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Maximum-likelihood models of codon substitution were used to test for positive Darwinian selection at the vesicle protein pantophysin in two allelic lineages segregating in the Atlantic cod Gadus morhua and in 18 related species of marine gadid fishes. Positive selection was detected in the two intravesicular loops of the integral membrane protein but not in four membrane-spanning regions or the 3' cytoplasmic tail. The proportion of positively selected sites (24.9%) and the mean nonsynonymous/synonymous rate ratio (omega = d(N)/d(S) = 5.35) were both greater in the first intravesicular (IV1) domain compared with the second intravesicular (IV2) domain (11.0% positively selected sites with mean omega = 3.76). Likelihood ratio tests comparing models that assume identical omega ratios along all branches of the phylogeny to those that allow omega ratios to vary among lineages were not significant for either the IV1 or IV2 domains, indicating that the selective pressures favoring amino acid replacements have operated consistently in both regions during the diversification of the group. Positive selection was observed in the IV1 domain in both G. morhua allelic lineages, and, although three of the four codons that differ between alleles were targets of positive selection in the broader group, no similar polymorphisms were detected in other taxa. The two G. morhua Pan I alleles appeared to have evolved before the speciation event separating it from its sister taxon, Theragra chalcogramma, and on the basis of a standard mtDNA clock are estimated to be at least 2 Myr old. Although the function of pantophysin remains unknown, the strong signal of positive selection at specific sites in the IV1 and IV2 domains may help clarify its role in cellular trafficking pathways.

Genetic isolation by distance (IBD) has rarely been described in marine species with high potential for dispersal at both the larval and adult life-history stages. Here, we report significant relationships between inferred levels of gene flow and geographic distance in the Atlantic cod, Gadus morhua, at 10 nuclear restriction-fragment-length-polymorphism (RFLP) loci at small regional scales in the western north Atlantic region (< 1,600 km) that mirror those previously detected over its entire geographic range (up to 7,300 km). Highly significant allele frequency differences were observed among eight northwestern Atlantic populations, although the mean FST for all 10 loci was only 0.014. Despite this weak population structuring, the distance separating populations explained between 54% and 62% of the variation in gene flow depending on whether nine or 10 loci were used to estimate Nm. Across the species' entire geographic range, highly significant differences were observed among six regional populations at nine of the 10 loci (mean FST = 0.068) and seven loci exhibited significant negative relationships between gene flow and distance. At this large geographic scale, natural selection acting in the vicinity of one RFLP locus (GM798) had a significant effect on the correlation between gene flow and distance, and eliminating it from the analysis caused the coefficient of determination to increase from 17% to 62%. The role of vicariance was assessed by sequentially removing populations from the analysis and was found to play a minor role in contributing to the relationship between gene flow and distance at either geographic scale. The correlation between gene flow and distance detected in G. morhua at small and large spatial scales suggests that dispersal distances and effective population sizes are much smaller than predicted for the species and that the recent age of populations, rather than extensive gene flow, may be responsible for its weak population structure. Our results suggest that interpreting limited genetic differences among populations as reflecting high levels of ongoing gene flow should be made with caution.

High levels of gene flow have been implicated in producing uniform patterns of allozyme variation among populations of many marine fish species. We have examined whether gene flow is responsible for the limited population structure in the Atlantic cod, Gadus morhua L., by comparing the previously published patterns of variation at 10 allozyme loci to 17 nuclear restriction fragment length polymorphism (RFLP) loci scored by 11 anonymous cDNA clones. Unlike the allozyme loci, highly significant differences were observed among all populations at the DNA markers in a pattern consistent with an isolation-by-distance model of population structure. The magnitude of allele frequency variation at the nuclear RFLP loci significantly exceeded that observed at the protein loci (chi 2 = 24.6, d.f. = 5, P < 0.001). Estimates of gene flow from the private alleles method were similar for the allozymes and nuclear RFLPs. From the infinite island model, however, estimates of gene flow from the DNA markers were fivefold lower than indicated by the proteins. The discrepancy between gene flow estimates, combined with the observation of a large excess of rare RFLP alleles, suggests that the Atlantic cod has undergone a recent expansion in population size and that populations are significantly displaced from equilibrium. Because gene flow is a process that affects all loci equally, the heterogeneity observed among populations at the DNA level eliminates gene flow as the explanation for the homogeneous allozyme patterns. Our results suggest that a recent origin of cod populations has acted to constrain the extent of population differentiation observed at weakly polymorphic loci and implicate a role for selection in affecting the distribution of protein variation among natural populations in this species.