North Atlantic marine communities through time

How and why ecological communities change their species membership over time and space is a central issue in ecology and evolution. Phylogeographic approaches based on animal mitochondrial DNA sequences have been important for revealing historical patterns of individual species and can provide qualitative comparisons among species. Exciting new methods, particularly implementing approximate Bayesian computation (ABC – Beaumont et al. 2002 ), now allow model‐based quantitative comparisons among species and permit the probabilistic exploration of alternative community‐level hypotheses (see review by Hickerson et al. 2010 ). In this issue of Molecular Ecology, Ilves et al. (2010) use an ABC approach to bring fresh insights into the well‐studied question of how North Atlantic coastal species contracted and expanded their ranges in response to late Pleistocene/Holocene climate fluctuations.     

Contrasting quaternary histories in an ecologically divergent sister pair of low-dispersing intertidal fish (Xiphister) revealed by multilocus DNA analysis

Recurrent glacial advances have shaped community histories across the planet. While biogeographic responses to glaciations likely varied with latitude, the consequences for temperate marine communities histories are less clear. By coalescent analyses of multiloci DNA sequence data (mitochondrial DNA control region, alpha-enolase intron, and alpha-tropomyosin intron) collected from a low-dispersing sister pair of rocky intertidal fishes commonly found from southeastern Alaska to California (Xiphister atropurpureus and X. mucosus), we uncover two very different responses to historical glaciations. A variety of methods that include a simulation analysis, coestimates of migration and divergence times, and estimates of minimum ages of populations sampled up and down the North American Pacific coast all strongly revealed a history of range persistence in X. atropurpureus and extreme range contraction and expansion from a southern refugium in X. mucosus. Furthermore, these conclusions are not sensitive to the independent estimates of the DNA substitution rates we obtain. While gene flow and dispersal are low in both species, the widely different histories are rather likely to have arisen from ecological differences such as diet breadth, generation time, and habitat specificity.     

Late glacial history of the cold-adapted freshwater fish Cottus gobio,revealed by microsatellites

The distribution of genetic diversity at 10 highly polymorphic microsatellite loci within the European freshwater fish, Cottus gobio, L. was examined. The sampling range comprised a large geographical scale including lineages known to be highly divergent at both mitochondrial DNA (mtDNA) and allozymes. An analysis of genetic variability within populations showed that expected heterozygosity and allelic richness could be explained largely by current effective population sizes. Evidence was found, however, that historical processes predating the last major glaciation affected allelic richness. In addition to confirming the large-scale patterns from earlier studies, the microsatellite data revealed new insights into recent processes by analysing genetic structure within ancient lineages defined by mtDNA data. Stepwise mutation model (SMM) and nonSMM-based methods demonstrated a clear genetic structuring within the Northwestern European lineage comprising populations from Britain and Belgium, and within the Central European lineage populations from the rivers Danube, Elbe and Main. Supported by an analysis of genetic variability within populations these results showed that the bullhead populations most probably persisted throughout the last major glaciation within the British Isles and within the drainages of the rivers Elbe and Main. Such observations provide the first genetic evidence for a glacial refugium in such close proximity to the European glacial margins.     

Phylogeography and historical ecology of the North Atlantic intertidal

Abstract Recent glaciation covered the full extent of rocky intertidal habitat along the coasts of New England and the Canadian Maritimes. To test whether this glaciation in fact caused wholesale extinction of obligate rocky intertidal invertebrates, and thus required a recolonization from Europe, we compared American and European populations using allelic diversity and techniques adapted from coalescent theory. Mitochondrial DNA sequences were collected from amphi-Atlantic populations of three cold-temperate obligate rocky intertidal species (a barnacle, Semibalanus balanoides , and two gastropods, Nucella lapillus and Littorina obtusata ) and three cold-temperate habitat generalist species (a seastar, Asterias rubens ; a mussel, Mytilus edulis , and an isopod, Idotea balthica ). For many of these species we were able to estimate the lineage-specific mutation rate based on trans-Arctic divergences between Pacific and Atlantic taxa. These data indicate that some obligate rocky intertidal taxa have colonized New England from European populations. However, the patterns of persistence in North America indicate that other life-history traits, including mechanisms of dispersal, may be more important for surviving dramatic environmental and climatic change.     

