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- High and distinct range-edge genetic diversity despite local bottlenecksPublication . Assis, J.; Castilho Coelho, N.; Alberto, F.; Valero, Myriam; Raimondi, P. T.; Reed, D. C.; Serrão, EsterThe genetic consequences of living on the edge of distributional ranges have been the subject of a largely unresolved debate. Populations occurring along persistent low latitude ranges (rear-edge) are expected to retain high and unique genetic diversity. In contrast, currently less favourable environmental conditions limiting population size at such range-edges may have caused genetic erosion that prevails over past historical effects, with potential consequences on reducing future adaptive capacity. The present study provides an empirical test of whether population declines towards a peripheral range might be reflected on decreasing diversity and increasing population isolation and differentiation. We compare population genetic differentiation and diversity with trends in abundance along a latitudinal gradient towards the peripheral distribution range of Saccorhiza polyschides, a large brown seaweed that is the main structural species of kelp forests in SW Europe. Signatures of recent bottleneck events were also evaluated to determine whether the recently recorded distributional shifts had a negative influence on effective population size. Our findings show decreasing population density and increasing spatial fragmentation and local extinctions towards the southern edge. Genetic data revealed two well supported groups with a central contact zone. As predicted, higher differentiation and signs of bottlenecks were found at the southern edge region. However, a decrease in genetic diversity associated with this pattern was not verified. Surprisingly, genetic diversity increased towards the edge despite bottlenecks and much lower densities, suggesting that extinctions and recolonizations have not strongly reduced diversity or that diversity might have been even higher there in the past, a process of shifting genetic baselines.
- Fast sporophyte replacement after removal suggests banks of latent microscopic stages of Laminaria Ochroleuca (phaeophyceae) in tide pools in northern PortugalPublication . Barradas, Ana; Alberto, F.; Engelen, Aschwin; Serrão, EsterThis study investigated the effects of a physical disturbance consisting of the removal of adult kelps (Laminaria ochroleuca Bachelot de la Pylaie)and their corresponding understorey turf assemblage in tide pools in northern Portugal.
- Assessing genetic diversity in clonal organisms: low diversity or low resolution? Combining power and cost efficiency in selecting markersPublication . ARNAUD-HAOND, Sophie; Alberto, F.; Teixeira, Sara; Procaccini, G.; Serrão, Ester; Duarte, C. M.The increasing use of molecular tools to study populations of clonal organisms leads us to question whether the low polymorphism found in many studies reflects limited genetic diversity in populations or the limitations of the markers used. Here we used microsatellite datasets for two sea grass species to provide a combinatory statistic, combined with a likelihood approach to estimate the probability of identical multilocus genotypes (MLGs) to be shared by distinct individuals, in order to ascertain the efficiency of the markers used and to optimize cost-efficiently the choice of markers to use for deriving unbiased estimates of genetic diversity. These results strongly indicate that conclusions from studies on clonal organisms derived using markers showing low polymorphism, including microsatellites, should be reassessed using appropriate polymorphic markers.
- Genetic homogeneity in the seagrass Cymodocea nodosa at its northern Atlantic limit revealed through RAPDPublication . Alberto, Filipe; Mata, Leonardo; Santos, RuiRandom amplified polymorphic DNA (RAPD) markers were used to analyse the genetic variability of the dioecious seagrass Cymodocea nodosa Ucria (Ascherson) in the Ria Formosa lagoon, Portugal, the species' northern limit in the Atlantic. Three individuals from each of 6 meadows were genotyped with 28 primers. Meadows described previously as having flower marks were compared with meadows where flowers did not occur. A single polymorphic band, specific for one meadow, was observed in a total of 177 fragments. The lack of genetic variability among meadows both with and without flower indicates that flower production is not associated with a higher level of genetic variation. The genetic homogeneity of C, nodosa in the Ria Formosa suggests a founder effect, produced by a single or a limited number of migrants composing the colonising gene pool, This hypothesis is supported by the geographic isolation from other populations as the nearest populations lie more than 300 km away from the Ria Formosa. The lack of reproductive success of C, nodosa in Ria Formosa natural park and its low genetic variability are important factors in the conservation of this species since recolonisation can only occur through vegetative growth.
- 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.
- 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.
