João Neiva

Shift happens: trailing edge contraction associated with recent warming trends threatens a distinct genetic lineage in the marine macroalga Fucus vesiculosus

BackgroundSignificant 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.ResultsOver 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.ConclusionsWe 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).

Surfing the wave on a borrowed board: range expansion and spread of introgressed organellar genomes in the seaweed Fucus ceranoides L.

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.

Fine-scale genetic breaks driven by historical range dynamics and ongoing density-barrier effects in the estuarine seaweed Fucus ceranoides L.

BackgroundFactors 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.ResultsVariation 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.ConclusionsThe 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.

Feeding habits of the velvet belly lanternshark Etmopterus spinax (Chondrichthyes: Etmopteridae) off the Algarve, southern Portugal

Etmopterus spinax is one of the most abundant predators of the upper continental slope off the Algarve (southern Portugal), where it is captured in large quantities in deep-water fisheries. The feeding habits of E. spinax off the Algarve were investigated through the analysis of stomach contents of 376 individuals. Prey composition was described and maturity, sex and size related variations in the diet analysed. The overall diet of E. spinax suggested a fairly generalized benthopelagic foraging behaviour primarily tuned to pelagic macroplankton/microneckton, teleost fish and cephalopods. Sex and maturity related differences in the diet were not significant. Two main ontogenic diet shifts were observed at about 17 and 28 cm total length. Small and medium sized immature sharks had a diet dominated by eurybathic crustaceans, chiefly Meganyctiphanes norvegica and Pasiphaea sivado . Larger individuals consumed more teleosts and cephalopods, in part associated with scavenging as a new feeding strategy. With increasing shark size the diet diversified both in terms of resources exploited and prey size.

Genes Left Behind: Climate Change Threatens Cryptic Genetic Diversity in the Canopy-Forming Seaweed Bifurcaria bifurcata

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.

Climate Oscillations, Range Shifts and Phylogeographic Patterns of North Atlantic Fucaceae

Members of the seaweed family Fucaceae have been recurrent models in North Atlantic phylogeographic research; numerous studies have been published since 2000, and this review synthesizes their major findings. Fucoid species exhibited diverse responses to glacial–interglacial cycles, but evidence indicates there were a few common refugial areas such as north-western Iberia, the Celtic Sea (Brittany/Ireland) region and the North-west Atlantic. In genetically rich refugial areas, pervasive genetic breaks confirmed presently limited gene flow between adjacent distinct genetic groups. In contrast with the maintenance of sharp genetic breaks, most species experienced extensive migration during post-glacial expansion. Poleward migrations in the North-east Atlantic followed routes along north-western Ireland and the transgressing English Channel. These patterns support the role of density-blocking in maintaining sharp genetic breaks at contact zones, and of long-distance dispersal from range edges in mediating expansion into uninhabited regions. The data also indicate that expansions involve mostly the genetic groups located at range edges rather than the entire species’ gene pool, both poleward during interglacials and toward warmer regions during glacial periods. Fucoid expansions have also been linked to introgressive recombination of genomes at (and beyond) contact zones and to gene surfing leading to present large-scale dominance by alleles that were located at the expanding edge. Phylogeographic approaches have also proven useful to identify and track the sources of introductions linked to marine traffic. The integration of environmental niche models with molecular data have further allowed hindcasting southern distributions during glaciation and predicting the potentially negative effects of future climate warming, including the loss of vulnerable, unique trailing-edge lineages, as species’ ranges are predicted to continue shifting northward. Collectively, these studies have contributed greatly to elucidating the links between past and ongoing climatic shifts, range dynamics and geographical patterns of genetic variability in the North Atlantic.

Characterization of 12 polymorphic microsatellite markers in the sugar kelp Saccharina latissima

Saccharina 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 < HE < 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.

Genetic diversity of Saccharina latissima (Phaeophyceae) along a salinity gradient in the North Sea–Baltic Sea transition zone

The North Sea–Baltic Sea transition zone constitutes a boundary area for the kelp species Saccharina latissima due to a strong salinity gradient operating in the area. Furthermore, the existence of S. latissima there, along Danish waters, is fairly patchy as hard bottom is scarce. In this study, patterns of genetic diversity of S. latissima populations were evaluated along the salinity gradient area of Danish waters (here designated brackish) and were compared to reference sites (here designated marine) outside the gradient area, using microsatellite markers. The results showed that the S. latissima populations were structured into two clusters corresponding to brackish versus marine sites, and that gene flow was reduced both between clusters and between populations within clusters. In addition, results provided empirical evidence that marginal populations of S. latissima in the salinity gradient area exhibited a distinct genetic structure when compared to marine ones. Brackish populations were less diverse, more related, and showed increased differentiation over distance compared to marine populations. The isolation of the brackish S. latissima populations within the salinity gradient area of Danish waters in conjunction with their general low genetic diversity makes these populations vulnerable to ongoing environmental and climate change, predicted to result in declining salinity in the Baltic Sea area that may alter the future distribution and performance of S. latissima in the area.

Fucus cottonii (Fucales, Phaeophyceae) is not a single genetic entity but a convergent salt-marsh morphotype with multiple independent origins

In 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.

Cryptic diversity, geographical endemism and allopolyploidy in NE Pacific seaweeds

BackgroundMolecular 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.ResultsThe 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.ConclusionsThis 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.