Ricardo Alía

Potential for evolutionary responses to climate change – evidence from tree populations

Evolutionary responses are required for tree populations to be able to track climate change. Results of 250 years of common garden experiments show that most forest trees have evolved local adaptation, as evidenced by the adaptive differentiation of populations in quantitative traits, reflecting environmental conditions of population origins. On the basis of the patterns of quantitative variation for 19 adaptation-related traits studied in 59 tree species (mostly temperate and boreal species from the Northern hemisphere), we found that genetic differentiation between populations and clinal variation along environmental gradients were very common (respectively, 90% and 78% of cases). Thus, responding to climate change will likely require that the quantitative traits of populations again match their environments. We examine what kind of information is needed for evaluating the potential to respond, and what information is already available. We review the genetic models related to selection responses, and what is known currently about the genetic basis of the traits. We address special problems to be found at the range margins, and highlight the need for more modeling to understand specific issues at southern and northern margins. We need new common garden experiments for less known species. For extensively studied species, new experiments are needed outside the current ranges. Improving genomic information will allow better prediction of responses. Competitive and other interactions within species and interactions between species deserve more consideration. Despite the long generation times, the strong background in quantitative genetics and growing genomic resources make forest trees useful species for climate change research. The greatest adaptive response is expected when populations are large, have high genetic variability, selection is strong, and there is ecological opportunity for establishment of better adapted genotypes.

Genetic variation and migration pathways of maritime pine (Pinus pinaster Ait) in the Iberian peninsula

Abstract The genetic variability and migration pathways of Pinus pinaster after glaciation in the Iberian peninsula was studied by means of 18 loci from 12 natural populations of the species. The analysis showed the existence of three groups of populations with different levels of diversity and patterns of recolonization. The southern Iberian group displays a high level of diversity, with a stepping-stone model of variation. The presence of rare alleles in this group and their position in the phylogenetic tree suggest the existence of refugia during glaciations in this zone. The eastern Iberian group also has high levels of diversity but is clearly separate from the first group based on their genetic distances. The Atlantic group displays a low level of diversity that could be interpreted as a rapid recolonization of the entire area by the Eastern group that has not yet developed to a divergence in this area. The southern Iberian range is indicated to be the dispersal centre of the species after the last glaciation.

Increased selfing and correlated paternity in a small population of a predominantly outcrossing conifer, Pinus sylvestris

Outcrossing rate, the rates of ovule and seed abortion, and levels of correlated paternity were estimated in a small population of Pinus sylvestris, a predominantly outcrossing conifer, and were compared with estimates from two widely dispersed woodlands of the same species, showing a range of densities. On average, seed trees of the small population showed an eight‐fold higher selfing rate (25 vs. 3%) and a 100‐fold greater incidence of correlated paternity (19.6 vs. 0.2%) than did trees from the large populations. No evidence was found of pollen limitation within the remnant stand, as suggested by ovule abortion rates. Investigation of the mating patterns in the small population, based on the unambiguous genealogy of 778 open‐pollinated seeds, showed a large departure from random mating. Only 8% of the possible mating pairs within the stand were observed. Correlated paternity rate within a maternal sibship was negatively associated (rs = −0.398, P < 0.050) with the distance to the nearest neighbour, and shared paternity among maternal sibships was negatively correlated (rs = −0.704, P < 0.001) with the distance between seed trees. Numerical simulations, based on the estimated individual pollen dispersal kernel, suggest that restricted dispersal might have been the key factor affecting mating patterns in the small population and, together with low population density, may account for the observed mating system variation between the small and the large populations. The results of this study show that a severe size reduction may substantially affect the mating system of a wind‐pollinated, typically outcrossed plant species.

Molecular footprints of local adaptation in two Mediterranean conifers

This study combines neutrality tests and environmental correlations to identify nonneutral patterns of evolution in candidate genes related to drought stress in two closely related Mediterranean conifers, Pinus pinaster Ait. and P. halepensis Mill. Based on previous studies, we selected twelve amplicons covering six candidate genes that were sequenced in a large sample spanning the full range of these two species. Neutrality tests relatively robust to demography (DHEW compound test and maximum likelihood multilocus Hudson-Kreitman-Aguadé test) were used to detect selection events at different temporal scales. Environmental associations between variation at candidate genes and climatic variables were also examined. These combined approaches detected distinct genes that may be targeted by selection, most of them specific to only one of the two conifers, despite their recent divergence (<10 Ma). An exception was 4-coumarate: CoA ligase, a gene involved in the production of various important secondary products that appeared to play a role in local adaptation processes of both pines. Another remarkable result was that all significant environmental correlations involved temperature indices, highlighting the importance of this climatic factor as a selective driver on Mediterranean pines. The ability to detect natural selection at the DNA sequence level depends on the nature and the strength of the selection events, on the timescale at which they occurred, and on the sensitivity of the methods to other evolutionary forces that can mimic selection (e.g., demography and population structure). Using complementary approaches can help to capture different aspects of the evolutionary processes that govern molecular variation at both intra- and interspecific levels.

