Ricardo T. Pereyra

Rapid speciation in a newly opened postglacial marine environment, the Baltic Sea.

BackgroundTheory predicts that speciation can be quite rapid. Previous examples comprise a wide range of organisms such as sockeye salmon, polyploid hybrid plants, fruit flies and cichlid fishes. However, few studies have shown natural examples of rapid evolution giving rise to new species in marine environments.ResultsUsing microsatellite markers, we show the evolution of a new species of brown macroalga (Fucus radicans) in the Baltic Sea in the last 400 years, well after the formation of this brackish water body ~8–10 thousand years ago. Sympatric individuals of F. radicans and F. vesiculosus (bladder wrack) show significant reproductive isolation. Fucus radicans, which is endemic to the Baltic, is most closely related to Baltic Sea F. vesiculosus among north Atlantic populations, supporting the hypothesis of a recent divergence. Fucus radicans exhibits considerable clonal reproduction, probably induced by the extreme conditions of the Baltic. This reproductive mode is likely to have facilitated the rapid foundation of the new taxon.ConclusionThis study represents an unparalleled example of rapid speciation in a species-poor open marine ecosystem and highlights the importance of increasing our understanding on the role of these habitats in species formation. This observation also challenges presumptions that rapid speciation takes place only in hybrid plants or in relatively confined geographical places such as postglacial or crater lakes, oceanic islands or rivers.

FREQUENT CLONALITY IN FUCOIDS (FUCUS RADICANS AND FUCUS VESICULOSUS; FUCALES, PHAEOPHYCEAE) IN THE BALTIC SEA(1).

Asexual reproduction by cloning may affect the genetic structure of populations, their potential to evolve, and, among foundation species, contributions to ecosystem functions. Macroalgae of the genus Fucus are known to produce attached plants only by sexual recruitment. Recently, however, clones of attached plants recruited by asexual reproduction were observed in a few populations of Fucus radicans Bergström et L. Kautsky and F. vesiculosus L. inside the Baltic Sea. Herein we assess the distribution and prevalence of clonality in Baltic fucoids using nine polymorphic microsatellite loci and samples of F. radicans and F. vesiculosus from 13 Baltic sites. Clonality was more common in F. radicans than in F. vesiculosus, and in both species it tended to be most common in northern Baltic sites, although variation among close populations was sometimes extensive. Individual clonal lineages were mostly restricted to single or nearby locations, but one clonal lineage of F. radicans dominated five of 10 populations and was widely distributed over 550 × 100 km of coast. Populations dominated by a few clonal lineages were common in F. radicans, and these were less genetically variable than in other populations. As thalli recruited by cloning produced gametes, a possible explanation for this reduced genetic variation is that dominance of one or a few clonal lineages biases the gamete pool resulting in a decreased effective population size and thereby loss of genetic variation by genetic drift. Baltic fucoids are important habitat‐forming species, and genetic structure and presence of clonality have implications for conservation strategies.

Genetic biodiversity in the Baltic Sea: species-specific patterns challenge management

Information on spatial and temporal patterns of genetic diversity is a prerequisite to understanding the demography of populations, and is fundamental to successful management and conservation of species. In the sea, it has been observed that oceanographic and other physical forces can constitute barriers to gene flow that may result in similar population genetic structures in different species. Such similarities among species would greatly simplify management of genetic biodiversity. Here, we tested for shared genetic patterns in a complex marine area, the Baltic Sea. We assessed spatial patterns of intraspecific genetic diversity and differentiation in seven ecologically important species of the Baltic ecosystem—Atlantic herring (Clupea harengus), northern pike (Esox lucius), European whitefish (Coregonus lavaretus), three-spined stickleback (Gasterosteus aculeatus), nine-spined stickleback (Pungitius pungitius), blue mussel (Mytilus spp.), and bladderwrack (Fucus vesiculosus). We used nuclear genetic data of putatively neutral microsatellite and SNP loci from samples collected from seven regions throughout the Baltic Sea, and reference samples from North Atlantic areas. Overall, patterns of genetic diversity and differentiation among sampling regions were unique for each species, although all six species with Atlantic samples indicated strong resistence to Atlantic-Baltic gene-flow. Major genetic barriers were not shared among species within the Baltic Sea; most species show genetic heterogeneity, but significant isolation by distance was only detected in pike and whitefish. These species-specific patterns of genetic structure preclude generalizations and emphasize the need to undertake genetic surveys for species separately, and to design management plans taking into consideration the specific structures of each species.

Complex spatial clonal structure in the macroalgae Fucus radicans with both sexual and asexual recruitment.

