A rapid and extensive range contraction of the southern border of a marine intertidal species occurred, with a northward shift of the historical limit of about 11° latitude. This remarkable distributional shift consists of a latitudinal reduction of about 23% of the entire species range along eastern Atlantic shores and has resulted in the erosion of a cryptic evolutionary lineage at this trailing edge. Additionally, the range contraction is consistent with significant increases in SST throughout most of the coastal area studied.
Range shift in southern Iberia
Systematic shifts in geographical ranges of species and increased extinction risk has emerged as one of the most pervasive biological responses to recent anthropogenic climate warming. The general trend shows range expansion towards higher latitudes; however, redistribution dynamics at southern range margins are less clear (for example, ). While on land, southern or 'trailing' range boundaries of terrestrial ectotherms may not shift consistently towards the poles with climate warming, marine species ranges match more closely their limits of thermal tolerance. Thus, range shifts will show a more predictable southern range contraction in the marine realm .
Extinction of southern edge populations along the Iberian Peninsula has been reported for other marine cold temperate species . Another study conducted along this stretch of coast highlights the complexity in making generalizations about range shifts for intertidal species . The extensive historical records reviewed in our study indicate that until the late 1980s abundant populations of F. vesiculosus were still present along the entire Moroccan and Iberian Atlantic coasts, while in the early 2000s extensive populations of this alga still persisted in southern Portugal. When these records are compared with our more recent surveys (2009 to 2011), a major contraction of the southern range margin of this keystone intertidal species (that is, from southern Morocco to central Portugal, latitudinal reduction of more than 1,200 km) is revealed. Taken together with past studies, there is a strong indication that the northward distributional shift along the Portuguese coast occurred very recently, probably within the last decade. This range contraction is an order of magnitude larger than the range shifts recorded for other species over the last 50 years along the Northeast Atlantic (for example, [31, 37]).
Trends in SST indicated that the large scale disappearance of southern populations of F. vesiculosus is correlated with warming of North African and southwest Iberian coastal waters, with steady year-round increases averaging >0.2°C/decade over the last three decades. Seasonal thermal extremes might also play a crucial role in defining the distribution of species through sudden population declines or die-offs . However, the key pressure exerted by increasing average SST may result from sub-lethal rather than catastrophic effects. In the North-Eastern Atlantic, the distributional limits of most warm and cold-water algal species seem to be set by sub-lethal effects of water temperature, through reduced reproduction and growth, rather than by lethal effects [34, 40]. Several other factors indirectly related or unrelated to changes in temperature may be responsible for the observed distributional shifts. These include biotic interactions (for example, grazing and competition ) and near-shore abiotic or anthropogenic effects (for example, pollution, coastal erosion, wave [38, 42]). Moreover, seaweed survival, growth, and reproduction are known to be largely affected by latitudinal variations in nutrient supply [43, 44]. However, mean or maximum water temperatures appear to be the best overall predictors of mortality events in the intertidal zone and the main determinants of large scale range contractions (for example, [36, 45–47]) as opposed to maximum air temperatures. Intertidal organisms are essentially at the same temperature as water during high tide, while thermal conditions experienced during low tide are more likely to be affected by individual physiological [48, 49] and behavioral  capacities and by the heterogeneity of intertidal microhabitats [51, 52].
