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- Genes left behind: Climate change threatens cryptic genetic diversity in the canopy-forming seaweed bifurcaria bifurcataPublication . Neiva, J.; Assis, J.; Coelho, Nelson; Fernandes, Francisco; Pearson, Gareth; Serrao, Ester A.The global redistribution of biodiversity will intensify in the coming decades of climate change, making projections of species range shifts and of associated genetic losses important components of conservation planning. Highly-structured marine species, notably brown seaweeds, often harbor unique genetic variation at warmer low-latitude rear edges and thus are of particular concern. Here, a combination of Ecological Niche Models (ENMs) and molecular data is used to forecast the potential near-future impacts of climate change for a warm-temperate, canopy forming seaweed, Bifurcaria bifurcata. ENMs for B. bifurcata were developed using marine and terrestrial climatic variables, and its range projected for 2040-50 and 2090-2100 under two greenhouse emission scenarios. Geographical patterns of genetic diversity were assessed by screening 18 populations spawning the entire distribution for two organelle genes and 6 microsatellite markers. The southern limit of B. bifurcata was predicted to shift northwards to central Morocco by the mid-century. By 2090-2100, depending on the emission scenario, it could either retreat further north to western Iberia or be relocated back to Western Sahara. At the opposing margin, B. bifurcata was predicted to expand its range to Scotland or even Norway. Microsatellite diversity and endemism were highest in Morocco, where a unique and very restricted lineage was also identified. Our results imply that B. bifurcata will maintain a relatively broad latitudinal distribution. Although its persistence is not threatened, the predicted extirpation of a unique southern lineage or even the entire Moroccan diversity hotspot will erase a rich evolutionary legacy and shrink global diversity to current (low) European levels. NW Africa and similarly understudied southern regions should receive added attention if expected range changes and diversity loss of warm-temperate species is not to occur unnoticed.
- Habitat continuity and geographic distance predict population genetic differentiation in giant kelpPublication . Filipe, A.; Raimondi, P. T.; Reed, D. C.; Coelho, Nelson; Raphael, L.; Allison, W.; Serrão, EsterIsolation by distance (IBD) models are widely used to predict levels of genetic connectivity as a function of Euclidean distance, and although recent studies have used GIS-landscape ecological approaches to improve the predictability of spatial genetic structure, few if any have addressed the effect of habitat continuity on gene flow. Landscape effects on genetic connectivity are even less understood in marine populations, where habitat mapping is particularly challenging. In this study, we model spatial genetic structure of a habitat-structuring species, the giant kelp Macrocystis pyrifera, using highly variable microsatellite markers. GIS mapping was used to characterize habitat continuity and distance between sampling sites along the mainland coast of the Santa Barbara Channel, and their roles as predictors of genetic differentiation were evaluated. Mean dispersal distance (σ) and effective population size (Ne) were estimated by comparing our IBD slope with those from simulations incorporating habitat continuity and spore dispersal characteristics of the study area. We found an allelic richness of 7–50 alleles/locus, which to our knowledge is the highest reported for macroalgae. The best regression model relating genetic distance to habitat variables included both geographic distance and habitat continuity, which were respectively, positively and negatively related to genetic distance. Our results provide strong support for a dependence of gene flow on both distance and habitat continuity and elucidate the combination of Ne and σ that explained genetic differentiation.