Abstract In dioecious species with both sexual and asexual reproduction, the spatial distribution of individual clones affects the potential for sexual reproduction and local adaptation. The seaweed Fucus radicans, endemic to the Baltic Sea, has separate sexes, but new attached thalli may also form asexually. We mapped the spatial distribution of clones (multilocus genotypes, MLGs) over macrogeographic (>500 km) and microgeographic (<100 m) scales in the Baltic Sea to assess the relationship between clonal spatial structure, sexual recruitment, and the potential for natural selection. Sexual recruitment was predominant in some areas, while in others asexual recruitment dominated. Where clones of both sexes were locally intermingled, sexual recruitment was nevertheless low. In some highly clonal populations, the sex ratio was strongly skewed due to dominance of one or a few clones of the same sex. The two largest clones (one female and one male) were distributed over 100–550 km of coast and accompanied by small and local MLGs formed by somatic mutations and differing by 1–2 mutations from the large clones. Rare sexual events, occasional long‐distance migration, and somatic mutations contribute new genotypic variation potentially available to natural selection. However, dominance of a few very large (and presumably old) clones over extensive spatial and temporal scales suggested that either these have superior traits or natural selection has only been marginally involved in the structuring of genotypes.

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

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.

Phenotypic variation in sexually and asexually recruited individuals of the Baltic Sea endemic macroalga Fucus radicans: in the field and after growth in a common-garden

BackgroundMost species of brown macroalgae recruit exclusively sexually. However, Fucus radicans, a dominant species in the northern Baltic Sea, recruits new attached thalli both sexually and asexually. The level of asexual recruitment varies among populations from complete sexual recruitment to almost (> 90%) monoclonal populations. If phenotypic traits have substantial inherited variation, low levels of sexual activity will decrease population variation in these traits, which may affect function and resilience of the species. We assessed the level of inherited variation in nine phenotypic traits by comparing variation within and among three monoclonal groups and one group of unique multilocus genotypes (MLGs) sampled in the wild.ResultsOf the nine phenotypic traits, recovery after freezing, recovery after desiccation, and phlorotannin content showed substantial inherited variation, that is, phenotypic variation in these traits were to a large extend genetically determined. In contrast, variation in six other phenotypic traits (growth rate, palatability to isopod grazers, thallus width, distance between dichotomies, water content after desiccation and photochemical yield under ambient conditions) did not show significant signals of genetic variation at the power of analyses used in the study. Averaged over all nine traits, phenotypic variation within monoclonal groups was only 68% of the variation within the group of different MLGs showing that genotype diversity does affect the overall level of phenotypic variation in this species.ConclusionsOur result indicates that, in general, phenotypic diversity in populations of Fucus radicans increases with increased multilocus genotype (MLG) diversity, but effects are specific for individual traits. In the light of Fucus radicans being a foundation species of the northern Baltic Sea, we propose that increased MLG diversity (leading to increased trait variation) will promote ecosystem function and resilience in areas where F. radicans is common, but this suggestion needs experimental support.

Neutral processes forming large clones during colonization of new areas

In species reproducing both sexually and asexually clones are often more common in recently established populations. Earlier studies have suggested that this pattern arises due to natural selection favouring generally or locally successful genotypes in new environments. Alternatively, as we show here, this pattern may result from neutral processes during species’ range expansions. We model a dioecious species expanding into a new area in which all individuals are capable of both sexual and asexual reproduction, and all individuals have equal survival rates and dispersal distances. Even under conditions that favour sexual recruitment in the long run, colonization starts with an asexual wave. After colonization is completed, a sexual wave erodes clonal dominance. If individuals reproduce more than one season, and with only local dispersal, a few large clones typically dominate for thousands of reproductive seasons. Adding occasional long‐distance dispersal, more dominant clones emerge, but they persist for a shorter period of time. The general mechanism involved is simple: edge effects at the expansion front favour asexual (uniparental) recruitment where potential mates are rare. Specifically, our model shows that neutral processes (with respect to genotype fitness) during the population expansion, such as random dispersal and demographic stochasticity, produce genotype patterns that differ from the patterns arising in a selection model. The comparison with empirical data from a post‐glacially established seaweed species (Fucus radicans) shows that in this case, a neutral mechanism is strongly supported.

Isolation and characterization of nuclear microsatellite loci in the northern shrimp, Pandalus borealis

We developed and characterized 20 microsatellite primer loci for the northern shrimp Pandalusborealis. All 20 loci were polymorphic with number of alleles ranging from 3 to 36 and with observed heterozygosity between 0.04 and 0.93. In addition, we tested the utility of these markers in three related shrimp species, P. montagui, Atlantopandaluspropinqvus and Dichelopandalusbonnieri. These new markers will prove useful in the identification of stock structure and hence, assessment of the commercially important species P. borealis.