- Standardizing methods to address clonality in population studies (Molecular Ecology) (2007) 16, (5115-5139))Publication . ARNAUD-HAOND, Sophie; Duarte, M.; Alberto, F.; Serrão, EsterAlthough clonal species are dominant in many habitats, from unicellular organisms to plants and animals, ecological and particularly evolutionary studies on clonal species have been strongly limited by the difficulty in assessing the number, size and longevity of genetic individuals within a population. The development of molecular markers has allowed progress in this area, and although allozymes remain of limited use due to their typically low level of polymorphism, more polymorphic markers have been discovered during the last decades, supplying powerful tools to overcome the problem of clonality assessment. However, population genetics studies on clonal organisms lack a standardized framework to assess clonality, and to adapt conventional data analyses to account for the potential bias due to the possible replication of the same individuals in the sampling. Moreover, existing studies used a variety of indices to describe clonal diversity and structure such that comparison among studies is difficult at best. We emphasize the need for standardizing studies on clonal organisms, and particularly on clonal plants, in order to clarify the way clonality is taken into account in sampling designs and data analysis, and to allow further comparison of results reported in distinct studies. In order to provide a first step towards a standardized framework to address clonality in population studies, we review, on the basis of a thorough revision of the literature on population structure of clonal plants and of a complementary revision on other clonal organisms, the indices and statistics used so far to estimate genotypic or clonal diversity and to describe clonal structure in plants. We examine their advantages and weaknesses as well as various conceptual issues associated with statistical analyses of population genetics data on clonal organisms. We do so by testing them on results from simulations, as well as on two empirical data sets of microsatellites of the seagrasses Posidonia oceanica and Cymodocea nodosa. Finally, we also propose a selection of new indices and methods to estimate clonal diversity and describe clonal structure in a way that should facilitate comparison between future studies on clonal plants, most of which may be of interest for clonal organisms in general.
- Is asexual reproduction more important at geographical limits? A genetic study of the seagrass Zostera marina in the Ria Formosa, PortugalPublication . Billingham, M. R.; Reusch, T. B. H.; Alberto, F.; Serrão, EsterIn populations of species that are able to reproduce both sexually and asexually, there may be local differences with regard to the relative importance of the 2 modes of reproduction. Studies of plant species with such a life history have shown that the contribution of sexual reproduction to population maintenance may be lower at the geographical margins, with genotypic diversity often used as an indicator of the relative importance of vegetative and sexual reproduction. This hypothesis was examined in a collection of samples of eelgrass Zostera marina (a marine flowering plant) from its eastern Atlantic southern limit (Ria Formosa, Portugal). Samples from 12 sites were genotyped using 9 microsatellite loci to compare within-site clonal and genetic diversity, and among-site distribution of genetic diversity, with previously published values from central sites. Sites within the Ria Formosa had lower clonal diversities (mean = 0.29, range = 0.07 to 0.68) than the central sites (mean = 0.86, range = 0.33 to 1.00), lower levels of expected heterozygosity (He = 0.423 vs 0.486) and exhibited heterozygote excesses rather than deficits. Similarly, genetic differentiation was found to be much greater in the Ria Formosa, with the FST of 0.233 being over 10-fold greater than that reported for populations in the Baltic Sea. Results from this study were consistent with previous findings of reduced sexual reproduction, genotypic diversity and among-population gene flow at species limits.
- 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.
- Disentangling the Influence of Mutation and Migration in Clonal Seagrasses Using the Genetic Diversity Spectrum for MicrosatellitesPublication . ARNAUD-HAOND, Sophie; Moalic, Yann; Hernandez-Garcia, Emilio; Eguíluz, Víctor M.; Alberto, Filipe; Serrao, Ester A.; Duarte, Carlos M.The recurrent lack of isolation by distance reported at regional scale in seagrass species was recently suggested to stem from stochastic events of large-scale dispersal. We explored the usefulness of phylogenetic information contained in microsatellite loci to test this hypothesis by using the Genetic Diversity Spectrum (GDS) on databases containing, respectively, 7 and 9 microsatellites genotypes for 1541 sampling units of Posidonia oceanica and 1647 of Cymodocea nodosa. The simultaneous increase of microsatellite and geographic distances that emerges reveals a coherent pattern of isolation by distance in contrast to the chaotic pattern previously described using allele frequencies, in particular, for the long-lived P. oceanica. These results suggest that the lack of isolation by distance, rather than the resulting from rare events of large-scale dispersal, reflects at least for some species a stronger influence of mutation over migration at the scale of the distribution range. The global distribution of genetic polymorphism may, therefore, result predominantly from ancient events of step-by-step (re) colonization followed by local recruitment and clonal growth, rather than contemporary gene flow. The analysis of GDS appears useful to unravel the evolutionary forces influencing the dynamics and evolution at distinct temporal and spatial scales by accounting for phylogenetic information borne by microsatellites, under an appropriate mutation model. This finding adds nuance to the generalization of the influence of large-scale dispersal on the dynamics of seagrasses.
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