- Deep reefs are climatic refugia for genetic diversity of marine forestsPublication . Assis, J.; Coelho, Nelson Castilho; Lamy, Thomas; Valero, Myriam; Alberto, Filipe; Serrão, EsterAimPast climate-driven range shifts shaped intraspecific diversities of species world-wide. Earlier studies, focused on glacial refugia, might have overlooked genetic erosion at lower latitudes associated with warmer periods. For marine species able to colonize deeper waters, depth shifts might be important for local persistence, preventing some latitudinal shifts, analogous to elevational refugia in terrestrial habitats. In this study, we asked whether past latitudinal or depth range shifts explain extant gene pools in Saccorhiza polyschides, a large habitat structuring brown alga distributed from coastal to offshore deep reefs.LocationNorth-east Atlantic and western Mediterranean basin.MethodsGenetic structure and diversity were inferred using seven microsatellite loci, for 27 sites throughout the entire distributional range. Ecological niche modelling (ENM) was performed with and without information about genetic structure (sub-taxon niche structure) to predict distributions for the Last Glacial Maximum (LGM), the warmer Mid-Holocene (MH) and the present.ResultsBoth ENM approaches predicted a wider potential distribution in deeper waters than is presently known, a post-glacial expansion to northern shores and the extirpation of southern edges during the warmer MH. Genetic data corroborated range dynamics, revealing three major genetic groups with current boundaries in the Bay of Biscay and the Lisbon coastal region, pinpointing ancient refugial origins. Despite extensive southern range contraction, the southernmost warmer regions are still the richest in genetic diversity, indicating long-term persistence of large populations. ENMs suggested that this could only have been possible due to stable refugia in deeper reefs.Main conclusionsThe global distribution of gene pools of temperate marine forests is explained by past range shifts that structured both latitudinal glacial refugia and depth refugia during warmer periods. Deep rear edge populations play a fundamental role during periods of extreme climate, allowing persistence and retaining some of the largest genetic diversity pools of the species' distribution.
- Microsatellite markers for the Arctic copepod Calanus glacialis and cross-amplification with C. finmarchicusPublication . Weydmann, Agata; Coelho, Nelson; Ramos, Ana; Serrao, Ester A.; Pearson, GarethCalanus glacialis is a major component of Arctic zooplankton and a keystone species in Arctic marine ecosystems. Due to the observed climate warming, its numbers are being reduced to the advantage of a sibling Atlantic species Calanus finmarchicus. We developed and characterized the first set of microsatellite markers in this species to investigate its population genetic structure and dispersal capabilities. Nine polymorphic loci displayed an average of 7.3 alleles (range between 2 and 13) and the levels of expected heterozygosity ranged from 0.039 to 0.806. These provide a valuable tool to understand present connectivity patterns across Arctic regions, look for signatures of past climate effects and predict the response to future climate-driven environmental changes. Additionally, due to the cross-amplification with C. finmarchicus, the markers can be used to discriminate between these sibling species.
- Characterization of ten highly polymorphic microsatellite loci for the intertidal mussel Perna perna, and cross species amplification within the genusPublication . Coelho, Nelson; I Zardi, Gerardo; Pearson, G. A.; Serrão, Ester; Nicastro, Katy RThe brown mussel Perna perna (Linnaeus, 1758) is a dominant constituent of intertidal communities and a strong invader with multiple non-native populations distributed around the world. In a previous study, two polymorphic microsatellite loci were developed and used to determine population-level genetic diversity in invasive and native P. perna populations. However, higher number of microsatellite markers are required for reliable population genetic studies. In this context, in order to understand P. perna origins and history of invasion and to compare population genetic structure in native versus invaded areas, we developed 10 polymorphic microsatellite markers. Findings Described microsatellite markers were developed from an enriched genomic library. Analyses and characterization of loci using 20 individuals from a population in Western Sahara revealed on average 11 alleles per locus (range: 5–27) and mean gene diversity of 0.75 (range: 0.31 - 0.95). One primer pair revealed possible linkage disequilibrium while heterozygote deficiency was significant at four loci. Six of these markers cross-amplified in P. canaliculus (origin: New Zealand). Conclusions Developed markers will be useful in addressing a variety of questions concerning P. perna, including dispersal scales, genetic variation and population structure, in both native and invaded areas.