Trans‐Pacific and trans‐Arctic pathways of the intertidal macroalga Fucus distichus L. reveal multiple glacial refugia and colonizations from the North Pacific to the North Atlantic

Aim We examined the phylogeography of the cold‐temperate macroalgal species Fucus distichus L., a key foundation species in rocky intertidal shores and the only Fucus species to occur naturally in both the North Pacific and the North Atlantic. Location North Pacific and North Atlantic oceans (42° to 77° N). Methods We genotyped individuals from 23 populations for a mitochondrial DNA (mtDNA) intergenic spacer (IGS) (n = 608) and the cytochrome c oxidase subunit I (COI) region (n = 276), as well as for six nuclear microsatellite loci (n = 592). Phylogeographic structure and connectivity were assessed using population genetic and phylogenetic network analyses. Results IGS mtDNA haplotype diversity was highest in the North Pacific, and divergence between Pacific haplotypes was much older than that of the single cluster of Atlantic haplotypes. Two ancestral Pacific IGS/COI clusters led to a widespread Atlantic cluster. High mtDNA and microsatellite diversities were observed in Prince William Sound, Alaska, 11 years after severe disturbance by the 1989 Exxon Valdez oil spill. Main conclusions At least two colonizations occurred from the older North Pacific populations to the North Atlantic between the opening of the Bering Strait and the onset of the Last Glacial Maximum. One colonization event was from the Japanese Archipelago/eastern Aleutians, and a second was from the Alaskan mainland around the Gulf of Alaska. Japanese populations probably arose from a single recolonization event from the eastern Aleutian Islands before the North Pacific–North Atlantic colonization. In the North Atlantic, the Last Glacial Maximum forced the species into at least two known glacial refugia: the Nova Scotia/Newfoundland (Canada) region and Andøya (northern Norway). The presence of two private haplotypes in the central Atlantic suggests the possibility of colonization from other refugia that are now too warm to support F. distichus. With the continuing decline in Arctic ice cover as a result of global climate change, renewed contact between North Pacific and North Atlantic populations of Fucus species is expected.     

Northern refugia and recent expansion in the North Sea: the case of the wrasse Symphodus melops (Linnaeus, 1758)

Pleistocene climate changes have imposed extreme conditions to intertidal rocky marine communities, forcing many species to significant range shifts in their geographical distributions. Phylogeographic analyses based on both mitochondrial and nuclear genetic markers provide a useful approach to unravel phylogeographic patterns and processes of species after this time period, to gain general knowledge of how climatic changes affect shifts in species distributions. We analyzed these patterns on the corkwing wrasse (Symphodus melops, Labridae), a rocky shore species inhabiting North Sea waters and temperate northeastern Atlantic Ocean from Norway to Morocco including the Azores, using a fragment of the mitochondrial control region and the first intron of the nuclear S7 ribosomal protein gene. We found that S. melops shows a clear differentiation between the Atlantic and the Scandinavian populations and a sharp contrast in the genetic diversity, high in the south and low in the north. Within each of these main geographic areas there is little or no genetic differentiation. The species may have persisted throughout the last glacial maximum in the southern areas as paleotemperatures were not lower than they are today in North Scandinavia. The North Sea recolonization most likely took place during the current interglacial and is dominated by a haplotype absent from the south of the study area, but present in Plymouth and Belfast. The possibility of a glacial refugium in or near the English Channel is discussed.     

