Rapid speciation in a newly opened postglacial marine environment, the Baltic Sea
© Pereyra et al; licensee BioMed Central Ltd. 2009
Received: 21 November 2008
Accepted: 31 March 2009
Published: 31 March 2009
Theory 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.
Using 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.
This 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.
Speciation is one of the most fundamental processes in evolutionary biology. It is a process in which the within population variation transforms into distinguishable groups of individuals through the evolution of intrinsic reproductive barriers . The speed at which this process happens is still intriguing and controversial  but estimates of speciation rates generally show that 105–107 years (yrs) are needed for new species to evolve . However, theory predicts that speciation can happen more quickly -often called "contemporary" or "rapid evolution"-, particularly in new or extreme environmental conditions where selection for adaptation is strong [2, 4, 5]. Despite these theoretical expectations, the evidence of rapid speciation is primarily limited to classical evolutionary models such as cichlid fishes in discrete geographical spaces as a Nicaraguan crater lake  where competition is expected to be high and reproductive isolation is likely to occur within, or Hawaiian fauna  where the high number of species are more likely to drive speciation . Evidence is also provided from fruit flies under laboratory conditions , from homoploid and polyploid hybrid plants [10, 11] and from anadromous sockeye salmon in which some degree of reproductive isolation evolved after 13 generations . For marine species, support for rapid speciation derives from the "white" sticklebacks and although the evidence is consistent with a rapid species origin, the estimates of divergence time do not correspond with the glacial history of these systems . Hence, the rapid foundation of new species in the marine environment remains to be proven.
In the marine realm, genetic divergence between populations is expected to evolve relatively slowly as recruits and propagules are readily transported by ocean currents . Hitherto, time estimates for marine speciation events that agree with geological events confirm the expectations of slow speciation; for example, the reproductive isolation between sister lineages of marine shrimps was completed >3.5 million years ago (Mya) , after the rise of the Isthmus of Panama.
Results and discussion
Genetic variability among microsatellite loci examined
(n = 39)
(n = 117)
F. vesiculosus other populations
(n = 123)
Pairwise FST values of population differentiation
Phylogeographic affinities of F. radicans
We constructed a neighbour-joining tree based on Cavalli-Sforza genetic distances adding samples from one allopatric locality of F. radicans and one of F. vesiculosus from inside the Baltic, and three localities of F. vesiculosus from outside the Baltic (North Sea, Norwegian Sea and White Sea) (Fig. 2A). This analysis showed F. radicans emerging as a single monophyletic taxon derived from a F. vesiculosus lineage, but distinct from F. vesiculosus with high bootstrap support (Fig. 2C). The population tree indicated a close relationship between F. radicans and Gulf of Bothnia F. vesiculosus, suggesting that F. radicans recently diverged from this F. vesiculosus lineage. Further clustering of F. vesiculosus populations mainly corresponds to geographical designations and the genetic distances between them are in agreement with a previous study suggesting that this divergence reflects constrained gene flow even at small geographic scale .
Time of divergence
An alternative scenario to the hypothesis of recent speciation is that F. radicans may have originated outside the Baltic and entered the newly formed sea as a previously diverged lineage that remained differentiated (and became extinct outside the Baltic Sea). This scenario is weakened by our phylogeographic data: our neighbour-joining tree showed a close relationship of F. radicans with Baltic populations of F. vesiculosus that strongly supports an F. radicans origin within the Baltic. Yet, accurate times of speciation are difficult to estimate due to the lack of variation in sequence loci. Neither nuclear or mtDNA sequences were able to resolve the phylogenetic relationships between both taxa [17, 19, 21], further suggesting a recent origin of F. radicans. Consequently, we calculated a microsatellite-based estimate of time since divergence of F. radicans and F. vesiculosus using a coalescent approach. This analysis indicated that F. radicans and F. vesiculosus started to diverge from a common panmictic population sometime between 125 and 2475 yrs ago (95%HPD; posterior distribution peak at ~400 yrs ago, Fig. 5A). Hence, separation took place after the Baltic underwent the transition from marine to brackish water, less than 4 kya. The hypothesis that F. radicans arouse recently is further strengthened by the fact that it is endemic to the Baltic Sea.
We considered the mating system as a potential isolating mechanism between F. radicans and F. vesiculosus. Fucus vesiculosus has separate sexes and was until recently reported to reproduce exclusively sexually through external fertilization. Experiments show limited capacity of F. vesiculosus to reproduce in low salinities by reducing the longevity and motility of the gametes [22, 23], low fertilization success and egg polyspermy . However, asexual reproduction (20%) has also been reported in Baltic populations of F. vesiculosus . Likewise, F. radicans has permanent and well established populations in all its distributional range, with separate sexes and sexual reproduction taking place the same way as in F. vesiculosus. However, it shows high extent of clonality and re-attachment experiments in both species show that detached thallus fragments of F. radicans have considerably higher capacity to re-attach (80%) than those of F. vesiculosus (15%) .
