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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.
  • Genetic diversity increases with depth in red gorgonian populations of the Mediterranean Sea and the Atlantic Ocean
    Publication . Pilczynska, Joanna; Cocito, Silvia; Boavida, Joana; Serrao, Ester; Assis, J.; Fragkopoulou, Eliza; Queiroga, Henrique
    In the ocean, the variability of environmental conditions found along depth gradients exposes populations to contrasting levels of perturbation, which can be reflected in the overall patterns of species genetic diversity. At shallow sites, resource availability may structure large, persistent and well-connected populations with higher levels of diversity. In contrast, the more extreme conditions, such as thermal stress during heat waves, can lead to population bottlenecks and genetic erosion, inverting the natural expectation. Here we examine how genetic diversity varies along depth for a long-lived, important ecosystem-structuring species, the red gorgonian, Paramuricea clavata.
  • Climate-induced range shifts shaped the present and threaten the future genetic variability of a marine brown alga in the Northwest Pacific
    Publication . Song, Xiao-Han; Assis, Jorge; Jie Zhang, Jie; Gao, Xu; Cho, Han-Gil; Duan, De-Lin; Serrao, Ester; Hu, Zi-Min
    Glaciation-induced environmental changes during the last glacial maximum (LGM) have strongly influenced species' distributions and genetic diversity patterns in the northern high latitudes. However, these effects have seldom been assessed on sessile species in the Northwest Pacific. Herein, we chose the brown alga Sargassum thunbergii to test this hypothesis, by comparing present population genetic variability with inferred geographical range shifts from the LGM to the present, estimated with species distribution modelling (SDM). Projections for contrasting scenarios of future climate change were also developed to anticipate genetic diversity losses at regional scales. Results showed that S. thunbergii harbours strikingly rich genetic diversity and multiple divergent lineages in the centre-northern range of its distribution, in contrast with a poorer genetically distinct lineage in the southern range. SDM hindcasted refugial persistence in the southern range during the LGM as well as post-LGM expansion of 18 degrees of latitude northward. Approximate Bayesian computation (ABC) analysis further suggested that the multiple divergent lineages in the centre-northern range limit stem from post-LGM colonization from the southern survived lineage. This suggests divergence due to demographic bottlenecks during range expansion and massive genetic diversity loss during post-LGM contraction in the south. The projected future range of S. thunbergii highlights the threat to unique gene pools that might be lost under global changes.
  • 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.
  • Is asexual reproduction more important at geographical limits? A genetic study of the seagrass Zostera marina in the Ria Formosa, Portugal
    Publication . Billingham, M. R.; Reusch, T. B. H.; Alberto, F.; Serrão, Ester
    In 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.
  • Polymorphic microsatellite markers in the brown seaweed Fucus vesiculosus
    Publication . Candeias, Rui; Casado-Amezúa, Pilar; Pearson, G. A.; Serrão, Ester; Teixeira, Sara
    Background: 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.
  • Spectrum of genetic diversity and networks of clonal organisms
    Publication . Rozenfeld, A. F.; ARNAUD-HAOND, Sophie; Hernández-García, E.; Eguíluz, Víctor M.; Matías, M. A.; Serrão, Ester; Duarte, C. M.
    Clonal reproduction characterizes a wide range of species including clonal plants in terrestrial and aquatic ecosystems, and clonal microbes such as bacteria and parasitic protozoa, with a key role in human health and ecosystem processes. Clonal organisms present a particular challenge in population genetics because, in addition to the possible existence of replicates of the same genotype in a given sample, some of the hypotheses and concepts underlying classical population genetics models are irreconcilable with clonality. The genetic structure and diversity of clonal populations were examined using a combination of new tools to analyse microsatellite data in the marine angiosperm Posidonia oceanica. These tools were based on examination of the frequency distribution of the genetic distance among ramets, termed the spectrum of genetic diversity (GDS), and of networks built on the basis of pairwise genetic distances among genets. Clonal growth and outcrossing are apparently dominant processes, whereas selfing and somatic mutations appear to be marginal, and the contribution of immigration seems to play a small role in adding genetic diversity to populations. The properties and topology of networks based on genetic distances showed a ‘small-world’ topology, characterized by a high degree of connectivity among nodes, and a substantial amount of substructure, revealing organization in subfamilies of closely related individuals. The combination of GDS and network tools proposed here helped in dissecting the influence of various evolutionary processes in shaping the intra-population genetic structure of the clonal organism investigated; these therefore represent promising analytical tools in population genetics.
  • Intraspecific genetic lineages of a marine mussel show behavioural divergence and spatial segregation over a tropical/subtropical biogeographic transition
    Publication . Zardi, Gerardo I.; Nicastro, Katy R; McQuaid, C. D.; Castilho, Rita; Costa, Joana; Serrão, Ester; Pearson, G. A.
    Background: Intraspecific variability is seen as a central component of biodiversity. We investigated genetic differentiation, contemporary patterns of demographic connectivity and intraspecific variation of adaptive behavioural traits in two lineages of an intertidal mussel (Perna perna) across a tropical/subtropical biogeographic transition. Results: Microsatellite analyses revealed clear genetic differentiation between western (temperate) and eastern (subtropical/tropical) populations, confirming divergence previously detected with mitochondrial (COI) and nuclear (ITS) markers. Gene flow between regions was predominantly east-to-west and was only moderate, with higher heterozygote deficiency where the two lineages co-occur. This can be explained by differential selection and/or oceanographic dynamics acting as a barrier to larval dispersal. Common garden experiments showed that gaping (periodic closure and opening of the shell) and attachment to the substratum differed significantly between the two lineages. Western individuals gaped more and attached less strongly to the substratum than eastern ones. Conclusions: These behavioural differences are consistent with the geographic and intertidal distributions of each lineage along sharp environmental clines, indicating their strong adaptive significance. We highlight the functional role of diversity below the species level in evolutionary trends and the need to understand this when predicting biodiversity responses to environmental change.
  • Microsatellite markers for the giant kelp macrocystis pyrifera
    Publication . Alberto, F.; Whitmer, A.; Coelho, N. C.; Zippay, M.; E, Varela-Álvarez; Raimondi, P. T.; Reed, D. C.; Serrão, Ester
    We report the isolation and characterization of 16 microsatellite loci to study the population genetics of the giant kelp, Macrocystis pyrifera. Markers were obtained by screening a genomic library enriched for microsatellite motifs. Of the 37 primer pairs defined, 16 amplified clean polymorphic microsatellites and are described. These loci identified a number of alleles ranging from three to forty (mean = 16.5, and gene diversity ranging from 0.469 to 0.930 (mean = 0.774). The isolation and characterization of these highly polymorphic markers will greatly benefit much needed studies on the molecular ecology of this important macroalga.
  • 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, Ester
    The 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.