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  • Population genetics of Zostera noltii along the west Iberian coast: Consequences of small population size, habitat discontinuity and near-shore currents
    Publication . Diekmann, O. E.; Coyer, J. A.; Ferreira, J.; Olsen, J. L.; Stam, W. T.; Pearson, G. A.; Serrão, Ester
    The effects of oceanographic patterns on marine genetic biodiversity along the SW Iberian Peninsula are poorly understood. We addressed the question of whether gene flow in this region depends solely on geographic distance between isolated patches of suitable habitat or if there are superimposed effects correlated with other factors such as current patterns. Zostera noltii, the dwarf eelgrass, is the keystone habitat-structuring seagrass species on intertidal mudflats along the Iberian west coast. We used 9 microsatellite loci to analyze population genetic diversity and differentiation for all existing 8 populations from NW Spain (Ria de Vigo) to SW Spain (Puerto Real, Cadiz). Populations are highly genetically differentiated as shown by high significant FST,Wright’s fixation index, (0.08 to 0.26) values. A neighbor-joining tree based on Reynold’s distances computed from allele frequencies revealed a split between northern and southern populations (bootstrap support of 84%). This pattern of differentiation can be explained by (1) ocean surface current patterns present during Z. noltii’s reproductive season which cause a dispersal barrier between the northern and southern populations of this region, (2) habitat isolation, due to large geographic distances between suitable habitats, preventing frequent gene flow, and (3) small effective population sizes, causing high drift and thus faster differentiation rates.
  • Genetic and oceanographic tools reveal high population connectivity and diversity in the endangered pen shell Pinna nobilis
    Publication . Wesselmann, Marlene; Gonzalez-Wanguemert, Mercedes; Serrao, Ester A.; Engelen, Aschwin H.; Renault, Lionel; Garcia-March, Jose R.; Duarte, Carlos M.; Hendriks, Iris
    For marine meta-populations with source-sink dynamics knowledge about genetic connectivity is important to conserve biodiversity and design marine protected areas (MPAs). We evaluate connectivity of a Mediterranean sessile species, Pinna nobilis. To address a large geographical scale, partial sequences of cytochrome oxidase I (COI, 590 bp) were used to evaluate phylogeographical patterns in the Western Mediterranean, and in the whole basin using overlapping sequences from the literature (243 bp). Additionally, we combined (1) larval trajectories based on oceanographic currents and early life-history traits and (2) 10 highly polymorphic microsatellite loci collected in the Western Mediterranean. COI results provided evidence for high diversity and low inter-population differentiation. Microsatellite genotypes showed increasing genetic differentiation with oceanographic transport time (isolation by oceanographic distance (IBD) set by marine currents). Genetic differentiation was detected between Banyuls and Murcia and between Murcia and Mallorca. However, no genetic break was detected between the Balearic populations and the mainland. Migration rates together with numerical Lagrangian simulations showed that (i) the Ebro Delta is a larval source for the Balearic populations (ii) Alicante is a sink population, accumulating allelic diversity from nearby populations. The inferred connectivity can be applied in the development of MPA networks in the Western Mediterranean.
  • Past climate-driven range shifts structuring intraspecific biodiversity levels of the giant kelp (Macrocystis pyrifera) at global scales
    Publication . Assis, Jorge; Alberto, Filipe; Macaya, Erasmo C.; Coelho, Nelson; Faugeron, Sylvain; Pearson, Gareth; Ladah, Lydia; Reed, Daniel C.; Raimondi, Peter; Mansilla, Andrés; Brickle, Paul; Zuccarello, Giuseppe C.; Serrao, Ester
    The paradigm of past climate-driven range shifts structuring the distribution of marine intraspecific biodiversity lacks replication in biological models exposed to comparable limiting conditions in independent regions. This may lead to confounding effects unlinked to climate drivers. We aim to fill in this gap by asking whether the global distribution of intraspecific biodiversity of giant kelp (Macrocystis pyrifera) is explained by past climate changes occurring across the two hemispheres. We compared the species' population genetic diversity and structure inferred with microsatellite markers, with range shifts and long-term refugial regions predicted with species distribution modelling (SDM) from the last glacial maximum (LGM) to the present. The broad antitropical distribution of Macrocystis pyrifera is composed by six significantly differentiated genetic groups, for which current genetic diversity levels match the expectations of past climate changes. Range shifts from the LGM to the present structured low latitude refugial regions where genetic relics with higher and unique diversity were found (particularly in the Channel Islands of California and in Peru), while post-glacial expansions following similar to 40% range contraction explained extensive regions with homogenous reduced diversity. The estimated effect of past climate-driven range shifts was comparable between hemispheres, largely demonstrating that the distribution of intraspecific marine biodiversity can be structured by comparable evolutionary forces across the global ocean. Additionally, the differentiation and endemicity of regional genetic groups, confers high conservation value to these localized intraspecific biodiversity hotspots of giant kelp forests.
  • Population genetics of dwarf eelgrass Zostera noltii throughout its biogeographic range
    Publication . 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.
