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Reciprocal transplants support a plasticity-first scenario during colonisation of a large hyposaline basin by a marine macro alga

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ABSTRACT

Background: Establishing populations in ecologically marginal habitats may require substantial phenotypic changes that come about through phenotypic plasticity, local adaptation, or both. West-Eberhard’s “plasticity-first” model suggests that plasticity allows for rapid colonisation of a new environment, followed by directional selection that develops local adaptation. Two predictions from this model are that (i) individuals of the original population have high enough plasticity to survive and reproduce in the marginal environment, and (ii) individuals of the marginal population show evidence of local adaptation. Individuals of the macroalga Fucus vesiculosus from the North Sea colonised the hyposaline (≥2–3‰) Baltic Sea less than 8000 years ago. The colonisation involved a switch from fully sexual to facultative asexual recruitment with release of adventitious branches that grow rhizoids and attach to the substratum. To test the predictions from the plasticity-first model we reciprocally transplanted F. vesiculosus from the original population (ambient salinity 24‰) and from the marginal population inside the Baltic Sea (ambient salinity 4‰). We also transplanted individuals of the Baltic endemic sister species F. radicans from 4 to 24‰. We assessed the degree of plasticity and local adaptation in growth and reproductive traits after 6 months by comparing the performance of individuals in 4 and 24‰.

Results: Branches of all individuals survived the 6 months period in both salinities, but grew better in their native salinity. Baltic Sea individuals more frequently developed asexual traits while North Sea individuals initiated formation of receptacles for sexual reproduction.

Conclusions: Marine individuals of F. vesiculosus are highly plastic with respect to salinity and North Sea populations can survive the extreme hyposaline conditions of the Baltic Sea without selective mortality. Plasticity alone would thus allow for an initial establishment of this species inside the postglacial Baltic Sea at salinities where reproduction remains functional. Since establishment, the Baltic Sea populations have evolved adaptations to extreme hyposaline waters and have in addition evolved asexual recruitment that, however, tends to impede local adaptation. Overall, our results support the “plasticity-first” model for the initial colonisation of the Baltic Sea by Fucus vesiculosus.

Electronic supplementary material: The online version of this article (doi:10.1186/s12898-017-0124-1) contains supplementary material, which is available to authorized users.

No MeSH data available.


Map showing sampling sites and the Baltic Sea salinity gradient. Source: Online Map Creation-Martin Weinelt, http://aquarius.ifm-geomar.de, visited 2009.05.01
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Fig1: Map showing sampling sites and the Baltic Sea salinity gradient. Source: Online Map Creation-Martin Weinelt, http://aquarius.ifm-geomar.de, visited 2009.05.01

Mentions: We sampled F. radicans and F. vesiculosus (73 individuals in total) from a sympatric site on the Swedish coast of the northern Baltic Sea (Skagsudde, N 63°11′21″, E 19°0′13″; Fig. 1). In addition, we sampled 20 individuals of F. vesiculosus from a North Sea population on the Swedish west coast (Saltö, N 58°52′16″, E 11°7′11″; Fig. 1). The Baltic samples were from a depth of 3–6 m and an average salinity of 4‰, while the North Sea samples were from the intertidal, with fluctuating salinity around an average of 24‰ (range 15–30‰). Sampling was performed in July 2011 and fresh thalli were brought to the laboratory and stored in tanks with water of ambient salinity (4 and 24‰, respectively). We hereafter refer to each of these three samples (F. radicans from the Baltic Sea, F. vesiculosus from the Baltic Sea, and F. vesiculosus from the North Sea) as our three “populations”. Formal identification of the individuals within each sample was done by D.J. on basis of morphological criteria and microsatellite genotype.Fig. 1


Reciprocal transplants support a plasticity-first scenario during colonisation of a large hyposaline basin by a marine macro alga
Map showing sampling sites and the Baltic Sea salinity gradient. Source: Online Map Creation-Martin Weinelt, http://aquarius.ifm-geomar.de, visited 2009.05.01
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC5382403&req=5

Fig1: Map showing sampling sites and the Baltic Sea salinity gradient. Source: Online Map Creation-Martin Weinelt, http://aquarius.ifm-geomar.de, visited 2009.05.01
Mentions: We sampled F. radicans and F. vesiculosus (73 individuals in total) from a sympatric site on the Swedish coast of the northern Baltic Sea (Skagsudde, N 63°11′21″, E 19°0′13″; Fig. 1). In addition, we sampled 20 individuals of F. vesiculosus from a North Sea population on the Swedish west coast (Saltö, N 58°52′16″, E 11°7′11″; Fig. 1). The Baltic samples were from a depth of 3–6 m and an average salinity of 4‰, while the North Sea samples were from the intertidal, with fluctuating salinity around an average of 24‰ (range 15–30‰). Sampling was performed in July 2011 and fresh thalli were brought to the laboratory and stored in tanks with water of ambient salinity (4 and 24‰, respectively). We hereafter refer to each of these three samples (F. radicans from the Baltic Sea, F. vesiculosus from the Baltic Sea, and F. vesiculosus from the North Sea) as our three “populations”. Formal identification of the individuals within each sample was done by D.J. on basis of morphological criteria and microsatellite genotype.Fig. 1

View Article: PubMed Central - PubMed

ABSTRACT

Background: Establishing populations in ecologically marginal habitats may require substantial phenotypic changes that come about through phenotypic plasticity, local adaptation, or both. West-Eberhard’s “plasticity-first” model suggests that plasticity allows for rapid colonisation of a new environment, followed by directional selection that develops local adaptation. Two predictions from this model are that (i) individuals of the original population have high enough plasticity to survive and reproduce in the marginal environment, and (ii) individuals of the marginal population show evidence of local adaptation. Individuals of the macroalga Fucus vesiculosus from the North Sea colonised the hyposaline (≥2–3‰) Baltic Sea less than 8000 years ago. The colonisation involved a switch from fully sexual to facultative asexual recruitment with release of adventitious branches that grow rhizoids and attach to the substratum. To test the predictions from the plasticity-first model we reciprocally transplanted F. vesiculosus from the original population (ambient salinity 24‰) and from the marginal population inside the Baltic Sea (ambient salinity 4‰). We also transplanted individuals of the Baltic endemic sister species F. radicans from 4 to 24‰. We assessed the degree of plasticity and local adaptation in growth and reproductive traits after 6 months by comparing the performance of individuals in 4 and 24‰.

Results: Branches of all individuals survived the 6 months period in both salinities, but grew better in their native salinity. Baltic Sea individuals more frequently developed asexual traits while North Sea individuals initiated formation of receptacles for sexual reproduction.

Conclusions: Marine individuals of F. vesiculosus are highly plastic with respect to salinity and North Sea populations can survive the extreme hyposaline conditions of the Baltic Sea without selective mortality. Plasticity alone would thus allow for an initial establishment of this species inside the postglacial Baltic Sea at salinities where reproduction remains functional. Since establishment, the Baltic Sea populations have evolved adaptations to extreme hyposaline waters and have in addition evolved asexual recruitment that, however, tends to impede local adaptation. Overall, our results support the “plasticity-first” model for the initial colonisation of the Baltic Sea by Fucus vesiculosus.

Electronic supplementary material: The online version of this article (doi:10.1186/s12898-017-0124-1) contains supplementary material, which is available to authorized users.

No MeSH data available.