Identifying refugia from climate change using coupled ecological and genetic data in a transitional Mediterranean-temperate tree species (original) (raw)

Environmental Heterogeneity Explains the Genetic Structure of Continental and Mediterranean Populations of Fraxinus angustifolia Vahl

PLoS ONE, 2012

Tree species with wide distributions often exhibit different levels of genetic structuring correlated to their environment. However, understanding how environmental heterogeneity influences genetic variation is difficult because the effects of gene flow, drift and selection are confounded. We investigated the genetic variation and its ecological correlates in a windpollinated Mediterranean tree species, Fraxinus angustifolia Vahl, within a recognised glacial refugium in Croatia. We sampled 11 populations from environmentally divergent habitats within the Continental and Mediterranean biogeographical regions. We combined genetic data analyses based on nuclear microsatellite loci, multivariate statistics on environmental data and ecological niche modelling (ENM). We identified a geographic structure with a high genetic diversity and low differentiation in the Continental region, which contrasted with the significantly lower genetic diversity and higher population divergence in the Mediterranean region. The positive and significant correlation between environmental and genetic distances after controlling for geographic distance suggests an important influence of ecological divergence of the sites in shaping genetic variation. The ENM provided support for niche differentiation between the populations from the Continental and Mediterranean regions, suggesting that contemporary populations may represent two divergent ecotypes. Ecotype differentiation was also supported by multivariate environmental and genetic distance analyses. Our results suggest that despite extensive gene flow in continental areas, long-term stability of heterogeneous environments have likely promoted genetic divergence of ashes in this region and can explain the present-day genetic variation patterns of these ancient populations. Citation: Temunović M, Franjić J, Satovic Z, Grgurev M, Frascaria-Lacoste N, et al. (2012) Environmental Heterogeneity Explains the Genetic Structure of Continental and Mediterranean Populations of Fraxinus angustifolia Vahl. PLoS ONE 7(8): e42764.

Genetic resources and forestry in the Mediterranean region in relation to global change

Annals of Silvicultural Research, 2015

The purpose of this review is to examine a few aspects of global change effects on forest genetic resources and their interaction. Genetic resources can provide many opportunities for the development of adaptive forest management in the Mediterranean region. At the same time, forestry and its various disciplines can offer manifold chances to develop methods and techniques for the in situ and ex situ protection, as well as for the correct management of species and populations at risk because of climate change. Among these aspects, the studies on the Marker Assisted Selection are particularly taken into consideration, as well as the phenotypic plasticity and the different types of assisted migration. A special emphasis is given to genetic resources growing at marginal peripheral populations, which need to be safeguarded as possible containers of adaptive diversity. They are subjected, in fact, to an extreme climatic stress more than others.

Genetic patterns of habitat fragmentation and past climate-change effects in the Mediterranean high-mountain plantArmeria caespitosa(Plumbaginaceae)

American Journal of Botany, 2013

Current anthropogenic global warming constitutes one of the greatest long-term threats to biodiversity worldwide (Parmesan, 2006). Ongoing warming conditions abruptly increase the risk of plant extinction (i.e., Thuiller et al., 2005) and enhance the isolation of marginal populations (Ackerly and Monson, 2003). Biological responses to drivers of climatic change vary greatly in space and time (Loarie et al., 2009) and can include altitudinal and latitudinal shifts of populations and communities (Sturm et al., 2001 ; Peñuelas and Boada, 2003), increases in biological invasions (Walther et al., 2009), and changes in local community composition and structure (Jump and Peñuelas, 2005 ; Gottfried et al., 2012). However, little is known about microevolutionary responses, which may occur instead of, or in conjunction with, range shifts (Rodríguez-Trelles et al., 1998). Thus, genetic changes might be as important as demographic changes in determining species' responses. These microevolutionary responses can have profound implications not only in the genetic diversity and structure of species in marginal populations, but also across whole species ranges (Hughes et al., 2008 ; Kawecki, 2008) as well as in the accuracy of future predictions under current global change. Landscape genetics approaches integrate the effect of landscape connectivity into gene fl ow and genetic structure analyses and help us to better understand local adaptation processes (Holderegger et al., 2010). This is especially true for plants inhabiting discrete habitats for which new insights are required (Reusch and Wood, 2007). Thus, the study of the main population genetic parameters (such as genetic diversity, estimates of gene fl ow, or the incipient process of local adaptation and genes involved) is essential not only to characterize the degree of isolation of populations and estimate their genetic relatedness but also to assess how they are responding to global change (Kawecki,

Patterns of polymorphism resulting from long-range colonization in the Mediterranean conifer Aleppo pine

