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- Broad scale agreement between intertidal habitats and adaptive traits on a basis of contrasting population genetic structurePublication . I Zardi, Gerardo; Nicastro, Katy R; Ferreira Costa, J.; Serrão, Ester; Pearson, G. A.Understanding the extent to which neutral processes and adaptive divergence shape the spatial structure of natural populations is a major goal in evolutionary biology and is especially important for the identification of significant levels of biodiversity. Our results identified replicated habitat-specific (adaptive) phenotypic divergence in the brown macroalga Fucus vesiculosus that is independent of population (neutral) genetic structure. F. vesiculosus inhabits contiguous and contrasting marine to estuarine intertidal habitats. Combining analyses of genetic and phenotypic traits of populations living under differential selective regimes (estuaries and open coast), we investigated levels of neutral genetic differentiation and adaptive physiological responses to emersion stress. In southwest England (SW UK) and northern Iberia (N. Iberia), populations living in estuaries and marine coastal habitats were genetically characterized at six microsatellite loci. In N. Iberia, two clades with limited admixture were recovered, each including one open coast site and the adjacent estuarine location. In contrast, SW UK samples clustered according to habitat and formed three distinct groups of genotypes; one including the two open coast locations and the other two representing each of the estuarine sites. Temperature loggers revealed distinct emersion regimes that characterized each habitat type independently of the region, while water and air temperature profiles showed site-specific trends. Despite acclimation under usual conditions, trait means of emersion stress resilience showed a strong phenotypic divergence between habitats, consistent with environmental clines in exposure time observed in the different habitats. We demonstrate that neutral genetic clusters do not reflect locally adapted population units. Our results identified replicated habitat-specific (adaptive) phenotypic divergence that is independent of population (neutral) genetic structure in F. vesiculosus. The significance of such findings extends beyond the theoretical evolutionary and ecological interest of discovering parallel adaptive responses to the broader implications for conservation of intraspecific biodiversity.
- Drifting fronds and drifting alleles: range dynamics, local dispersal and habitat isolation shape the population structure of the estuarine seaweed Fucus ceranoidesPublication . Neiva, J.; Pearson, G. A.; Valero, Myriam; Serrão, EsterAim: The seaweed Fucus ceranoides is restricted to spatially discrete estuarine habitats and lacks planktonic dispersal phases; it is therefore expected to exhibit strong population differentiation. Its cold-temperate affinities and mtDNA variation imply that the northern part of the species’ range, where F. ceranoides is now ubiquitous, was recently colonized after the onset of the last deglaciation, potentially resulting in areas with greater genetic homogeneity. Here we examine the population structure of F. ceranoides to test these predictions, emphasizing the contrasting genetic signatures of limited dispersal in refugial versus recently colonized regions. Location: North-eastern Atlantic estuaries from Portugal to Norway. Methods: A total of 504 individuals from 21 estuarine sites spanning the entire range of F. ceranoides were sampled and genotyped for nine microsatellite loci. Population structure was inferred from several genotypic and allele-frequency analyses. Geographical patterns of genetic diversity were used to reconstruct the historical biogeography of the species. Results: Genetic diversity and regional population differentiation showed a consistent decline with increasing latitude. Southernmost populations harboured most of the endemic variation, whereas the northern populations (> 55 N) were almost fixed for the same alleles across loci. In southern and central regions of its distribution, F. ceranoides showed striking population subdivision, with many of the sampled estuaries corresponding to coherent genetic units that were easily discriminated from one another with standard clustering methods. Main conclusions: The geographical pattern of genetic diversity supports the long-term refugial status of Iberia and a post-glacial range expansion of F. ceranoides into previously glaciated latitudes. Despite the species’ capacity to colonize newly available habitats, the genetic structure of F. ceranoides outside the recently (re)colonized range reveals that gene flow between populations is extremely low. This study provides a remarkable example of how infrequent and spatially limited dispersal can have contrasting effects at the scales of metapopulation (connectivity) versus range dynamics (habitat tracking), and of how dispersal restrictions can result in either genetic divergence or homogeneity depending on the maturity and demographic conditions of the populations.
- Population genetics of dwarf eelgrass Zostera noltii throughout its biogeographic rangePublication . Coyer, J. A.; Diekmann, O. E.; Serrão, Ester; Procaccini, G.; Milchakova, N.; Pearson, G. A.; Stam, W. T.; Olsen, J. L.The marine angiosperm Zostera noltii (dwarf eelgrass), an important facilitator species and food source for invertebrates and waterfowl, predominantly inhabits intertidal habitats along eastern Atlantic shores from Mauritania to southern Norway/Kattegat Sea and throughout the Mediterranean, Black and Azov seas. We used 9 microsatellite loci to characterize population structure at a variety of spatial scales among 33 populations from 11 localities throughout the entire biogeographic range. Isolation by distance analysis suggested a panmictic genetic neighborhood of 100 to 150 km. At the global scale, a neighbor-joining tree based on Reynolds distances revealed strongly-supported groups corresponding to northern Europe, Mauritania and the Black/Azov Sea; separate Mediterranean and Atlantic-Iberian groups were poorly supported. Clones (genets with multiple ramets) were present in most populations but were generally small (ca. <3 m2). Exceptions were found in Mauritania (ca. 29 m in length), the Azov Sea (ca. 40 m in length) and the Black Sea (ca. 50 m in length). Although genetic diversity and allelic richness generally decreased from Mauritania to Denmark, the putative post-glacial recolonization route, both were unexpectedly high among populations from the German Wadden Sea.