- Cryptic diversity, geographical endemism and allopolyploidy in NE Pacific seaweedsPublication . Neiva, J.; Serrão, Ester; Anderson, Laura; Raimondi, Peter T.; Martins, Neusa; Gouveia, Licínia; Paulino, Cristina; Coelho, Nelson C.; Miller, Kathy A.; Reed, Daniel C.; Ladah, Lydia; Pearson, G. A.Background Molecular markers are revealing a much more diverse and evolutionarily complex picture of marine biodiversity than previously anticipated. Cryptic and/or endemic marine species are continually being found throughout the world oceans, predominantly in inconspicuous tropical groups but also in larger, canopy-forming taxa from well studied temperate regions. Interspecific hybridization has also been found to be prevalent in many marine groups, for instance within dense congeneric assemblages, with introgressive gene-flow being the most common outcome. Here, using a congeneric phylogeographic approach, we investigated two monotypic and geographically complementary sister genera of north-east Pacific intertidal seaweeds (Hesperophycus and Pelvetiopsis), for which preliminary molecular tests revealed unexpected conflicts consistent with unrecognized cryptic diversity and hybridization. Results The three recovered mtDNA clades did not match a priori species delimitations. H. californicus was congruent, whereas widespread P. limitata encompassed two additional narrow-endemic species from California - P. arborescens (here genetically confirmed) and P. hybrida sp. nov. The congruence between the genotypic clusters and the mtDNA clades was absolute. Fixed heterozygosity was apparent in a high proportion of loci in P. limitata and P. hybrida, with genetic analyses showing that the latter was composed of both H. californicus and P. arborescens genomes. All four inferred species could be distinguished based on their general morphology. Conclusions This study confirmed additional diversity and reticulation within NE Pacific Hesperophycus/Pelvetiopsis, including the validity of the much endangered, modern climatic relict P. arborescens, and the identification of a new, stable allopolyploid species (P. hybrida) with clearly discernable ancestry (♀ H. californicus x ♂ P. arborescens), morphology, and geographical distribution. Allopolyploid speciation is otherwise completely unknown in brown seaweeds, and its unique occurrence within this genus (P. limitata possibly representing a second example) remains enigmatic. The taxonomic separation of Hesperophycus and Pelvetiopsis is not supported and the genera should be synonymized; we retain only the latter. The transitional coastline between Point Conception and Monterey Bay represented a diversity hotspot for the genus and the likely sites of extraordinary evolutionary events of allopolyploid speciation at sympatric range contact zones. This study pinpoints how much diversity (and evolutionary processes) potentially remains undiscovered even on a conspicuous seaweed genus from the well-studied Californian intertidal shores let alone in other, less studied marine groups and regions/depths.
- Pan-Arctic population of the keystone copepod Calanus glacialisPublication . Weydmann, Agata; Coelho, Nelson C.; Serrão, Ester; Burzynski, Artur; Pearson, G. A.The copepod Calanus glacialis is endemic to the Arctic Ocean and peripheral seas and forms a key component of the Arctic marine ecosystems. It is the major contributor to zooplankton biomass, a predominant grazer, and an important prey for seabirds, and fish. As for a planktonic species, its dispersal is expected to be widespread and mediated by ocean currents. However, complex circulation patterns and the existence of semi-enclosed fjords and seas in the Arctic can be hypothesized to influence the population genetic structure of this species. In this study, we aimed to infer patterns of connectivity between populations of C. glacialis distributed around the Arctic and across putative barriers formed by oceanographic currents and semi-enclosed fjords and seas. To achieve this, we used 11 polymorphic microsatellite loci to genotype 189 individuals from 7 locations: Svalbard fjords (Kongsfjorden, Hornsund, Isfjorden, Rijpfjorden, and Storfjorden), White Sea, and Amundsen Gulf, thus providing greater genetic resolution over a larger biogeographical scale than in previous studies. The results revealed a lack of structure among all seven locations around the Arctic, indicating a panmictic population with large-scale gene flow. This study also supports the hypothesis that the planktonic fauna of the White Sea is not isolated from that of the other Arctic regions.
