus
Based on previous observations of sharp population structure [12,14,18], stability of allele frequencies through time [13], and evidence of adaptive variation in other arthropods [11], we set out to examine whether allozyme polymorphism observed at Pgi in Tigriopus californicus provided evidence of natural selection
Summary
There is considerable interest in quantifying adaptive variation among naturally occurring populations [1] and using this information in the management of populations [2], prospecting for adaptive variation in unknown genomes often requires considerable resources [3] or long-term experimental studies [4]. Phosphoglucose isomerase (Pgi, E.C. 5.3.1.9, known as glucose-6-phosphate isomerase) frequently exhibits polymorphism in natural populations and has been linked with natural selection in several taxa [6,7,8,9,10]. This has led Wheat [11] to argue that Pgi could be a useful candidate gene for studying adaptive genetic variation in a variety of arthropods. While Pgi variability in each population is not exceptional, the fact that variation is maintained when local populations are subject to fluctuations in population density due to their ephemeral tidepool habitat [15] suggests that Pgi polymorphism might be maintained by selection
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