Range‐wide phylogeography and gene zones in Pinus pinaster Ait. revealed by chloroplast microsatellite markers

Some 1339 trees from 48 Pinus pinaster stands were characterized by five chloroplast microsatellites, detecting a total of 103 distinct haplotypes. Frequencies for the 16 most abundant haplotypes (pk > 0.01) were spatially interpolated over a lattice made by 430 grid points. Fitting of spatially interpolated values on raw haplotype frequencies at the same geographical location was tested by regression analysis. A range‐wide ‘diversity map’ based on interpolated haplotype frequencies allowed the identification of one ‘hotspot’ of diversity in central and southeastern Spain, and two areas of low haplotypic diversity located in the western Iberian peninsula and Morocco. Principal component analysis (PCA) carried out on haplotypes frequency surfaces allowed the construction of a colour‐based ‘synthetic’ map of the first three PC components, enabling the detection of the main range‐scale genetic trends and the identification of three main ‘gene pools’ for the species: (i) a ‘southeastern’ gene pool, including southeastern France, Italy, Corsica, Sardinia, Pantelleria and northern Africa; (ii) an ‘Atlantic’ gene pool, including all the western areas of the Iberian peninsula; and (iii) a ‘central’ gene pool, located in southeastern Spain. Multivariate and amova analyses carried out on interpolated grid point frequency values revealed the existence of eight major clusters (‘gene zones’), whose genetic relationships were related with the history of the species. In addition, demographic models showed more ancient expansions in the eastern and southern ranges of maritime pine probably associated to early postglacial recolonization. The delineation of the gene zones provides a baseline for designing conservation areas in this key Mediterranean pine.

Performance of Pinus pinaster provenances in Spain : Interpretation of the genotype by environment interaction

The objective of this study was the interpretation of the genotype-environment interaction of 46 maritime pine (Pinus pinaster Ait.) provenances tested at five sites in central Spain. Statistical relationship of the interactions of survival, volume, and polycyclism with several climatic features from the places of origin and the trial sites were analyzed. Factorial regression models and (or) biadditive or multiplicative models were used. Simple factorial regression models were adequate to explain the interaction of the two yield-related variates. Precipitation at places of seed origin and altitude of trial locations as covariates were sufficient to explain the interaction of survival. Altitude of the site of origin and the estimate of the location main effect were sufficient to explain the interaction of wood volume. No simple factorial regression model could be found for polycyclism, a trait related to the form of the tree and wood quality. The interaction was complex enough to require a biadditive model with two terms. The agreement between the estimated value for each trait and their rank according to the means at each location is good enough to allow the selection of provenances based on these models. Breeding for specific adaptation should bring substantial genetic gains.

Genotypic variability and phenotypic plasticity of cavitation resistance in Fagus sylvatica L. across Europe

Xylem cavitation resistance is a key physiological trait correlated with species tolerance to extreme drought stresses. Little is known about the genetic variability and phenotypic plasticity of this trait in natural tree populations. Here we measured the cavitation resistance of 17 Fagus sylvatica populations representative of the full range of the species in Europe. The trees were grown in three field trials under contrasting climatic conditions. Our findings suggest that the genotypic variability of cavitation resistance is high between genotypes of a given population. By contrast, no significant differences were found for this trait across populations, the mean population cavitation resistance being remarkably constant in each trial. We found a significant site effect and a significant site × population interaction, suggesting that cavitation resistance has a high phenotypic plasticity and that this plasticity is under genetic control. The implications of our findings for beech forest management in a context of climate change are discussed.