Multilocus tests of Pleistocene refugia and ancient divergence in a pair of Atlantic Forest antbirds (Myrmeciza)

The Atlantic Forest (AF) harbours one of the most diverse vertebrate faunas of the world, including 199 endemic species of birds. Understanding the evolutionary processes behind such diversity has become the focus of many recent, primarily single locus, phylogeographic studies. These studies suggest that isolation in forest refugia may have been a major mechanism promoting diversification, although there is also support for a role of riverine and geotectonic barriers, two sets of hypotheses that can best be tested with multilocus data. Here we combined multilocus data (one mtDNA marker and eight anonymous nuclear loci) from two species of parapatric antbirds, Myrmeciza loricata and M. squamosa, and Approximate Bayesian Computation to determine whether isolation in refugia explains current patterns of genetic variation and their status as independent evolutionary units. Patterns of population structure, differences in intraspecific levels of divergence and coalescent estimates of historical demography fit the predictions of a recently proposed model of refuge isolation in which climatic stability in the northern AF sustains higher diversity and demographic stability than in the southern AF. However, a pre‐Pleistocene divergence associated with their abutting range limits in a region of past tectonic activity also suggests a role for rivers or geotectonic barriers. Little or no gene flow between these species suggests the development of reproductive barriers or competitive exclusion. Our results suggests that limited marker sampling in recent AF studies may compromise estimates of divergence times and historical demography, and we discuss the effects of such sampling on this and other studies.     

Diversity and trans-arctic invasion history of mitochondrial lineages in the North Atlantic Macoma balthica complex (Bivalvia: Tellinidae)

The history of repeated inter- or transoceanic invasions in bivalve mollusks of the circumpolar Macoma balthica complex was assessed from mtDNA COIII sequences. The data suggest that four independent trans-Arctic invasions, from the Pacific, gave rise to the current lineage diversity in the North Atlantic. Unlike in many other prominent North Atlantic littoral taxa, no evidence for (postinvasion) trans-Atlantic connections was found in the M. balthica complex. The earliest branch of the mtDNA tree is represented by the temperate-boreal North American populations (=Macoma petalum), separated from the M. balthica complex proper in the Early Pliocene at latest. The ensuing trans-Arctic invasions established the North European M. b. rubra, which now prevails on the North Sea and northeast Atlantic coasts, about two million years ago, and the currently northwest Atlantic M. balthica lineage in the Canadian Maritimes, in the Middle Pleistocene. The final reinvasion(s) introduced a lineage that now prevails in a number of North European marginal seas and is still hardly distinguishable from North Pacific mtDNA (M. b. balthica). We used coalescence simulation analyses to assess the age of the latest invasion from the Pacific to the northeast Atlantic. The results refute the hypothesis of recent, human-mediated reintroductions between northeast Pacific and the North European marginal seas in historical times. Yet they also poorly fit the alternative hypotheses of an early postglacial trans-Arctic invasion (< 11 thousand years ago), or an invasion during the previous Eemian interglacial (120 thousand years ago). Divergence time estimates rather fall in the Middle Weichselian before the Last Glacial Maximum, in conflict with the conventional thinking of trans-Arctic biogeographical connections; an early Holocene reinvasion may still be regarded as the most plausible scenario. Today, the most recently invaded Pacific mtDNA lineage is found admixed with the earlier established European Atlantic "rubra" lineage in the Baltic Sea and in Barents Sea populations east of the Varanger peninsula, and it is practically exclusive in the White and Pechora seas. Yet mtDNA does not always constitute an unequivocal taxonomic marker at individual level; the marginal populations represent hybrid swarms of the Atlantic and Pacific lineages in their nuclear genes.     

Paleoecological significance of laminated diatomaceous oozes during the middle-to-late Pleistocene,North Atlantic Ocean (IODP Site U1304)