New Phytologist, 2009

•The evolutionary outcomes of range expansion/contraction depend on the biological system considered and the interactions among the evolutionary forces in place. In this study, we examined the demographic history and the local polymorphism patterns of candidate genes linked to drought tolerance of a widespread Mediterranean conifer (Pinus halepensis).•To that end, we used cpSSRs and coalescence modelling of nuclear genes to infer the demographic history of natural populations covering the species range. Ten drought-response candidate genes were then examined for their patterns of polymorphism and tested for selection considering plausible demographic scenarios.•Our results revealed a marked loss of genetic diversity from the relictual Greek population towards the western range of the species, as well as molecular signatures of intense bottlenecks. Moreover, we found an excess of derived polymorphisms in several genes sampled in the western part of the range – a potential result of the action of natural selection on populations confronted with new environments following long-range colonization.•Wide-range expansions–contractions of forest trees are accompanied by strong selective pressures, resulting in distinct evolutionary units. This knowledge is of crucial importance for the conservation and management of forests in the face of climate change.The evolutionary outcomes of range expansion/contraction depend on the biological system considered and the interactions among the evolutionary forces in place. In this study, we examined the demographic history and the local polymorphism patterns of candidate genes linked to drought tolerance of a widespread Mediterranean conifer (Pinus halepensis).To that end, we used cpSSRs and coalescence modelling of nuclear genes to infer the demographic history of natural populations covering the species range. Ten drought-response candidate genes were then examined for their patterns of polymorphism and tested for selection considering plausible demographic scenarios.Our results revealed a marked loss of genetic diversity from the relictual Greek population towards the western range of the species, as well as molecular signatures of intense bottlenecks. Moreover, we found an excess of derived polymorphisms in several genes sampled in the western part of the range – a potential result of the action of natural selection on populations confronted with new environments following long-range colonization.Wide-range expansions–contractions of forest trees are accompanied by strong selective pressures, resulting in distinct evolutionary units. This knowledge is of crucial importance for the conservation and management of forests in the face of climate change.

Simulated climate change provokes rapid genetic change in the Mediterranean shrubFumana thymifolia

Global Change Biology, 2008

Rapid climate change will impose strong directional selection pressures on natural plant populations. Climate-linked genetic variation in natural populations indicates that an evolutionary response is possible. We investigated such a response by comparing individuals subjected to elevated drought and warming treatments with individuals establishing in an unmanipulated climate within the same population. We report that reduction in seedling establishment in response to climate manipulations is nonrandom and results from the selection pressure imposed by artificially warmed and droughted conditions. When compared against control samples, high single-locus genetic divergence occurred in drought and warming treatment samples, with genetic differentiation up to 37 times higher than background (mean neutral locus) genetic differentiation. These loci violate assumptions of selective neutrality, indicating the signature of natural selection by drought. Our results demonstrate that rapid evolution in response to climate change may be widespread in natural populations, based on genetic variation already present within the population.

Evolutionary rate and genetic load in an emblematic Mediterranean tree following an ancient and prolonged population collapse

Molecular Ecology, 2020

Severe bottlenecks significantly diminish the amount of genetic diversity and the speed at which it accumulates (i.e. evolutionary rate). They further compromise the efficiency of natural selection to eliminate deleterious variants, which may reach fixation in the surviving populations. Consequently, expanding and adapting to new environments may pose a significant challenge when strong bottlenecks result in genetic pauperization. Herein, we surveyed the patterns of nucleotide diversity, molecular adaptation and genetic load across 177 gene-loci in a circum-Mediterranean conifer (Pinus pinea L.) that represents one of the most extreme cases of genetic pauperization in widespread outbreeding taxa. We found very little genetic variation in both hypervariable nuclear microsatellites (SSRs) and gene-loci, which translated into genetic diversity estimates one order of magnitude lower than those previously reported for pines. Such values were consistent with a strong population decline that began some ~1Ma. Comparisons with the related and parapatric maritime pine (Pinus pinaster Ait.) revealed reduced rates of adaptive evolution (α and ωa) and a significant accumulation of genetic load. It is unlikely that these are the result from differences in mutation rate or linkage disequilibrium between the two species; instead they are the presumable outcome of contrasting demographic histories affecting both the speed at which these taxa accumulate genetic diversity, and the global efficacy of selection. Future studies, and programs for conservation and management, should thus start testing for the effects of genetic load on fitness, and integrating such effects into predictive models.

Are woody seeder plants more prone than resprouter to population genetic differentiation in Mediterranean-type ecosystems?

Evolutionary Ecology

High diversification of woody seeder lineages is characteristic of the south-western cape floristic region (CFR), South Africa, which has been explained as a consequence of its mild Mediterranean climate and reliable winter rainfall. Such climatic regime reduces the risk of post-fire recruitment failure, acting as an ecological filter that favours seeder populations, thus promoting genetic differentiation and diversification in seeder populations, as previously seen in the South African heath Erica coccinea. To explore this hypothesis further, genetic population structure was investigated in two Mediterranean Erica species, one seeder (Erica umbellata) and the other resprouter (Erica australis), using nuclear microsatellites. These two species are endemic to the western Mediterranean Basin and co-occur in heathlands of the Strait of Gibraltar region. Mean annual rainfall in this region is similar to that from the south-western CFR, but summer stress is more marked and winter rainfal...