- Characterization of microsatellite loci in the dwarf eelgrass Zostera noltii (Zosteraceae) and cross-reactivity with Z. japonicaPublication . Coyer, J. A.; Reusch, T. B. H.; Stam, W. T.; Serrão, Ester; Pearson, G. A.; Procaccini, G.; Olsen, J. L.Zostera noltii is an important species of eelgrass occurring along European, north African, Mediterranean, Black Sea and Azov Sea coasts. Nine microsatellite loci were developed and no linkage disequilibrium was observed. Cross-amplification was observed for all loci (polymorphic) in Z. japonica ; only four loci amplified (monomorphic) in Z. marina.
- Polymorphic microsatellite markers in the brown seaweed Fucus vesiculosusPublication . Candeias, Rui; Casado-Amezúa, Pilar; Pearson, G. A.; Serrão, Ester; Teixeira, SaraBackground: Fucus vesiculosus is a brown seaweed dominant on temperate rocky shores of the northern hemisphere and, is typically distributed in the mid-upper intertidal zone. It is an external fertilizer that reproduces sexually, providing an excellent model to address conflicting theories related to mating systems and sexual selection. Microsatellite markers have been reported for several Fucus species, however the genomic libraries from where these markers have been isolated, have originated from two or more species pooled together (F. vesiculosus and F. serratus in one library; F. vesiculosus, F. serratus and Ascophyllum nodosum in a second library), or when the genomic DNA originated from only one species it was from Fucus spiralis. Although these markers cross-amplify F. vesiculosus individuals, the level of polymorphism has been low for relatedness studies. Findings: The microsatellite markers described here were obtained from an enriched genomic library, followed by 454 pyrosequencing. A total of 9 microsatellite markers were tested across 44 individuals from the North of Portugal. The mean number of alleles across loci was 8.7 and the gene diversity 0.67. Conclusions: The high variability displayed by these microsatellite loci should be useful for paternity analysis, assessing variance of reproductive success and in estimations of genetic variation within and between populations.
- Implications of mating system for genetic diversity of sister algal species: Fucus spiralis and Fucus vesiculosus (Heterokontophyta, Phaeophyceae)Publication . Perrin, C.; Daguin, C.; Van De Vliet, M. S.; Engel, C. R.; Pearson, G. A.; Serrão, EsterThe implications of mating system for genetic diversity were assessed in the sister species Fucus spiralis and Fucus vesiculosus using a combination of ten microsatellite markers. Five new microsatellite markers specific for F. spiralis were developed in order to increase marker resolution and complement the results (i.e. mating system and genetic diversity extended to a larger geographic scale) acquired using five microsatellite loci previously developed from a mixed fucoid seaweed DNA library that excluded F. spiralis. Low genetic diversities observed at the population and species level in F. spiralis using the five new F. spiralis-specific loci described here were consistent with the results obtained previously with non-specific microsatellite loci. Results revealed that selfing is characteristic in F. spiralis across its latitudinal distribution along the Iberian and French Atlantic coasts. Higher levels of within-population genetic diversity were observed in the outcrossing species F. vesiculosus, decreasing towards the southern distributional range of the species. Some cases of significant biparental inbreeding in this species are indicative of short gamete dispersal or mating of spatially or temporally structured populations. In contrast to within-population diversities, higher total genetic diversity among populations was observed in the hermaphroditic species in comparison to the dioecious F. vesiculosus.
- Fucus cottonii (Fucales, Phaeophyceae) is not a single genetic entity but a convergent salt-marsh morphotype with multiple independent originsPublication . Neiva, J.; Hansen, G. I.; Pearson, G. A.; Van De Vliet, M. S.; Maggs, C. A.; Serrão, EsterIn low-energy salt-marsh environments, Fucus spp. frequently exhibit an atypical morphology that is characterized by the absence of an anchoring holdfast and a trend towards reduced size and buoyancy, enhanced vegetative proliferation, and often the loss of sexual reproduction. Such forms, often referred to as ecads, presumably derive from typical attached forms, but their affinities are normally difficult to establish with confidence due to their simplified and largely convergent morphology. Minute salt-marsh forms growing partially embedded in the sediment occur on Atlantic and Pacific coasts and have traditionally been recognized as an independent entity, Fucus cottonii. In this study we analyse with four microsatellite loci two F. cottonii populations from salt-marshes of Oregon (NE Pacific) and Ireland (Europe, near the species type locality), as well as local populations of other Fucus spp. that could be considered potential source populations, either directly or via hybridization. Our results show that the F. cottonii from Oregon derive from F. gardneri whereas the Irish population is closer to F. spiralis. We conclude that F. cottonii is not a coherent genetic entity, but an artificial grouping of evolutionarily independent populations that converged into similar morphologies in different salt-marsh habitats.