Rise of oceanographic barriers in continuous populations of a cetacean: the genetic structure of harbour porpoises in Old World waters

Abstract

Background: Understanding the role of seascape in shaping genetic and demographic population structure is highly challenging for marine pelagic species such as cetaceans for which there is generally little evidence of what could effectively restrict their dispersal. In the present work, we applied a combination of recent individual-based landscape genetic approaches to investigate the population genetic structure of a highly mobile extensive range cetacean, the harbour porpoise in the eastern North Atlantic, with regards to oceanographic characteristics that could constrain its dispersal.

Results: Analyses of 10 microsatellite loci for 752 individuals revealed that most of the sampled range in the eastern North Atlantic behaves as a 'continuous' population that widely extends over thousands of kilometres with significant isolation by distance (IBD). However, strong barriers to gene flow were detected in the south-eastern part of the range. These barriers coincided with profound changes in environmental characteristics and isolated, on a relatively small scale, porpoises from Iberian waters and on a larger scale porpoises from the Black Sea.

Conclusion: The presence of these barriers to gene flow that coincide with profound changes in oceanographic features, together with the spatial variation in IBD strength, provide for the first time strong evidence that physical processes have a major impact on the demographic and genetic structure of a cetacean. This genetic pattern further suggests habitat-related fragmentation of the porpoise range that is likely to intensify with predicted surface ocean warming.

Figure 1

Bathymetric map of the eastern North Atlantic showing the approximate geographic sampled locations and sample sizes per location. Geographic locations are based on GPS coordinates or reported discovery location. The bar scales delimit the latitudinal range of the three spatial scales considered for the analyses of the North Atlantic (NAt) cluster: the global scale (1); the middle scale, south (2A), and north (2B) parts; and the small scale, the south (3A), middle (3B), and north (3C) parts. The map is projected using a gnomonic projection centred on the sampling centroid (scale units in km).

Figure 2

Estimated number of populations from Structure (a and b) and Geneland (c and d) analyses. Structure analyses: (a) mean (± SD) probabilities of the data [LnPr(X|K)] over 10 Structure replicated runs plotted as a function of the putative number of clusters (K). (b) Mean variations of probabilities of the data (Δ(LnPr(X|K)) between successive K considered in Structure analyses. For K clusters, this variation is calculated as Δ(LnPr(X|K))=LnPr(X|K)_k+1-LnPr(X|K)_k. Geneland analyses: posterior density distribution of the number of clusters estimated from Geneland analysis in 7 out of 10 replicates (c) and in the 3 remaining trials (d).

Figure 3

Estimated population structure from Structure analyses for K = 2 to K = 5. Each individual is represented by a thin horizontal line divided into K coloured segments that represent the individual's estimated membership fractions in K clusters. Black lines separate individuals from different geographic areas labelled on the right. Each plot, produced with Distruct [79], is based on the highest-probability run (of ten) at that value of K. Individuals are arranged based on their origins and sorted with increasing latitude.

Figure 4

Estimated population structure from Geneland analyses for the two modal solutions K = 3 and K = 4. Each individual is represented by a thin horizontal line divided into K coloured segments that represent the individual's estimated membership fractions in K clusters. Black lines separate individuals from different geographic areas labelled on the right. Each plot, produced with Distruct [79], is based on the highest-probability run at that value of K. Individuals are arranged based on their origins and sorted with increasing latitude.

Figure 5

Maps of Geneland individual assignments to clusters for K = 4 (scale units in km). The three plots represent the assignment of pixels to each cluster: (a) Black Sea cluster; (b) Iberian cluster; and (c) North Atlantic cluster. The assignments of pixels to the fourth cluster are not shown, as no individuals are assigned to it ("ghost cluster", see text for further details). The highest membership values are in light yellow and the level curves illustrate the spatial changes in assignment values. The plot is based on the highest-probability run at that value of K.

Figure 6

Genetic and geographic distance for pairs of sampled geographic areas. Yellow triangles indicate comparison between pairs of sampled localities within the same cluster; blue squares indicate pairs with one sampled locality in the NAt cluster and the IB cluster; red diamonds indicate pairs with one sampled locality in the NAt cluster and the BS cluster; and black circle indicate the comparison between the IB and the BS cluster.

Figure 7

Climatological (1997–2006) annual sea surface chlorophyll concentrations. Data obtained with Sea-viewing Wide Field-of-view Sensor (SeaWIFS, modified from [80]).