The abundance of species is generally expected to peak at the center of their distributional range and decline with adverse conditions towards the range limits (for example, ). However, several empirical studies have challenged the 'abundant center' view of species distribution , such as in the intertidal zone where localized variations in the thermal environment due to climatic and tidal interactions disrupt monotonic latitudinal temperature clines [54–56]. In particular, delivery of cold waters by upwelling is not directly correlated with atmospheric processes, providing an opportunity for regional de-coupling of global warming and the creation of refugial areas where intertidal communities can escape the effects of projected climatic changes [57, 58]. Strong upwelling events off the northwest Iberian coastline reinforce latitudinal temperature gradients , while local upwelling further south (for example, the Cape Ghir region in Morocco, 31°N) disrupts latitudinal thermal clines. The latter constitutes one of the most persistent (year-round) upwelling cells along the northwest African coast . The SST data clearly indicate that the upwelling region around Cape Ghir has not experienced significant warming, in contrast to adjacent non-upwelling areas (but see below). As a result, and in contrast to the Portuguese coastline, this upwelling cell disrupts the regional thermal latitudinal cline. Despite suggestions that upwelling could provide refugia from the thermal stress of ocean warming [57, 58], our results show that F. vesiculosus populations affected by cold upwelled waters have also undergone extinction. In Cape Ghir, warming rates show variation at monthly timescales, with a significant SST increase of about 0.28°C/decade in March (http://coastalwarming.com) and maximum SST peaking occasionally over 24°C . Although monthly SST anomalies and high temperature events are less frequent and intense than in contiguous non-upwelling areas, they might be strong enough to cause extinction. Furthermore, effects of climate variability can be aggravated if isolation limits gene flow between populations, increasing genetic loss to drift with consequent loss of evolvability to cope with future environmental change . While northern populations are well connected by continuous patches of F. vesiculosus, populations at the southern edge were fragmented and spatially isolated prior to extinction, potentially limiting population size and increasing susceptibility to drastic demographic and genetic variation.
Interestingly, patches of F. vesiculosus persist within the Bay of Cadiz, along the retreating front. This represents a restricted (extending less than 1 km along the coast) population confined to very sheltered areas within the bay (personal observation). The forecasted warming trend suggests that this small and isolated relict population faces a high risk of extinction, and this prediction is further supported by the extinction of nearby (less than 10 km distant) populations (for example, La Caleta and Playa de la Victoria).
Range shifts in northern Iberia
Along eastern Atlantic shores, F. vesiculosus extends its northern distributional limit in Norway, also inhabiting the northernmost and brackish regions of the Baltic Sea and in the White Sea into brackish tidal marshlands. Within the range of F. vesiculosus, there is a well-documented gap along the SW French coast (French Basque Country and Gascony) due to lack of rocky substratum . In contrast to the southern clade, our results indicate that the present distributional range of the northern lineage in Iberia has been affected minimally, with a contraction of approximately 70 km at the southern limit of this gap (Spanish Basque Country). Notably, F. vesiculosus individuals from other regions in Europe are genetically closer to the northern Iberian clade identified in our study by the same markers . A graphical model based on IPCC (Intergovernmental Panel on Climate Change; ) scenarios predicted the range decline observed in our study . This model extends its forecast until 2050 predicting that, by 2025, cold water species, including F. vesiculosus, will disappear completely from the Bay of Biscay.
In Northern Spain, recent distributional declines have also been reported for Fucus serratus , Himanthalia elongata  and three kelp species , most probably caused by significant increases in SST  and unusually intense warm inflow of seawater during autumn-winter in 2006 . Interestingly, despite these warming trends, present SST at the eastern limit of F. vesiculosus in Northern Spain is lower than that at the southern limit in Portugal. This suggests that the two genetic lineages have different thermal tolerances or that distinct factors are setting their distribution limit. Indeed, different genetic lineages or populations inhabiting different areas within a species' distributional range can show diverse resistance or resilience to abiotic stresses (for example, [49, 71]). For example, along Atlantic European shores, southern edge populations of F. serratus are less resilient to desiccation and heat shock than central populations . Future experimental approaches could allow explicit tests for signs of local adaptation between southern and northern lineages of F. vesiculosus.