We examined diatom assemblages in a series of remarkable laminated diatomaceous ooze (LDO) horizons in the marine sediments from Integrated Ocean Drilling Program (IODP) Site U1304 to reconstruct the middle-to-late Pleistocene paleoceanographic evolution of the northern North Atlantic Ocean. Four confirmed diatom biohorizons combined with calcareous nannofossil and paleomagnetic stratigraphies established the chronological framework for the material. The planktonic, araphid, needle-like species Thalassiothrix longissima was the greatest contributor to the LDO facies. From the results of a principal component analysis using the percent abundances of 65 significant (p = 5%) diatom taxa, except for Tx. longissima, which was extremely dominant in almost all horizons observed, we identified two principal component (PC) axes. Taxa probably associated with the stratigraphic distribution of the major zonal marker Neodenticula seminae (ranging from 1.26 to 0.84 Ma in this ocean) loaded on PC1 with a high value. PC2 was related to the ocean surface temperature. The stratigraphic variability of the PC2 score indicated that switching between warm- and cold-water assemblages occurred concurrently with LDO deposition (or extreme Tx. longissima dominance) episodes in several horizons (particularly after 0.84 Ma), suggesting that the Subarctic Convergence (SAC) oceanic front passed over Site U1304 during Pleistocene glacial/interglacial cycles. Our floral evidence supports the model of nearly monospecific LDO formation caused by the enhanced physical accumulation of particular diatoms such as Tx. longissima. On the other hand, Nd. seminae, which probably contributes to spring phytoplankton blooms in the modern ocean, was present only between 1.26 and 0.84 Ma in this area. Thus, we infer that the main contributor of export flux in the regional annual primary production cycle would have shifted drastically from one of a spring phytoplankton bloom leader (Nd. seminae) to minor but mass dump assemblages (Tx. longissima etc.) in the mid-Pleistocene.     

The role of the North Atlantic Drift in the millennial timescale glacial climate fluctuations

The Greenland ice core records show that the overall cold climate of the last glacial period was repeatedly interrupted by short, rapid warmings. The events, known as Dansgaard-Oeschger (D-O) events, are strongly imprinted in the North Atlantic marine records suggesting that they were linked to North Atlantic circulation changes. However, the causes of the D-O events are poorly understood and they represent one of the most intriguing puzzles of the last glacial period. In order to investigate a possible mechanism we have studied variations in the distribution of benthic and planktonic foraminifera, oxygen isotopes and ice rafted debris during the last glacial period in eight cores from the North Atlantic and the Nordic Seas taken at mid depth from 853 to 1760 m. The parameters indicate, in agreement with previous studies, that the circulation system during the interstadials resembled the present system. Atlantic surface water flowed north into the Nordic Seas, where most of it sank through convection and, as cold deep water, flowed back into the North Atlantic. During the stadials, a halocline was established in the Nordic Seas and in the northernmost part of the North Atlantic and the outflow from the Nordic Seas stopped. However, below the cold, light surface layer, the relatively warm water of the North Atlantic Drift continued to flow across the North Atlantic and into the Nordic Seas, here warming up the deep-water masses. We suggest that the warm water gradually made the water column unstable. The pivotal abrupt climate warmings were caused by sudden upwelling of the deep, warm water masses causing overturning of the entire water column and onset of convection.     

Historical climate modelling predicts patterns of current biodiversity in the Brazilian Atlantic forest

Aim We aim to propose validated, spatially explicit hypotheses for the late Quaternary distribution of the Brazilian Atlantic forest, and thereby provide a framework for integrating analyses of species and genetic diversity in the region. Location The Atlantic forest, stretching along the Brazilian coast. Methods We model the spatial range of the forest under three climatic scenarios (current climate, 6000 and 21,000 years ago) with BIOCLIM and MAXENT. Historically stable areas or refugia are identified as the set of grid cells for which forest presence is inferred in all models and time projections. To validate inferred refugia, we test whether our models are matched by the current distribution of the forest and by fossil pollen data. We then investigate whether the location of inferred forest refugia is consistent with current patterns of species endemism and existing phylogeographical data. Results Forest models agree with pollen records and predict a large area of historical forest stability in the central corridor (Bahia), as well as a smaller refuge (Pernambuco) along the Brazilian coast, matching current centres of endemism in multiple taxa and mtDNA diversity patterns in a subset of the species examined. Less historical stability is predicted in coastal areas south of the Doce river, which agrees with most phylogeographical studies in that region. Yet some widely distributed taxa show high endemism in the southern Atlantic forest. This may be due to limitations of the modelling approach, differences in ecology and dispersal capability, historical processes not contemplated by the current study or inadequacy of the available test data sets. Main conclusions Palaeoclimatic models predict the presence of historical forest refugia in the Atlantic rain forest and suggest spatial variation in persistence of forests through the Pleistocene, predicting patterns of biodiversity in several local taxa. The results point to the need for further studies to document genetic and species endemism in the relatively poorly known and highly impacted areas of Atlantic rain forests of north‐eastern Brazil.     

