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- Genetic diversity of a marine foundation species,Laminaria hyperborea(Gunnerus) Foslie, along the coast of IrelandPublication . Schoenrock, Kathryn M.; O'Connor, Aisha M.; Mauger, Stephane; Valero, Myriam; MACHADO, JOÃO NEIVA; Serrao, Ester; Krueger-Hadfield, Stacy A.Worldwide, kelp populations are stressed by warming, increased storms and other anthropogenic disturbances. Marine population distributions are projected to retreat poleward with climate change if they cannot adapt to changing conditions, which would potentially lead to a regime shift in subtidal habitats. In Northern Europe,Laminaria hyperboreais a subtidal ecosystem engineer whose distribution has shifted over millennia, leaving predicted areas of high genetic diversity from the last glacial maximum (LGM) near its southern distribution limit in the Iberian Peninsula. In Ireland,L. hyperboreastructures communities by supporting diverse faunal assemblages and producing large quantities of organic carbon throughout the year. We investigated the genetic diversity of eight populations, ranging from the southern coast to the north-west of Ireland, using nine microsatellite loci. Diversity was found to be highest in Lough Hyne, a Special Area of Conservation (SAC), near the predicted climate refugium. We found evidence of isolation by distance, with high connectivity between populations that were geographically close, probably driven by short range dispersal ofL. hyperboreapropagules. Genetic diversity (measured as expected heterozygosity and allelic richness) was highest at Lough Hyne, and decreased northwards, as predicted from past range shifts. Expected heterozygosity was highest at Lough Hyne (0.706) and decreased northward, with the lowest value at Bridges of Ross (0.283). Based on these patterns, further fine-scale investigation into population diversity, dispersal and potential resilience in Irish kelp forests are necessary as warming and non-native species are observed more and more frequently.
- New microsatellite markers for the endemic Mediterranean seagrass Posidonia oceanicaPublication . Alberto, F.; Correia, L.; ARNAUD-HAOND, Sophie; Billot, C.; Duarte, C. M.; Serrão, EsterThe seagrass Posidonia oceanica is endemic to the Mediterranean Sea, where it plays an important role in coastal ecosystem dynamics. Because of this important role and concerns about the observed regression of some meadows, population genetic studies of this species have been promoted. However, the markers used until now were not polymorphic enough to efficiently assess the level and spatial pattern of genetic variability. Hypervariable molecular markers were obtained by screening a genomic library enriched for microsatellite dinucleotide repeats. Among 25 primer pairs defined, eight amplified polymorphic microsatellites with an encouraging level of variability at the two geographical scales sampled.
- 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.
- Characterization of 15 polymorphic microsatellite loci in the temperate reef fish Lepadogaster lepadogaster, developed using 454-sequencingPublication . Teixeira, Sara; Candeias, Rui; Klein, Maria; Serrão, Ester; Borges, R.Abstract The clingfish, Lepadogaster lepadogaster is a reef fish species, abundant in temperate nearshore rocky reefs of the Eastern Atlantic and central and Eastern Mediterranean. To study genetic variability and population connectivity of this species, we developed fifteen polymorphic microsatellite markers. These were tested in one population and all but one, showed no departure from Hardy–Weinberg equilibrium. Average overall observed heterozygosity was 0.66 and allelic richness was 8.9. Two primer pairs revealed possible linkage disequilibrium. These markers open perspectives for population genetic studies of this species to unravel connectivity and population biology, vital information for future conservation studies.