- Individual-based genetic analyses support asexual hydrochory dispersal in Zostera nolteiPublication . Berković, Buga; Coelho, Nelson; Gouveia, Licínia; Serrao, Ester; Alberto, FilipeDispersal beyond the local patch in clonal plants was typically thought to result from sexual reproduction via seed dispersal. However, evidence for the separation, transport by water, and re-establishment of asexual propagules (asexual hydrochory) is mounting suggesting other important means of dispersal in aquatic plants. Using an unprecedented sampling size and microsatellite genetic identification, we describe the distribution of seagrass clones along tens of km within a coastal lagoon in Southern Portugal. Our spatially explicit individual-based sampling design covered 84 km(2) and collected 3 185 Zostera noltei ramets from 803 sites. We estimated clone age, assuming rhizome elongation as the only mechanism of clone spread, and contrasted it with paleo-oceanographic sea level change. We also studied the association between a source of disturbance and the location of large clones. A total of 16 clones were sampled more than 10 times and the most abundant one was sampled 59 times. The largest distance between two samples from the same clone was 26.4 km and a total of 58 and 10 clones were sampled across more than 2 and 10 km, respectively. The number of extremely large clone sizes, and their old ages when assuming the rhizome elongation as the single causal mechanism, suggests other processes are behind the span of these clones. We discuss how the dispersal of vegetative fragments in a stepping-stone manner might have produced this pattern. We found higher probabilities to sample large clones away from the lagoon inlet, considered a source of disturbance. This study corroborates previous experiments on the success of transport and re-establishment of asexual fragments and supports the hypothesis that asexual hydrochory is responsible for the extent of these clones.
- Characterization of 12 polymorphic microsatellite markers in the sugar kelp Saccharina latissimaPublication . Paulino, Cristina; Neiva, J.; Coelho, Nelson C.; Aires, Tânia; Marba, Núria; Krause-Jensen, Dorte; Serrão, EsterSaccharina latissima is an ecologically and economically important kelp species native to the coastal regions of the Northern Hemisphere. This species has considerable phylogeographic structure and morphological plasticity, but lack of resolution of available genetic markers prevents a finer characterization of its genetic diversity and structure. Here, we describe 12 microsatellite loci identified in silico in a genomic library, and assess their polymorphism in three distant populations. Allelic richness at the species level was relatively high (5-23 alleles per locus), as was gene diversity within populations (0.42 < H (E) < 0.62). In addition, individuals readily form distinct genotypic clusters matching their populations of origin. The variation detected confirms the great potential of these markers to investigate the biogeography and population dynamics of S. latissima, and to better characterize its genetic resources for the establishing farming industry.
- Isolation by oceanographic distance explains genetic structure for Macrocystis pyrifera in the Santa Barbara ChannelPublication . Alberto, F.; Raimondi, P. T.; Reed, D. C.; Watson, J. R.; Siegel, D. A.; Mitarai, S.; Coelho, N. C.; Serrão, EsterOcean currents are expected to be the predominant environmental factor influencing the dispersal of planktonic larvae or spores; yet, their characterization as predictors of marine connectivity has been hindered by a lack of understanding of how best to use oceanographic data. We used a high-resolution oceanographic model output and Lagrangian particle simulations to derive oceanographic distances (hereafter called transport times) between sites studied for Macrocystis pyrifera genetic differentiation. We build upon the classical isolation-by-distance regression model by asking how much additional variability in genetic differentiation is explained when adding transport time as predictor. We explored the extent to which gene flow is dependent upon seasonal changes in ocean circulation. Because oceanographic transport between two sites is inherently asymmetric, we also compare the explanatory power of models using the minimum or the mean transport times. Finally, we compare the direction of connectivity as estimated by the oceanographic model and genetic assignment tests. We show that the minimum transport time had higher explanatory power than the mean transport time, revealing the importance of considering asymmetry in ocean currents when modelling gene flow. Genetic assignment tests were much less effective in determining asymmetry in gene flow. Summer-derived transport times, in particular for the month of June, which had the strongest current speed, greatest asymmetry and highest spore production, resulted in the best-fit model explaining twice the variability in genetic differentiation relative to models that use geographic distance or habitat continuity. The best overall model also included habitat continuity and explained 65% of the variation in genetic differentiation among sites.