Chloroplast DNA supports a hypothesis of glacial refugia over postglacial recolonization in disjunct populations of black pine (Pinus nigra) in western Europe

European black pine (Pinus nigra Arn.) is a widely distributed Mediterranean conifer. To test the hypothesis that fragmented populations in western Europe survived in situ during the last glacial rather than having been re-colonized in the postglacial period, genetic variation was assessed using a suite of 10 chloroplast DNA microsatellites. Among 311 individuals analysed, 235 haplotypes were detected revealing high levels of chloroplast haplotype diversity in most populations. Bayesian analysis using a model of linked loci, with no prior assumption of population structure, assigned individuals to 10 clusters that corresponded well with the six predefined sampling regions, while an analysis carried out at the population level and assuming unlinked loci, recovered the original six sampling regions. This regional structure was supported by a biogeographical analysis that detected five barriers, with the two most significant separating Alps from Corsica and southern Italy, and southern Spain from the Pyrenees. No signals of demographic expansion were detected, and comparisons of R(ST) with pR(ST) suggested that a stepwise mutational model was important in regional differentiation, but not in population-within-region differentiation. These tests support long-term persistence of the species within the six regions. The temporal depth estimate, assuming a high mutation rate in coalescent modelling, placed the deepest split between the Alps and the other regions at about 150 000 years ago, and the most recent split of Pyrenees from southern France at about 30 000 years ago. Taken together, the data suggest that chloroplast DNA is structured in black pine and disjunct populations in western Europe are likely to have been present during the Last Glacial Maximum.     

Population genetic isolation and limited connectivity in the purple finch (Haemorhous purpureus)

Using a combination of mitochondrial and z‐linked sequences, microsatellite data, and spatio‐geographic modeling, we examined historical and contemporary factors influencing the population genetic structure of the purple finch (Haemorhous purpureus). Mitochondrial DNA data show the presence of two distinct groups corresponding to the two subspecies, H. p. purpureus and H. p. californicus. The two subspecies likely survived in separate refugia during the last glacial maximum, one on the Pacific Coast and one east of the Rocky Mountains, and now remain distinct lineages with little evidence of gene flow between them. Southwestern British Columbia is a notable exception, as subspecies mixing between central British Columbia and Vancouver Island populations suggests a possible contact zone in this region. Z‐linked data support two mitochondrial groups; however, Coastal Oregon and central British Columbia sites show evidence of mixing. Contemporary population structure based on microsatellite data identified at least six genetic clusters: three H. p. purpureus clusters, two H. p. californicus clusters, and one mixed cluster, which likely resulted from high site fidelity and isolation by distance, combined with sexual selection on morphological characters reinforcing subspecies differences.     

Post-pleistocene demographic history of the North Atlantic endemic Irish moss Chondrus crispus: glacial survival, spatial expansion and gene flow

Range expansions and gene flow as micro-evolutionary processes played a leading role in the population demographic history of marine organisms. Herein, we sequenced partial mtDNA Cox1 gene from 26 assigned geographical populations to understand how Irish moss (Chondrus crispus) responded to severe climatic oscillations during the Pleistocene glaciations and contemporary forces such as gene flow. Phylogeographic patterns indicated that haplotype frequency distributions were strongly skewed, with nearly half found only in single samples and thus restricted to a single population. Analysis of molecular variance revealed that most of the variation was within populations with no significant genetic structuring on either side of the Atlantic. Demographic analyses indicated that ISI (Irish Sea and Ireland) and NS (the North Sea) areas experienced a slight trend of increase in population size over time, whereas EC (the English Channel) area experienced expansion beginning approximately 170,000-360,000 BP. The observed complex genetic pattern of C. crispus is consistent with a scenario of multiple unrelated founding events by survival of this species in at least three putative Pleistocene refugia along the European coastline, and subsequent trans-Atlantic dispersal combined with contiguous northward population expansion predating the LGM and geographically gene flow.     