Glacial refugia influence plant diversity patterns in the Mediterranean Basin

Journal of Biogeography, 2009

Aim The aims of this study were to assess the distribution of putative Mediterranean refugia of plants, to compare the locations of refugia and those of regional hotspots of plant biodiversity, and to provide a critical analysis of the Mediterranean refugium paradigm. Furthermore, we consider how biogeographical and genetic results can be combined to guide global conservation strategies. Location The Mediterranean region. Methods We started from a detailed analysis of the scientific literature (1993-2007) in order to identify refugia in the Mediterranean region, based on intraspecific phylogeographical studies of plant species. We used population locations together with gene-pool identity to establish the database, comparing patterns of phylogeographical concordance with the locations of Mediterranean refugia. We then tested the biogeographical congruence between two biodiversity components, namely phylogeographical refugia and regional hotspots. Results We identified 52 refugia in the Mediterranean bioclimatic region and confirmed the role played by the three major peninsulas, with a shared total of 25 refugia. We emphasize the importance of areas that have previously been attributed a lesser role (large Mediterranean islands, North Africa, Turkey, Catalonia). Of the 52 refugia identified, 33 are situated in the western Mediterranean Basin and 19 in the eastern part. The locations of the phylogeographically defined refugia are significantly associated with the 10 regional hotspots of plant biodiversity, with 26 of these refugia (i.e. 50%) occurring within the hotspots. Main conclusions The locations of refugia are determined by complex historical and environmental factors, the cumulative effects of which need to be considered because they have occurred since the Tertiary, rather than solely during the last glacial period. Refugia represent climatically stable areas and constitute a high conservation priority as key areas for the long-term persistence of species and genetic diversity, especially given the threat posed by the extensive environmental change processes operating in the Mediterranean region. The refugia defined here represent 'phylogeographical hotspots'; that is, significant reservoirs of unique genetic diversity favourable to the evolutionary processes of Mediterranean plant species.

Rangewide phylogeography of a bird-dispersed Eurasian shrub: Contrasting Mediterranean and temperate glacial refugia

Molecular Ecology, 2003

We studied the phylogeography of alder buckthorn ( Frangula alnus ), a bird-dispersed shrub or small tree distributed over most of Europe and West Asia and present in three of the four main refugia of West Palaearctic temperate woody plants: the Iberian Peninsula, the Balkans and Anatolia. A total of 78 populations from 21 countries were analysed for chloroplast DNA variation using polymerase chain reaction-restriction fragment length polymorphism (PCR-RFLP), and 21 different haplotypes were distinguished. We found a very strong overall population differentiation ( G ST = 0.81) and phylogeographical structure, and a sharp contrast between the haplotype-rich refugia and the almost completely uniform area of postglacial colonization. The haplotype network comprises three lineages made up of haplotypes from the Iberian Peninsula, Anatolia with the Caucasus, and temperate Europe. The Iberian and the Anatolian branches represent parts of a major lineage that spans over the whole northern Mediterranean Basin and some neighbouring areas and probably dates back to the Tertiary. Many haplotypes of this lineage are distributed locally and most populations are fixed for a single haplotype; these populations have apparently been very stable since their establishment, experiencing negligible gene flow and few mutations. The temperate European lineage consists of one very widespread and abundant plus six locally distributed haplotypes. Four of them are located in Southeast Europe, the putative refugium of all extant temperate European populations. Contrary to populations from Iberia and Anatolia, F. alnus populations from the southeastern European refugium have most genetic variation within populations. Bird-mediated seed dispersal has apparently allowed not only a very rapid postglacial expansion of F. alnus but also subsequent regular seed exchanges between populations of the largely continuous species range in temperate Europe. In contrast, the disjunct F. alnus populations persisting in Mediterranean mountain ranges seem to have experienced little gene flow and have therefore accumulated a high degree of differentiation, even at short distances. Populations from the southern parts of the glacial refugia have contributed little to the postglacial recolonization of Europe, but their longterm historical continuity has allowed them to maintain a unique store of genetic variation.

Vulnerability of dynamic genetic conservation units of forest trees in Europe to climate change

Global Change Biology, 2014

A transnational network of genetic conservation units for forest trees was recently documented in Europe aiming at the conservation of evolutionary processes and the adaptive potential of natural or man-made tree populations. In this study, we quantified the vulnerability of individual conservation units and the whole network to climate change using climate favourability models and the estimated velocity of climate change. Compared to the overall climate niche of the analysed target species populations at the warm and dry end of the species niche are underrepresented in the network. However, by 2100, target species in 33-65 % of conservation units, mostly located in southern Europe, will be at the limit or outside the species' current climatic niche as demonstrated by favourabilities below required model sensitivities of 95%. The highest average decrease in favourabilities throughout the network can be expected for coniferous trees although they are mainly occurring within units in mountainous landscapes for which we estimated lower velocities of change. Generally, the species-specific estimates of favourabilities showed only low correlations to the velocity of climate change in individual units, indicating that both vulnerability measures should be considered for climate risk analysis. The variation in favourabilities among target species within the same conservation units is expected to increase with climate change and will likely require a prioritization among co-occurring species. The present results suggest that there is a strong need to intensify monitoring efforts and to develop additional conservation measures for populations in the most vulnerable units. Also, our results call for continued transnational actions for genetic conservation of European forest trees, including the establishment of dynamic conservation populations outside the current species distribution ranges within European assisted migration schemes.