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).
Glacial vicariance is regarded as one of the most prevalent drivers of phylogeographic structure and speciation among high-latitude organisms, but direct links between ice advances and range fragmentation have been more difficult to establish in marine than in terrestrial systems. Here we investigate the evolution of largely disjunct (and potentially reproductively isolated) phylogeographic lineages within the amphi-boreal kelp Saccharina latissima s. l. Using molecular data (COI, microsatellites) we confirm that S. latissima comprises also the NE Pacific S. cichorioides complex and is composed of divergent lineages with limited range overlap and genetic admixture. Only a few genetic hybrids were detected throughout a Canadian Arctic/NW Greenland contact zone. The degree of genetic differentiation and sympatric isolation of phylogroups suggest that S. latissima s. l. represents a complex of incipient species. Phylogroup distributions compared with paleo-environmental reconstructions of the cryosphere further suggest that diversification within S. latissima results from chronic glacial isolation in disjunct persistence areas intercalated with ephemeral interglacial poleward expansions and admixture at high-latitude (Arctic) contact zones. This study thus supports a role for glaciations not just in redistributing pre-existing marine lineages but also as a speciation pump across multi-glacial cycles for marine organisms otherwise exhibiting cosmopolite amphi-boreal distributions.
The brown algae (Phaeophyceae) are a group of multicellular heterokonts that are ubiquitous in today's oceans. Large brown algae from multiple orders are the foundation to temperate coastal ecosystems globally, a role that extends into arctic and tropical regions, providing services indirectly through increased coastal productivity and habitat provisioning, and directly as a source of food and commercially important extracts. Recent multi-locus and genome-scale analyses have revolutionized our understanding of the brown algal phylogeny, providing a robust framework to test evolutionary hypotheses and interpret genomic variation across diverse brown algal lineages. Here, we review recent developments in our understanding of brown algal evolution based on modern advances in phylogenetics and functional genomics. We begin by summarizing modern phylogenetic hypotheses, illuminating the timescales over which the various brown algal orders diversified. We then discuss key insights on our understanding of brown algal life cycle variation and sexual reproduction systems derived from modern genomic techniques. We also review brown algal speciation mechanisms and the associated biogeographic patterns that have emerged globally. We conclude our review by discussing promising avenues for future research opened by genomic datasets, directions that are expected to reveal critical insights into brown algal evolution in past, present, and future oceans.
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.
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. ResultsThe 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.
Aim 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 meta‐population (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.
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.
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.
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