Length-weight relationships of seven fish species from tidepools of an intertidal rocky shore in the Gulf of Cadiz,Spain (NE Atlantic)

Length-weight relationships for seven fish species caught from tidepools in an intertidal rocky shore in the Gulf of Cadiz are presented. Fish were sampled monthly (April 2008–January 2012), using hand nets (mesh size 1.5 mm). The values of b parameter remained within the expected range of 2.5–3.5 for all fish species. An ANCOVA test was used to evaluate differences in the b growth parameter between females and males. Gobius cobitis, G. incognitus and G. paganellus showed significant differences in the parameters of the length-weight relationships according to the sex.     

Variation in mitochondrial DNA reveals multiple distant glacial refugia in black spruce (Picea mariana), a transcontinental North American conifer

Range-wide genetic variation of black spruce (Picea mariana) was studied using polymerase chain reaction-random fragment length polymorphism markers of the mitochondrial genome. Four polymorphic mitochondrial DNA (mtDNA) loci were surveyed and two or three alleles were detected at each locus, resulting in 10 multilocus mtDNA types or mitotypes. A significant subdivision of population genetic diversity was detected (GST = 0.671; NST = 0.726), suggesting low levels of gene flow among populations. The distribution of mitotypes was not random (NST > GST; P < 0.05) and revealed four partially overlapping zones, presumably representative of different glacial populations. Comparison of the genetic structure derived from mtDNA markers and the colonization paths previously deduced from the fossil and pollen records allow us to infer at least three southern and one northeastern glacial populations for black spruce. The patterns revealed in this study suggest that black spruce shares its biogeographical history with other forest-associated North American species.     

'SSW to NNE'– North Atlantic Oscillation affects the progress of seasons across Europe

Three European plant phenological network datasets were analysed for latitudinal and longitudinal gradients of nine phenological ‘seasons’ spanning the entire year. The networks were: (1) the historical first European Phenological Network (1882–1941) by Hoffmann & Ihne, (2) the network of the International Phenological Gardens in Europe (1959–1998), founded by Schnelle & Volkert in 1957 and based on cloned plants, and (3) a dataset (1951–1998) that was recently collated during the EU Fifth Framework project POSITIVE, which included network data of seven Central and Eastern European countries. Our study is most likely the first, for over a century, to analyse average onset and year‐to‐year variability of the progress of seasons across a continent. For early, mid, and late spring seasons we found a marked progress of the seasonal onset from SW to NE throughout Europe, more precisely from WSW to ENE in early spring, then from SW to NE and finally from SSW to NNE in late spring, as exhibited by the relationship between latitudinal and longitudinal gradients. The movement of summer was more south to north directed, as the longitudinal gradient (west–east component) strongly declined or was even of opposite sign. Autumn, as shown by leaf colouring dates, arrived from NE to SW. Possible reasons for the differences among the three datasets are discussed. The annual variability of latitudinal and longitudinal gradients of the seasons across Europe was closely related to the North Atlantic Oscillation (NAO) index; in years with high NAO in both winter and spring, the west–east component of progress was more pronounced; in summer and autumn, the pattern of the seasons may be more uniform.     

Phylogeography of ninespine sticklebacks (Pungitius pungitius) in North America: glacial refugia and the origins of adaptive traits

The current geographical distribution of the ninespine stickleback (Pungitius pungitius) was shaped in large part by the glaciation events of the Pleistocene epoch (2.6 Mya–10 Kya). Previous efforts to elucidate the phylogeographical history of the ninespine stickleback in North America have focused on a limited set of morphological traits, some of which are likely subject to widespread convergent evolution, thereby potentially obscuring relationships among populations. In this study, we used genetic information from both mitochondrial DNA (mtDNA) sequences and nuclear microsatellite markers to determine the phylogenetic relationships among ninespine stickleback populations. We found that ninespine sticklebacks in North America probably dispersed from at least three glacial refugia—the Mississippi, Bering, and Atlantic refugia—not two as previously thought. However, by applying a molecular clock to our mtDNA data, we found that these three groups diverged long before the most recent glacial period. Our new phylogeny serves as a critical framework for examining the evolution of derived traits in this species, including adaptive phenotypes that evolved multiple times in different lineages. In particular, we inferred that loss of the pelvic (hind fin) skeleton probably evolved independently in populations descended from each of the three putative North American refugia.