Asymmetric gene flow and the evolutionary maintenance of genetic diversity in small, peripheral Atlantic salmon populations

Abstract

Small populations may be expected to harbour less genetic variation than large populations, but the relation between census size (N), effective population size (N e), and genetic diversity is not well understood. We compared microsatellite variation in four small peripheral Atlantic salmon populations from the Iberian peninsula and three larger populations from Scotland to test whether genetic diversity was related to population size. We also examined the historical decline of one Iberian population over a 50-year period using archival scales in order to test whether a marked reduction in abundance was accompanied by a decrease in genetic diversity. Estimates of effective population size (N e) calculated by three temporal methods were consistently low in Iberian populations, ranging from 12 to 31 individuals per generation considering migration, and from 38 to 175 individuals per generation if they were regarded as closed populations. Corresponding N e/N ratios varied from 0.02 to 0.04 assuming migration (mean=0.03) and from 0.04 to 0.18 (mean=0.10) assuming closed populations. Population bottlenecks, inferred from the excess of heterozygosity in relation to allelic diversity, were detected in all four Iberian populations, particularly in those year classes derived from a smaller number of returning adults. However, despite their small size and declining status, Iberian populations continue to display relatively high levels of heterozygosity and allelic richness, similar to those found in larger Scottish populations. Furthermore, in the R. Asón no evidence was found for a historical loss of genetic diversity despite a marked decline in abundance during the last five decades. Thus, our results point to two familiar paradigms in salmonid conservation: (1)␣endangered populations can maintain relatively high levels of genetic variation despite their small size, and (2) marked population declines may not necessarily result in a significant loss of genetic diversity. Although there are several explanations for such results, microsatellite data and physical tagging suggest that high levels of dispersal and asymmetric gene flow have probably helped to maintain genetic diversity in these peripheral populations, and thus to avoid the negative consequences of inbreeding.