Divergence among species and populations of Mediterranean pines in biomass allocation of seedlings grown under two watering regimes

Seedlings of four populations each of Pinus pinaster, P. halepensis, P. canariensis and P. pinea were grown in controlled conditions to evaluate both inter- and intra-specific differences in response to watering. We submitted half of the plants to a moderate water stress and after 22 weeks, we recorded height, stem diameter and root, stem and leaves dry weight. Patterns and amounts of phenotypic changes, including changes in biomass allocation, were analysed. We found a scant response in P. canariensis, P. pinaster and P. halepensis presented high population divergence for phenotypic changes, and P. pinea showed marked allocational shifts and no population divergence. The phenotypic changes observed within species are interpreted as a plastic response. The variation encountered within P. halepensis and P. pinaster may be indicative of specialisation to either resource-rich or resource-poor habitats, being populations from favourable sites more plastic. P. pinea exhibited a very uniform plastic response, indicating generalist behaviour.RésuméDes semis de quatre populations de Pinus pinaster, de P. halepensis, de P. canariensis, et de P. pinea ont été élevés en conditions contrôlées pour évaluer au niveau inter- et intra-spécifique les différences de réponse au régime d’alimentation hydrique. Nous avons soumis la moitié des plants à un stress hydrique modéré et après 22 semaines nous avons mesuré leur hauteur, le diamètre de la tige et des racines, le poids sec de la tige et des feuilles. Les modèles et l’importance des changements phénotypiques, incluant les variations d’allocation de biomasse ont été analysés. Nous avons trouvé une faible réponse pour P. canariensis; P. pinaster et P. halepensis ont présenté une importante divergence des populations au plan des changements phénotypiques, et P. pinea a montré une modification sensible au plan de l’allocation de biomasse sans divergence de population. Les changements phénotypiques observés chez les espèces ont été interprétés comme une réponse en terme de plasticité. Les variations rencontrées chez P. halepensis et P. pinaster peuvent être l’indice d’une spécialisation pour des habitats riches ou pauvres en terme de ressources. P. pinea a présenté une plasticité uniforme de réponse, révélant un comportement généraliste.

Effective gene dispersal and female reproductive success in Mediterranean maritime pine (Pinus pinaster Aiton).

Understanding population‐scale processes that affect allele frequency changes across generations is a long‐standing interest in genetic, ecological and evolutionary research. In particular, individual differences in female reproductive success and the spatial scale of gene flow considerably affect evolutionary change and patterns of local selection. In this study, a recently developed maximum‐likelihood (ML) method based on established offspring, the Seedling Neighbourhood Model, was applied and exponentially shaped dispersal kernels were fitted to both genetic and ecological data in a widespread Mediterranean pine, Pinus pinaster Aiton. The distribution of female reproductive success in P. pinaster was very skewed (about 10% of trees mothered 50% of offspring) and significant positive female selection gradients for diameter (γ = 0.7293) and cone crop (γ = 0.4524) were found. The selective advantage of offspring mothered by bigger trees could be due to better‐quality seeds. These seeds may show more resilience to severe summer droughts and microsite variation related to water and nutrient availability. Both approaches, ecological and of parentage, consistently showed a long‐distance dispersal component in saplings that was not found in dispersal kernels based on seed shadows, highlighting the importance of Janzen‐Connell effects and microenvironmental variation for survival at early stages of establishment in this Mediterranean key forest tree.

To grow or to seed: ecotypic variation in reproductive allocation and cone production by young female Aleppo pine (Pinus halepensis, Pinaceae)

Age and size at the first reproduction and the reproductive allocation of plants are linked to different life history strategies. Aleppo pine only reproduces through seed, and, as such, early female reproduction confers high fitness in its infertile highly fire-prone habitats along the Mediterranean coast because life expectancy is short. We investigated the extent of ecotypic differentiation in female reproductive allocation and examined the relation between early female reproduction and vegetative growth. In a common-garden experiment, the threshold age and size at first female reproduction and female reproductive allocation at age seven differed significantly among Aleppo pine provenances of ecologically distinct origin. Significant correlations among reproductive features of the provenances and the ecological traits of origin were found using different analytical tools. In nonlinear models of cone counts vs. stem volume, medium-sized trees (not the largest trees) produced the highest cone yield, confirming that, at the individual level, early female reproduction is incompatible with fast vegetative growth. The contribution of founder effects and adaptation to contrasting fire regimes may be confounding factors. But considering all traits analyzed, the geographical patterns of resource allocation by Aleppo pine suggest ecotypic specialization for either resource-poor (favoring early reproduction) or resource-rich (favoring vegetative growth) habitats.