Divergence within and among Seaweed Siblings (Fucus vesiculosus and F. radicans) in the Baltic Sea

Abstract

Closely related taxa provide significant case studies for understanding evolution of new species but may simultaneously challenge species identification and definition. In the Baltic Sea, two dominant and perennial brown algae share a very recent ancestry. Fucus vesiculosus invaded this recently formed postglacial sea 8000 years ago and shortly thereafter Fucus radicans diverged from this lineage as an endemic species. In the Baltic Sea both species reproduce sexually but also recruit fully fertile new individuals by asexual fragmentation. Earlier studies have shown local differences in morphology and genetics between the two taxa in the northern and western Bothnian Sea, and around the island of Saaremaa in Estonia, but geographic patterns seem in conflict with a single origin of F. radicans. To investigate the relationship between northern and Estonian distributions, we analysed the genetic variation using 9 microsatellite loci in populations from eastern Bothnian Sea, Archipelago Sea and the Gulf of Finland. These populations are located in between earlier studied populations. However, instead of bridging the disparate genetic gap between N-W Bothnian Sea and Estonia, as expected from a simple isolation-by-distance model, the new populations substantially increased overall genetic diversity and showed to be strongly divergent from the two earlier analysed regions, showing signs of additional distinct populations. Contrasting earlier findings of increased asexual recruitment in low salinity in the Bothnian Sea, we found high levels of sexual reproduction in some of the Gulf of Finland populations that inhabit extremely low salinity. The new data generated in this study supports the earlier conclusion of two reproductively isolated but very closely related species. However, the new results also add considerable genetic and morphological complexity within species. This makes species separation at geographic scales more demanding and suggests a need for more comprehensive approaches to further disentangle the intriguing relationship and history of the Baltic Sea fucoids.

Fig 1. Proportions of unique and clonal ramets in Baltic Sea Fucus vesiculosus and F. radicans populations.

Unique genotypes are sexually recruited or rare clones. Clonal ramets are all asexually recruited. Salinities are indicated in Practical Salinity Units. F. vesiculosus populations are marked in red and italic letters, F. radicans in green and regular letters, and four unassigned populations (see text) are marked in blue and underlined letters. Populations of the two species having the same letters are sympatric.

Fig 2. Principal component analysis separating populations based on microsatellite allele frequency distributions.

(A) All populations analysed together, including 12 of F. vesiculosus (circles), 13 of F. radicans (squares), and 4 unassigned (triangles). Colours indicate different regions (blue = North Sea; green = Baltic Proper; white = Estonian coast; purple = north Bothnian Sea; red = west Bothnian Sea; yellow = east Bothnian Sea; grey = Archipelago Sea and black = Gulf of Finland). Populations with the same letter are sympatric. Analysis was done on genet level with 10,000 randomizations. The overall F_ST is 0.19, which indicates a highly significant genetic structure (p = 0.0001). (B) Same populations as in (A) but the more divergent populations (N, O, P, Q and V) removed to better resolve the relationship between the remaining populations.

Fig 3. STRUCTURE analyses of five pairs of sympatric Fucus populations.

Populations D1, E1, F1, V1 and W1 are F. radicans while D2, E2, F2, V2 and W2 are F. vesiculosus. Analyses are based on genetic variation in 9 microsatellite loci. Vertical bars indicate assignment probability for each genet to any of two genetic groups (K = 2). Left side of the panel are analyses with the software option LOCPRIOR, while right side are without LOCPRIOR.

Fig 4. STRUCTURE analyses of Finnish, Russian and Estonian Fucus populations.

Populations J, K, L, M, V1, W1 and X are F. radicans and N, O, P, Q, V2, W2 and Y are Fucus vesiculosus. Populations R, S, T and U were not possible to clearly assigned to species based on morphological criteria. All analyses are based on genetic variation in 9 microsatellite loci. Colour of vertical bars indicate individual genet assignment probabilities to any of five genetic groups (K = 5, which was supported by values of Pr (X|K, not shown). Black vertical lines separate the different populations.

Fig 5. Directional relative migration network of Finnish, Russian and Estonian Fucus populations.

Species and areas are designated the same symbols and colours as in Fig 2. Population positions indicate relatedness from the perspective of gene flow. Arrows indicate the direction of gene flow, and numbers (and arrow shading/thickness) show the values of directional migration relative to the highest value in the analysis (in this case from population J to population K).