A legacy of contrasting spatial genetic structure on either side of the Atlantic-Mediterranean transition zone in a marine protist

Abstract

The mechanisms that underpin the varied spatial genetic structures exhibited by free-living marine microorganisms remain controversial, with most studies emphasizing a high dispersal capability that should redistribute genetic diversity in contrast to most macroorganisms whose populations often retain a genetic signature of demographic response to historic climate fluctuations. We quantified the European phylogeographic structure of the marine flagellate Oxyrrhis marina and found a marked difference in spatial genetic structure, population demography, and genetic diversity between the northwest Atlantic and Mediterranean Sea that reflects the persistent separation of these regions as well as context-dependent population responses to contrasting environments. We found similar geographic variation in the level of genetic diversity in the sister species Oxyrrhis maritima. Because the capacity for wide dispersal is not always realized, historic genetic footprints of range expansion and contraction persist in contemporary populations of marine microbes, as they do in larger species. Indeed, the well-described genetic effects of climatic variation on macroorganisms provide clear, testable hypotheses about the processes that drive genetic divergence in marine microbes and thus about the response to future environmental change.

Fig. 1.

Sampling locations (n = 149) and distribution of the main clades of O. marina and O. maritima from the European seascape. For O. marina colors indicate clade/model cluster: blue, clade 1; yellow, clade 2a; red, clade 2b. For O. maritima (gray symbols) triangles indicate clade 3, and stars indicate clade 4. Open circles are locations that were sampled but did not contain Oxyrrhis. Red lines denote boundaries between the four main regions (the Siculo-Tunisian strait, the Strait of Gibraltar, and Cape Finisterre). Dashed black lines indicate the boundaries used to define the 12 populations (gray numbers) used for rarefaction analysis of haplotype diversity.

Fig. 2.

Majority rule consensus Bayesian phylogenetic tree of European Oxyrrhis isolates based on a concatenated alignment of three gene fragments (5.8S ITS rDNA, COI, and α-tubulin; total alignment length 1,338 bp). Node labels are posterior probabilities based on 10⁶ permutations. Branch labels indicate the sample size (number of haplotypes) as the first number in branch label, followed by a three-letter location code and the country of origin. Clades for O. marina are synonymous with model clusters from the Structure analysis (Fig. 4).

Fig. 3.

Calibrated COI phylogenetic tree for European Oxyrrhis isolates based on a sequence substitution rate of 0.01 substitutions per million years. Errors for each dated node are upper and lower 95% posterior densities. MSC, Messinian Salinity Crisis; LP, Late Pleistocene glaciations; LGM, Last Glacial Maximum.

Fig. 4.

Structure plot for K = three model clusters for samples of O. marina. Each isolate of O. marina is depicted by a vertical line that is partitioned into K colored sections (colors as in Fig. 1). The length of each section is proportional to the estimated membership coefficient (Q_ind) of each cluster. Clusters are synonymous with clades (Fig.1): cluster 1 (blue) is equivalent to clade 1, cluster 2a (yellow) is equivalent to clade 2a, and cluster 2b (red) is equivalent to clade 2b.