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- Shift happens: trailing edge contraction associated with recent warming trends threatens a distinct genetic lineage in the marine macroalga Fucus vesiculosusPublication . Nicastro, Katy R; I Zardi, Gerardo; Teixeira, Sara; Neiva, J.; Serrão, Ester; Pearson, G. A.Significant effects of recent global climate change have already been observed in a variety of ecosystems, with evidence for shifts in species ranges, but rarely have such consequences been related to the changes in the species genetic pool. The stretch of Atlantic coast between North Africa and North Iberia is ideal for studying the relationship between species distribution and climate change as it includes the distributional limits of a considerable number of both cold- and warm-water species. We compared temporal changes in distribution of the canopy-forming alga Fucus vesiculosus with historical sea surface temperature (SST) patterns to draw links between range shifts and contemporary climate change. Moreover, we genetically characterized with microsatellite markers previously sampled extinct and extant populations in order to estimate resulting cryptic genetic erosion. Results Over the past 30 years, a geographic contraction of the southern range edge of this species has occurred, with a northward latitudinal shift of approximately 1,250 km. Additionally, a more restricted distributional decline was recorded in the Bay of Biscay. Coastal SST warming data over the last three decades revealed a significant increase in temperature along most of the studied coastline, averaging 0.214°C/decade. Importantly, the analysis of existing and extinct population samples clearly distinguished two genetically different groups, a northern and a southern clade. Because of the range contraction, the southern group is currently represented by very few extant populations. This southern edge range shift is thus causing the loss of a distinct component of the species genetic background. Conclusions We reveal a climate-correlated diversity loss below the species level, a process that could render the species more vulnerable to future environmental changes and affect its evolutionary potential. This is a remarkable case of genetic uniqueness of a vanishing cryptic genetic clade (southern clade).
- Drifting fronds and drifting alleles: range dynamics, local dispersal and habitat isolation shape the population structure of the estuarine seaweed Fucus ceranoidesPublication . Neiva, J.; Pearson, G. A.; Valero, Myriam; Serrão, EsterAim: The seaweed Fucus ceranoides is restricted to spatially discrete estuarine habitats and lacks planktonic dispersal phases; it is therefore expected to exhibit strong population differentiation. Its cold-temperate affinities and mtDNA variation imply that the northern part of the species’ range, where F. ceranoides is now ubiquitous, was recently colonized after the onset of the last deglaciation, potentially resulting in areas with greater genetic homogeneity. Here we examine the population structure of F. ceranoides to test these predictions, emphasizing the contrasting genetic signatures of limited dispersal in refugial versus recently colonized regions. Location: North-eastern Atlantic estuaries from Portugal to Norway. Methods: A total of 504 individuals from 21 estuarine sites spanning the entire range of F. ceranoides were sampled and genotyped for nine microsatellite loci. Population structure was inferred from several genotypic and allele-frequency analyses. Geographical patterns of genetic diversity were used to reconstruct the historical biogeography of the species. Results: Genetic diversity and regional population differentiation showed a consistent decline with increasing latitude. Southernmost populations harboured most of the endemic variation, whereas the northern populations (> 55 N) were almost fixed for the same alleles across loci. In southern and central regions of its distribution, F. ceranoides showed striking population subdivision, with many of the sampled estuaries corresponding to coherent genetic units that were easily discriminated from one another with standard clustering methods. Main conclusions: The geographical pattern of genetic diversity supports the long-term refugial status of Iberia and a post-glacial range expansion of F. ceranoides into previously glaciated latitudes. Despite the species’ capacity to colonize newly available habitats, the genetic structure of F. ceranoides outside the recently (re)colonized range reveals that gene flow between populations is extremely low. This study provides a remarkable example of how infrequent and spatially limited dispersal can have contrasting effects at the scales of metapopulation (connectivity) versus range dynamics (habitat tracking), and of how dispersal restrictions can result in either genetic divergence or homogeneity depending on the maturity and demographic conditions of the populations.
- 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, EsterFor 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 canaliculataPublication . Neiva, J.; Assis, J.; Fernandes, F.; Pearson, G. A.; Serrão, EsterAim: 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.
- 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.
- Fine-scale genetic breaks driven by historical rangedynamics and ongoing density-barrier effects in theestuarine seaweed Fucus ceranoides L.Publication . Neiva, J.; Pearson, G. A.; Valero, Myriam; Serrão, EsterFactors promoting the emergence of sharp phylogeographic breaks include restricted dispersal, habitat discontinuity, physical barriers, disruptive selection, mating incompatibility, genetic surfing and secondary contact. Disentangling the role of each in any particular system can be difficult, especially when species are evenly distributed across transition zones and dispersal barriers are not evident. The estuarine seaweed Fucus ceranoides provides a good example of highly differentiated populations along its most persistent distributional range at the present rear edge of the species distribution, in NW Iberia. Intrinsic dispersal restrictions are obvious in this species, but have not prevented F. ceranoides from vastly expanding its range northwards following the last glaciation, implying that additional factors are responsible for the lack of connectivity between neighbouring southern populations. In this study we analyze 22 consecutive populations of F. ceranoides along NW Iberia to investigate the processes generating and maintaining the observed high levels of regional genetic divergence. Results Variation at seven microsatellite loci and at mtDNA spacer sequences was concordant in revealing that Iberian F. ceranoides is composed of three divergent genetic clusters displaying nearly disjunct geographical distributions. Structure and AFC analyses detected two populations with an admixed nuclear background. Haplotypic diversity was high in the W sector and very low in the N sector. Within each genetic cluster, population structure was also pervasive, although shallower. Conclusions The deep divergence between sectors coupled with the lack of support for a role of oceanographic barriers in defining the location of breaks suggested 1) that the parapatric genetic sectors result from the regional reassembly of formerly vicariant sub-populations, and 2) that the genetic discontinuities at secondary contact zones (and elsewhere) are maintained despite normal migration rates. We conclude that colonization and immigration, as sources of gene-flow, have very different genetic effects. Migration between established populations is effectively too low to prevent their differentiation by drift or to smooth historical differences inherited from the colonization process. F. ceranoides, but possibly low-dispersal species in general, appear to be unified to a large extent by historical, non-equilibrium processes of extinction and colonization, rather than by contemporary patterns of gene flow.
- Fucus cottonii (Fucales, Phaeophyceae) is not a single genetic entity but a convergent salt-marsh morphotype with multiple independent originsPublication . Neiva, J.; Hansen, G. I.; Pearson, G. A.; Van De Vliet, M. S.; Maggs, C. A.; Serrão, EsterIn low-energy salt-marsh environments, Fucus spp. frequently exhibit an atypical morphology that is characterized by the absence of an anchoring holdfast and a trend towards reduced size and buoyancy, enhanced vegetative proliferation, and often the loss of sexual reproduction. Such forms, often referred to as ecads, presumably derive from typical attached forms, but their affinities are normally difficult to establish with confidence due to their simplified and largely convergent morphology. Minute salt-marsh forms growing partially embedded in the sediment occur on Atlantic and Pacific coasts and have traditionally been recognized as an independent entity, Fucus cottonii. In this study we analyse with four microsatellite loci two F. cottonii populations from salt-marshes of Oregon (NE Pacific) and Ireland (Europe, near the species type locality), as well as local populations of other Fucus spp. that could be considered potential source populations, either directly or via hybridization. Our results show that the F. cottonii from Oregon derive from F. gardneri whereas the Irish population is closer to F. spiralis. We conclude that F. cottonii is not a coherent genetic entity, but an artificial grouping of evolutionarily independent populations that converged into similar morphologies in different salt-marsh habitats.