Genetic diversity under threat
Reduction in genetic variation gives independent evidence of the severity of population and habitat contraction. Estimating losses in genetic diversity associated with habitat contraction and environmental change is one of the key challenges in biodiversity research. The intensity of genetic loss largely depends on the geographical distribution of genetic diversity within the species, including cryptic diversification. Our analyses revealed two clusters, coinciding with more northern and southern locations, distinguished by several analyses based on allele frequencies, and containing unique alleles within each group, in the five microsatellite loci here used. The differentiation between northern and southern lineages in F. vesiculosus was clearly established using a large number of distinct genetic markers including 13 protein coding genes  and 35 SNP markers . The separation between these lineages of F. vesiculosus is older than the divergence between other more recently evolved species within the genus Fucus , highlighting their conservation value. The same multigene assays [70, 71] could not be performed on the old DNA left from the extinct populations here studied, thus our genetic analyses of the extinct populations are only based on five microsatellites, yet these were sufficient to reveal unique alleles.
The divergence between northern and southern lineages does not appear to be absolute, since a few individuals appear to occur in mixed populations (STRUCTURE analysis; for example, RE, OV, RM). Additionally, individuals from RE, not only diverge from southern populations, but emerge as the most distinct within the northern clade (CA analysis) with no apparent geographical explanation. This appears geographically unexpected, but patterns of genetic structure and differentiation are not necessarily maintained by prominent ecological/oceanographic barriers to dispersal . For example, in Fucus ceranoides, distant (but relatively similar) populations do not necessarily exchange more migrants than closer (but relatively distinct) populations ; historical patterns of extinction and colonization may play a more important role than ongoing gene flow in determining the extent of genetic divergence between extant populations.
Presently, the distributional range of the southern clade is restricted within approximately two degrees of latitude (17% of the historical range) and southern intra-specific genetic diversity is represented by few extant populations under threat from climatic warming. Given that predictions of future climate indicate a further rise in SST , there is a real risk of extinction of the southern phylogeographic distinctiveness owing to climatic shifts. In contrast, for long-term conservation purposes, it is reasonable to assume that, despite the relatively small range decline, the diversity of the northern clade is not under immediate risk of reduction because populations of this same genetic group are still present throughout Northern Europe.
Past and present distributional ranges of the southern lineage are characterized by markedly higher SST than those of the northern lineage; it can be hypothesized that the existence of this lineage is explained by local adaptation or phenotypic plasticity to withstand warmer waters. Our multi-locus genetic data represent neutral genetic change and do not necessarily reflect evolutionary responses to selection. However, divergent lineages often arise in areas of speciation (for example, [76, 77]). Indeed, recent data indicate that the hermaphroditic species F. virsoides, F. spiralis and the recently-described F. guiryi  are derived from a dioecious ancestor sister to the southern clade of F. vesiculosus . The potential loss of the cryptic southern F. vesiculosus lineage could end ongoing diversification (or speciation) processes and compromise the adaptive potential of the species as a whole in the face of future global warming.
In this study, genetic diversity of F. vesiculosus, as expressed by both gene diversity and allelic richness, was higher in northern Iberian populations than in the southern lineage. Higher genetic diversity in the northern Iberian region can be a signature of higher temporal stability of large populations while the opposite, in the southern region, could be the result of lower population sizes and/or temporal variability (that is, bottlenecks, extinctions/recolonizations) of the trailing edge populations. Higher diversity could also result from secondary contact between distinct lineages and/or from hybridization and introgression. While F. vesiculosus co-occurs with other fucoids throughout the majority of its range, including Northern Iberia, Southern Iberian individuals occur in allopatry. Therefore, hybridization events are likely only within and to the north of the contact zone between the sympatric and allopatric ranges . Given the apparently small population sizes (small patches) of the populations of the southern group, which are, thus, prone to drift and bottlenecks, and their geographical isolation (separated by tens to hundreds of km), it is perhaps surprising that genetic diversity, although lower, still remains so close to northern levels. Regardless of the cause behind the current within-clade diversity, their genetic distinctiveness implies that the total diversity of F. vesiculosus would be significantly reduced should these last remaining populations also become extinct.