High and distinct range-edge genetic diversity despite local bottlenecks

Abstract

The genetic consequences of living on the edge of distributional ranges have been the subject of a largely unresolved debate. Populations occurring along persistent low latitude ranges (rear-edge) are expected to retain high and unique genetic diversity. In contrast, currently less favourable environmental conditions limiting population size at such range-edges may have caused genetic erosion that prevails over past historical effects, with potential consequences on reducing future adaptive capacity. The present study provides an empirical test of whether population declines towards a peripheral range might be reflected on decreasing diversity and increasing population isolation and differentiation. We compare population genetic differentiation and diversity with trends in abundance along a latitudinal gradient towards the peripheral distribution range of Saccorhiza polyschides, a large brown seaweed that is the main structural species of kelp forests in SW Europe. Signatures of recent bottleneck events were also evaluated to determine whether the recently recorded distributional shifts had a negative influence on effective population size. Our findings show decreasing population density and increasing spatial fragmentation and local extinctions towards the southern edge. Genetic data revealed two well supported groups with a central contact zone. As predicted, higher differentiation and signs of bottlenecks were found at the southern edge region. However, a decrease in genetic diversity associated with this pattern was not verified. Surprisingly, genetic diversity increased towards the edge despite bottlenecks and much lower densities, suggesting that extinctions and recolonizations have not strongly reduced diversity or that diversity might have been even higher there in the past, a process of shifting genetic baselines.

Figure 1. Sampling scheme for S . polyschides (cells represent the sampling units) within 25 km cells along the study range, and for detailed northern-southern comparisons within sub-cells of 5 km.

Expected heterozygosity (H_E), allele number, coefficient of variation of density and mean density (values increase from right to left; North: white circles, Center: grey circles, South: black circles) plotted against latitude (decimal degrees at WGS84). R-squared and p-values for linear models (dashed lines) fitted for sites with density records and genetic samples.

Figure 2. Historical distribution of S . polyschides based on surveys (2008 and 2010) and literature records (only comparable sites are shown; Open circle: presence, Black circle: absence).

Habitat availability shown in black (Rocky reef; data from Portuguese sedimentary charts [70]) along the coast for depths above 20 m (the observed depth distribution of S . polyschides [92]). Genetic subdivision of S . polyschides based on STRUCTURE. The proportions of individual multilocus genotypes assigned to K=3 virtual clusters are indicated by the colours. Standardized allele richness (Std A), Mean F _ST, Mean Jost’s D and number of unique alleles per genetic group.

Figure 3. Isolation by distance of S . polyschides .

Estimates of pairwise genetic differentiation (F _ST/(1-F _ST)) plotted against pairwise minimum site distance in kilometres for (i) northern sites (white circles), (ii) central sites (grey circles) and (iii) southern sites (black circles). Mantel non-parametric tests based on 1x10⁵ permutations between pairwise genetic differentiation and pairwise site distance.