  • Surfing the wave on a borrowed board: Range expansion and spread of introgressed organellar genomes in the seaweed Fucus ceranoides L.
    Publication . Neiva, J.; Pearson, G. A.; Valero, Myriam; Serrão, Ester
    For many taxa, introgression represents an important source of genetic variation, but the specific contexts allowing locally introgressed material to spread and largely replace native allelic lineages throughout a species range remain poorly understood. Recent demographic-genetic simulations of spatial expansions show that the stochastic surfing of alien alleles during range expansions may constitute a general mechanism leading to extensive introgression, but empirical evidence remain scarce and difficult to distinguish from selection. In this study, we report a compelling case of such a phenomenon in the estuarine alga Fucus ceranoides. We re-assessed the phylogenetic relationships among F. ceranoides and its marine congeners F. vesiculosus and F. spiralis using nuclear, mitochondrial and chloroplast sequence data, and conducted a mtDNA phylogeographic survey in F. ceranoides. Our phylogenetic analyses revealed a recent and asymmetric introgression of a single F. vesiculosus cytoplasm into F. ceranoides. The phylogeographic scope of introgression was striking, with native and introgressed mtDNA displaying disjunct distributions south and north of the English Channel. A putative Pleistocene climatic refugium was detected in NW Iberia, and the extensive and exclusive spread of the alien cytoplasm throughout Northern Europe was inferred to have occurred concurrently with the species post-glacial, northwards range expansion. This massive spread of a foreign organelle throughout the entire post-glacial recolonization range represents good empirical evidence of an alien cytoplasm surfing the wave of a range expansion and the first description of such a phenomenon in the marine realm.
  • Species distribution models and mitochondrial DNA phylogeography suggest an extensive biogeographical shift in the high-intertidal seaweed Pelvetia canaliculata
    Publication . Neiva, J.; Assis, J.; Fernandes, F.; Pearson, G. A.; Serrão, Ester
    Aim: Species distributions have been continuously adjusting to changing climatic conditions throughout the glacial–interglacial cycles. In the marine realm, evidence suggests that latitudinal range shifts, involving both spatial expansions and trailingedge contractions, may represent a common response to climatic oscillations. The biogeographical histories of coastal organisms, however, have been inferred primarily using molecular markers, potentially overlooking past range dynamics beyond contemporary rear edges. In this study we combined species distribution models (SDMs) and mitochondrial DNA (mtDNA) data to investigate the biogeographical history of the high-intertidal seaweed Pelvetia canaliculata. We investigated the hypotheses that its distribution is set by both marine and terrestrial climates and that its range has shifted northwards since the Last Glacial Maximum. Location North-eastern Atlantic intertidal from Portugal to Norway. Methods: In total, 432 individuals at 27 sites covering the extant range of Pelvetia canaliculata were sampled and sequenced for a c. 500 bp mtDNA intergenic spacer. A niche model was developed using marine and terrestrial variables. Range dynamics were reconstructed based on the geographical patterns of genetic variation and on the SDM projections for the Last Glacial Maximum (LGM) and the present. Results: The best distribution models incorporated both marine and terrestrial variables. LGM projections revealed suitable habitat between southern Morocco and the periglacial shorelines of the Celtic Sea. Pelvetia canaliculata exhibited a highly structured phylogeography, being subdivided into three largely disjunct lineages, two of them endemic to Iberia. The central/northern European lineage exhibited the highest haplotypic diversity and showed a consistent decline in nucleotide diversity and haplotypic richness at higher latitudes. Main conclusions: Assuming species/climate equilibrium, SDMs supported the hypothesis of a post-glacial latitudinal range shift. Molecular variation revealed contrasting demographic behaviours in Iberian and periglacial regions. In Iberia the low haplotypic diversity suggested complex range dynamics that are not fully captured by SDM projections. Periglacial regions, identified as the source of poleward colonization, were inferred to have been comparatively more stable. Greater attention should be paid to marine range dynamics at low-latitude range margins, particularly in genetically structured low-dispersal species exhibiting southern endemic variation.
  • Genetic Divergence for the Amphibian Pleurodeles waltl in Southwest Portugal: Dispersal Barriers Shaping Geographic Patterns
    Publication . Van Vliet, Mirjam; Diekmann, Onno; Machado, Margarida; Beebee, Trevor J. C.; Beja, Pedro; Serrao, Ester A.
    Dispersal and vicariance are the principal mechanisms responsible for the formation of biogeographic patterns, driven or maintained by the role of past and current barriers to dispersal. Southwest Portugal harbors a rich endemic fauna and flora where strongly differentiated taxa can be observed, suggesting ancient isolating mechanisms acted in this region. In this study, we used information from two partial mitochondrial sequences, combined with information from microsatellite loci and amplification success, to investigate biogeographic patterns of genetic divergence in populations of Pleurodeles waltl in Portugal. Our results demonstrate genetic differentiation at different time frames creating distinct populations in southwest Portugal, which might have arisen following isolation by a large river estuary and mountainous barriers. Habitat destruction associated with agricultural intensification raises conservation concerns over the unique biodiversity in this region.