- Genetic differentiation and secondary contact zone in the seagrass Cymodocea nodosa across the Mediterranean-Atlantic transition regionPublication . Alberto, F.; Massa, S. I.; Manent, P.; Diaz-Almela, E.; ARNAUD-HAOND, Sophie; Duarte, C. M.; Serrão, EsterAim A central question in evolutionary ecology is the nature of environmental barriers that can limit gene flow and induce population genetic divergence, a first step towards speciation. Here we study the geographical barrier constituted by the transition zone between the Atlantic Ocean and the Mediterranean Sea, using as our model Cymodocea nodosa, a seagrass distributed throughout the Mediterranean and in the Atlantic, from central Portugal to Mauritania. We also test predictions about the genetic footprints of Pleistocene glaciations. Location The Atlantic–Mediterranean transition region and adjacent areas in the Atlantic (Mauritania to south-west Portugal) and the Mediterranean. Methods We used eight microsatellite markers to compare 20 seagrass meadows in the Atlantic and 27 meadows in the Mediterranean, focusing on the transition between these basins. Results Populations from these two regions form coherent groups containing several unique, high-frequency alleles for the Atlantic and for the Mediterranean, with some admixture west of the Almeria–Oran Front (Portugal, south-west Spain and Morocco). These are populations where only one or a few genotypes were found, for all but Cadiz, but remarkably still show the footprint of a contact zone. This extremely low genotypic richness at the Atlantic northern edge contrasts with the high values (low clonality) at the Atlantic southern edge and in most of the Mediterranean. The most divergent populations are those at the higher temperature range limits: the southernmost Atlantic populations and the easternmost Mediterranean, both potential footprints of vicariance. Main conclusions A biogeographical transition region occurs close to the Almeria–Oran front. A secondary contact zone in Atlantic Iberia and Morocco results from two distinct dispersal sources: the Mediterranean and southernmost Atlantic populations, possibly during warmer interglacial or post-glacial periods. The presence of high-frequency diagnostic alleles in present-day disjunct populations from the southernmost Atlantic region indicates that their separation from all remaining populations is ancient, and suggests an old, stable rear edge.
- 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.
- Highly polymorphic microsatellite markers for the short-snouted seahorse (hippocampus hippocampus), including markers from a closely related species the long-snouted seahorse (hippocampus guttulatus)Publication . Van De Vliet, M. S.; Diekmann, O. E.; Serrão, EsterSpecies of the family Syngnathidae are increasingly being investigated for conservation purposes but also for mating system and genetic parentage studies. The availability of highly polymorphic markers will be of great importance to conduct these kinds of studies. This paper describes the development and characterization of 10 polymorphic microsatellite markers for Hippocampus hippocampus and the utility of nine markers which were developed for a closely related species Hippocampus guttulatus. The number of alleles per locus developed for H. hippocampus ranged from 14 to 30, with levels of heterozygosity between 0.90 and 0.95. Most of the markers were successfully cross-amplified in the sister species, giving clear and unambiguous peaks and maintaining high levels of polymorphism.
- Vicariance patterns in the Mediterranean Sea: East-west cleavage and low dispersal in the endemic seagrass Posidonia oceanicaPublication . ARNAUD-HAOND, Sophie; Migliaccio, M.; Diaz-Almela, E.; Teixeira, Sara; Van De Vliet, M. S.; Alberto, F.; Procaccini, G.; Duarte, C. M.; Serrão, EsterAim The seagrass, Posidonia oceanica is a clonal angiosperm endemic to the Mediterranean Sea. Previous studies have suggested that clonal growth is far greater than sexual recruitment and thus leads to low clonal diversity within meadows. However, recently developed microsatellite markers indicate that there are many different genotypes, and therefore many distinct clones present. The low resolution of markers used in the past limited our ability to estimate clonality and assess the individual level. New high-resolution dinucleotide microsatellites now allow genetically distinct individuals to be identified, enabling more reliable estimation of population genetic parameters across the Mediterranean Basin. We investigated the biogeography and dispersal of P. oceanica at various spatial scales in order to assess the influence of different evolutionary factors shaping the distribution of genetic diversity in this species. Location The Mediterranean. Methods We used seven hypervariable microsatellite markers, in addition to the five previously existing markers, to describe the spatial distribution of genetic variability in 34 meadows spread throughout the Mediterranean, on the basis of an average of 35.6 (± 6.3) ramets sampled. Results At the scale of the Mediterranean Sea as a whole, a strong east–west cleavage was detected (amova). These results are in line with those obtained using previous markers. The new results showed the presence of a putative secondary contact zone at the Siculo-Tunisian Strait, which exhibited high allelic richness and shared alleles absent from the eastern and western basins. F statistics (pairwise θ ranges between 0.09 and 0.71) revealed high genetic structure between meadows, both at a small scale (about 2 to 200 km) and at a medium scale within the eastern and western basins, independent of geographical distance. At the intrameadow scale, significant spatial autocorrelation in six out of 15 locations revealed that dispersal can be restricted to the scale of a few metres. Main conclusions A stochastic pattern of effective migration due to low population size, turnover and seed survival is the most likely explanation for this pattern of highly restricted gene flow, despite the importance of an a priori seed dispersal potential. The east–west cleavage probably represents the outline of vicariance caused by the last Pleistocene ice age and maintained to this day by low gene flow. These results emphasize the diversity of evolutionary processes shaping the genetic structure at different spatial scales.
- 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.
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