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  • Assessing genetic diversity in clonal organisms: low diversity or low resolution? Combining power and cost efficiency in selecting markers
    Publication . 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.
  • Comparative analysis of stability-genetic diversity in seagrass (Posidonia oceanica) meadows yields unexpected results
    Publication . ARNAUD-HAOND, Sophie; Marbà, N.; Diaz-Almela, E.; Serrão, Ester; Duarte, C. M.
    The diversity–stability relationship is the subject of a long-standing debate in ecology, but the genetic component of diversity has seldom been explored. In this study, we analyzed the interplay between genetic diversity and demographic responses to environmental pressures. This analysis included 30 meadows formed by the Mediterranean endemic seagrass, Posidonia oceanica, showing a wide range of population dynamics ranging from a near equilibrium state to steep decline due to strong environmental pressures close to aquaculture installations. Our results show that sedimentation rates are much better predictors of mortality than clonal or genetic components. An unexpected positive trend was observed between genotypic diversity and mortality, along with a negative relationship between allelic richness and net population growth. Yet such trends disappeared when excluding the most extreme cases of disturbance and mortality, suggesting the occurrence of a threshold below which no relationship exists. These results contrast with the positive relationship between genotypic diversity and resistance or resilience observed in previous manipulative experiments on seagrass. We discuss the reasons for this discrepancy, including the difficulties in designing experiments reflecting the complexity of natural meadows.
  • New microsatellite markers for the endemic Mediterranean seagrass Posidonia oceanica
    Publication . Alberto, F.; Correia, L.; ARNAUD-HAOND, Sophie; Billot, C.; Duarte, C. M.; Serrão, Ester
    The 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 region
    Publication . Alberto, F.; Massa, S. I.; Manent, P.; Diaz-Almela, E.; ARNAUD-HAOND, Sophie; Duarte, C. M.; Serrão, Ester
    Aim  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.
  • Network analysis identifies weak and strong links in a metapopulation system
    Publication . Rozenfeld, A. F.; ARNAUD-HAOND, Sophie; Hernández-García, E.; Eguíluz, Víctor M.; Serrão, Ester; Duarte, C. M.
    The identification of key populations shaping the structure and connectivity of metapopulation systems is a major challenge in population ecology. The use of molecular markers in the theoretical framework of population genetics has allowed great advances in this field, but the prime question of quantifying the role of each population in the system remains unresolved. Furthermore, the use and interpretation of classical methods are still bounded by the need for a priori information and underlying assumptions that are seldom respected in natural systems. Network theory was applied to map the genetic structure in a metapopulation system by using microsatellite data from populations of a threatened seagrass, Posidonia oceanica, across its whole geographical range. The network approach, free from a priori assumptions and from the usual underlying hypotheses required for the interpretation of classical analyses, allows both the straightforward characterization of hierarchical population structure and the detection of populations acting as hubs critical for relaying gene flow or sustaining the metapopulation system. This development opens perspectives in ecology and evolution in general, particularly in areas such as conservation biology and epidemiology, where targeting specific populations is crucial.
  • Standardizing methods to address clonality in population studies (Molecular Ecology) (2007) 16, (5115-5139))
    Publication . ARNAUD-HAOND, Sophie; Duarte, M.; Alberto, F.; Serrão, Ester
    Although 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.
  • Genetic structure at range edge: Low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations
    Publication . ARNAUD-HAOND, Sophie; Teixeira, Sara; Massa, S. I.; Billot, C.; Saenger, P.; Coupland, G.; Duarte, C. M.; Serrão, Ester
    Understanding the genetic composition and mating systems of edge populations provides important insights into the environmental and demographic factors shaping species’ distribution ranges. We analysed samples of the mangrove Avicennia marina from Vietnam, northern Philippines and Australia, with microsatellite markers. We compared genetic diversity and structure in edge (Southeast Asia, and Southern Australia) and core (North and Eastern Australia) populations, and also compared our results with previously published data from core and southern edge populations. Comparisons highlighted significantly reduced gene diversity and higher genetic structure in both margins compared to core populations, which can be attributed to very low effective population size, pollinator scarcity and high environmental pressure at distribution margins. The estimated level of inbreeding was significantly higher in northeastern populations compared to core and southern populations. This suggests that despite the high genetic load usually associated with inbreeding, inbreeding or even selfing may be advantageous in margin habitats due to the possible advantages of reproductive assurance, or local adaptation. The very high level of genetic structure and inbreeding show that populations of A. marina are functioning as independent evolutionary units more than as components of a metapopulation system connected by gene flow. The combinations of those characteristics make these peripheral populations likely to develop local adaptations and therefore to be of particular interest for conservation strategies as well as for adaptation to possible future environmental changes.
  • Evolutionary and ecological trees and networks
    Publication . Hernández-García, E.; Herrada, E. A.; Rozenfeld, A. F.; Tessone, C. J.; Eguíluz, Víctor M.; Duarte, C. M.; ARNAUD-HAOND, Sophie; Serrão, Ester
    Evolutionary relationships between species are usually represented in phylogenies, i.e. evolutionary trees, which are a type of networks. The terminal nodes of these trees represent species, which are made of individuals and populations among which gene flow occurs. This flow can also be represented as a network. In this paper we briefly show some properties of these complex networks of evolutionary and ecological relationships. First, we characterize large scale evolutionary relationships in the Tree of Life by a degree distribution. Second, we represent genetic relationships between individuals of a Mediterranean marine plant, Posidonia oceanica, in terms of a Minimum Spanning Tree. Finally, relationships among plant shoots inside populations are represented as networks of genetic similarity.
  • Vicariance patterns in the Mediterranean Sea: East-west cleavage and low dispersal in the endemic seagrass Posidonia oceanica
    Publication . ARNAUD-HAOND, Sophie; Migliaccio, M.; Diaz-Almela, E.; Teixeira, Sara; Van De Vliet, M. S.; Alberto, F.; Procaccini, G.; Duarte, C. M.; Serrão, Ester
    Aim  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.
  • Travelling in time with networks: revealing present day hybridization versus ancestral polymorphism between two species of brown algae, Fucus vesiculosus and F. spiralis
    Publication . Moalic, Y.; ARNAUD-HAOND, Sophie; Perrin, C.; Pearson, G. A.; Serrão, Ester
    Background: Hybridization or divergence between sympatric sister species provides a natural laboratory to study speciation processes. The shared polymorphism in sister species may either be ancestral or derive from hybridization, and the accuracy of analytic methods used thus far to derive convincing evidence for the occurrence of present day hybridization is largely debated. Results: Here we propose the application of network analysis to test for the occurrence of present day hybridization between the two species of brown algae Fucus spiralis and F. vesiculosus. Individual-centered networks were analyzed on the basis of microsatellite genotypes from North Africa to the Pacific American coast, through the North Atlantic. Two genetic distances integrating different time steps were used, the Rozenfeld (RD; based on alleles divergence) and the Shared Allele (SAD; based on alleles identity) distances. A diagnostic level of genotype divergence and clustering of individuals from each species was obtained through RD while screening for exchanges through putative hybridization was facilitated using SAD. Intermediate individuals linking both clusters on the RD network were those sampled at the limits of the sympatric zone in Northwest Iberia. Conclusion: These results suggesting rare hybridization were confirmed by simulation of hybrids and F2 with directed backcrosses. Comparison with the Bayesian method STRUCTURE confirmed the usefulness of both approaches and emphasized the reliability of network analysis to unravel and study hybridization.