  • Palaeoclimatic conditions in the Mediterranean explain genetic diversity of Posidonia oceanica seagrass meadows
    Publication . Chefaoui, Rosa; Duarte, Carlos M.; Serrao, Ester A.
    Past environmental conditions in the Mediterranean Sea have been proposed as main drivers of the current patterns of distribution of genetic structure of the seagrass Posidonia oceanica, the foundation species of one of the most important ecosystems in the Mediterranean Sea. Yet, the location of cold climate refugia (persistence regions) for this species during the Last Glacial Maximum (LGM) is not clear, precluding the understanding of its biogeographical history. We used Ecological Niche Modelling together with existing phylogeographic data to locate Pleistocene refugia in the Mediterranean Sea and to develop a hypothetical past biogeographical distribution able to explain the genetic diversity presently found in P. oceanica meadows. To do that, we used an ensemble approach of six predictive algorithms and two Ocean General Circulation Models. The minimum SST in winter and the maximum SST in summer allowed us to hindcast the species range during the LGM. We found separate glacial refugia in each Mediterranean basin and in the Central region. Altogether, the results suggest that the Central region of the Mediterranean Sea was the most relevant cold climate refugium, supporting the hypothesis that long-term persistence there allowed the region to develop and retain its presently high proportion of the global genetic diversity of P. oceanica.
  • North Atlantic phylogeography and large-scale population differentiation of the seagrass Zostera marina L.
    Publication . Olsen, J. L.; Stam, W. T.; Coyer, J. A.; Reusch, T. B. H.; Billingham, M. R.; Boström, C.; Calvert, E.; Christie, H.; Granger, S.; La Lumière, R.; Milchakova, N.; Oudot-Le Secq, M.- P.; Procaccini, G.; Sanjabi, B.; Serrão, Ester; Veldsink, J.; Widdicombe, S.; Wyllie-Echeverria, S.
    As the most widespread seagrass in temperate waters of the Northern Hemisphere, Zostera marina provides a unique opportunity to investigate the extent to which the historical legacy of the last glacial maximum (LGM18 000–10 000 years BP) is detectable in modern population genetic structure. We used sequences from the nuclear rDNA–internal transcribed spacer (ITS) and chloroplast mat K-intron, and nine microsatellite loci to survey 49 populations (> 2000 individuals) from throughout the species’ range. Minimal sequence variation between Pacific and Atlantic populations combined with biogeographical groupings derived from the microsatellite data, suggest that the trans-Arctic connection is currently open. The east Pacific and west Atlantic are more connected than either is to the east Atlantic. Allelic richness was almost two-fold higher in the Pacific. Populations from putative Atlantic refugia now represent the southern edges of the distribution and are not genetically diverse. Unexpectedly, the highest allelic diversity was observed in the North Sea–Wadden Sea–southwest Baltic region. Except for the Mediterranean and Black Seas, significant isolation-by-distance was found from ~150 to 5000 km. A transition from weak to strong isolation-by-distance occurred at ~150 km among northern European populations suggesting this scale as the natural limit for dispersal within the metapopulation. Links between historical and contemporary processes are discussed in terms of the projected effects of climate change on coastal marine plants. The identification of a high genetic diversity hotspot in Northern Europe provides a basis for restoration decisions.
  • Evolution and diversification within the intertidal brown macroalgae Fucus spiralis/F. vesiculosus species complex in the North Atlantic
    Publication . Coyer, J. A.; Hoarau, G.; Costa, J. F.; Hogerdijk, B.; Serrão, Ester; Billard, E.; Valero, Myriam; Pearson, G. A.; Olsen, J. L.
    We examined 733 individuals of Fucusspiralis from 21 locations and 1093 Fucusvesiculosus individuals from 37 locations throughout their northern hemisphere ranges using nuclear and mitochondrial markers. Three genetic entities of F. spiralis were recovered. In northern and sympatric populations, the presence of "F. spiralis Low" in the mid-intertidal and "F. spiralis High" in the high-intertidal was confirmed and both co-occurred with the sister species F. vesiculosus. The third and newly-discovered entity, "F. spiralis South", was present mainly in the southern range, where it did not co-occur with F. vesiculosus. The South entity diverged early in allopatry, then hybridized with F. vesiculosus in sympatry to produce F. spiralis Low. Ongoing parallel evolution of F. spiralis Low and F. spiralis High is most likely due to habitat preference/local selection and maintained by preferentially selfing reproductive strategies. Contemporary populations of F. spiralis throughout the North Atlantic stem from a glacial refugium around Brittany involving F. spiralis High; F. spiralis South was probably unaffected by glacial episodes. Exponential population expansion for F. vesiculosus began during the Cromer and/Holstein interglacial period (300,000-200,000 yrs BP). Following the last glacial maximum (30,000-22,000 yrs BP), a single mtDNA haplotype from a glacial refugium in SW Ireland colonized Scandinavia, the Central Atlantic islands, and the W Atlantic.