Populations living in marginal environments typically switch or are capable of asexual reproduction , and this is also true for several species in the Baltic . Thus, the frequent clonal reproduction observed in F. radicans coupled with the low capacity of F. vesiculosus to reproduce sexual or asexually at low salinities may have facilitated the divergence between both taxa. The evolution of low-salinity tolerance might be seen as directional selection in F. radicans and F. vesiculosus. Clonality may have evolved through a single F. radicans individual successfully colonizing and producing a population in the hypo-saline environment or through reinforcement to reduce gene flow from F. vesiculosus populations not adapted to these conditions. In either case, reproductive isolation would appear as a by-product of adaptation.
The Baltic is an ecologically marginal and geographically peripheral marine habitat due to its permanent low salinity and geographic semi-isolation from the Atlantic. The salinity gradient from the inner Baltic to the North Sea spans an order of magnitude (3–30 psu), and has caused strong local adaptation in most of the marine lineages that survived the marine/brackish transition 4 kya . Directional selection is a strong promoter of speciation, even in the presence of gene flow [26–28]. More specifically, environmental stress along gradients has been highlighted as a potential source of new species . Although the exact mechanism of the F. vesiculosus – F. radicans speciation event remains unknown, the extreme environmental stress imposed by the brackish water environment of the Baltic has clearly contributed to the formation of the new species.
Fucus radicans is endemic to the Baltic Sea that formed only 8–10 kya. This species diverged from F. vesiculosus and divergence time estimates suggest that they split about 400 yrs ago. These dates are consistent with the transition of the Baltic from marine to brackish water, less than 4 kya and provide an unparalleled example of rapid speciation in marine ecosystems. These closely related species also offer further opportunities to increase our understanding of the role of species-poor systems -where competition is low and gene flow is expected to be high-, of peripheral extreme environments and of mixed reproductive modes in species formation.
Individuals of F. radicans and F. vesiculosus were collected from four different areas along the Swedish coast. The area of Öregrund (SW Gulf of Bothnia) included four sites in which the distributional ranges of both species overlap and individual plants occur in sympatry (Figs. 1, 2A and 2C). The following additional sites were also included: one sampling site at Järnäs (NW Gulf of Bothnia) where only F. radicans is found; Öregrund (OB, F. vesiculosus, n = 37, Fig. 2C); Öland (n = 43, Baltic) and Lysekil (n = 42, Swedish west coast) where only F. vesiculosus occurs. Two further populations of F. vesiculosus were sampled from Norway (n = 20) and the White Sea (n = 18) for use as outgroups. Total number of unique genotypes used for the analyses is provided in table 1.
DNA was extracted from dried algal tissue using DNeasy Plant MiniKit and samples were genotyped at nine microsatellites developed from Fucus species [30, 31]. Labelled products were poolplexed and resolved on a Beckman-Coulter automated sequencer and CeqMan 8000 software (Beckman-Coulter) was used for allele sizing.
For each species, the probability of identity of genotypes was calculated to distinguish between clones and identical genotypes by chance using GIMLET http://pbil.univ-lyon1.fr/software/Gimlet/gimlet%20frame1.html. The individuals representing clones were removed for all subsequent analyses. Allele variation and genetic diversity were obtained with POP100GENE http://www.montpellier.inra.fr/URLB/pop100gene/pop100gene.html (table 1 and Fig. 3). Tests for linkage disequilibrium, Hardy-Weinberg departures and their statistical significance were performed using GENEPOP 4.0 http://kimura.univ-montp2.fr/%7Erousset/Genepop.htm.
Population differentiation and Bayesian population assignment test
First, to identify and illustrate in the factorial space the degree of similarity in allelic states between populations of both taxa from Öregrund, where they occur in sympatry, a factorial correspondence analysis (FCA) was carried out using GENETIX 4.03 http://www.genetix.univ-montp2.fr/genetix/genetix.htm (Fig. 2B). Subsequently, to examine whether sympatric populations of F. radicans and F. vesiculosus are genetically different and to measure the difference magnitudes, F-statistics were calculated using FSTAT 2.9.3 http://www2.unil.ch/popgen/softwares/fstat.htm and significance levels were Bonferroni-corrected (table 2). Then, to assess the genetic affinities between species and populations a neighbour-joining tree was constructed using Cavalli-Sforza genetic distances with 10,000 bootstrap support replicates on locus information using POPULATIONS http://bioinformatics.org/~tryphon/populations/ (Fig. 2C). Finally, to provide an alternative classification of individuals and identification of potential hybrids, a Bayesian assignment analysis was also performed using STRUCTURE 2.2 http://pritch.bsd.uchicago.edu/software.html with a burn-in period of 50,000 and 1,000,000 iterations. The algorithm infers individual ancestry by assigning sampled individuals into a user-defined number of clusters (K)/populations that minimize genotypic disequilibrium under the assumption of random mating. The maximum number of clusters was set to K = 5, (Fig. 4).
Estimation of demographic parameters of species divergence
We thank A. Tatarenkov for advice during early stages of work and for comments on the manuscript, to B. Jönsson for assistance in the laboratory and to J. Havenhand, C. André, R. K. Butlin and B. Emerson for valuable comments. This work was financially supported by the Swedish Research Councils (VR and Formas) partly through the BaltGene research program and the Linnaeus initiative 'Adaptation to changing marine environments (ACME)'.
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