Mediterranean pines

Target species

MedForAct will focus on three conifers of the genus Pinus native to the Mediterranean basin: Aleppo pine (Pinus halepensis, Mill. 1768), maritime pine (P. pinaster Aiton, 1789), and stone pine (P. pinea L., 1753). Together, these species occupy an area of approximately five million hectares, or ~2 % of the total area of Mediterranean forests (del Río et al. 2017). They share a long history of interaction with humans, which has significantly shaped their biogeographic and demographic history, resulting in their current highly fragmented spatial distribution. 

Ecosystem services

Mediterranean pines have provided mankind with several goods, including timber and firewood, honey and resin, and edible pine nuts (P. pinea). Pine nuts deserve special mention because of their long history of trade across the Mediterranean since ancient times, their high nutritional value, which drives global demand, and their economic importance, with a market value of around €50 million (FAO Forest Resource Assessment 2010). Among the most important ecosystem services provided are carbon sequestration and soil protection against erosion, wind breakers along coastlines and water filtration, protection against salt spray, and the provision of recreational areas (Mechergui et al. 2021).

Phylogeny

The Mediterranean pines in question are part of a clade whose last common ancestor dates back to ~33 million years ago (Ma), when the ancestor of P. pinaster diverged from the lineage that now includes Aleppo pine and stone pine. Two further separate lineages arose at ~30 Ma, including the ancestors of P. pinea on one side and P. halepensis on the other (Jin et al. 2021). These species are moderately sympatric and, since the emergence of the most recent Aleppo pine, have shared at least 15 million years of evolutionary history in the dynamic geoclimatic context that shaped the present-day Mediterranean basin and climate.

Environmental adaptation

Like many other Mediterranean forest species, Aleppo pine, maritime pine and stone pine show adaptation to different habitats (with survival and growth correlating with temperature range and annual precipitation) and intraspecific differentiation in important drought-related functional traits (with water use efficiency and osmotic adjustment correlating with precipitation and cold hardiness; Ramírez‐Valiente et al. 2022). Two important types of adaptive responses can be triggered by environmental heterogeneity in space and time, namely intraspecific local adaptation and convergent local adaptation. The following is a (non-exhaustive) literature review of genes that have been suggested to be involved in environmental adaptation in Mediterranean pines.

Intraspecific local adaptation

Intraspecific (i.e., within-species) local adaptation is a key evolutionary process, driven by spatially divergent natural selection, that allows populations in their own (native) environment to gain an adaptive advantage over any population from outside (Kawecki & Ebert 2004; Savolainen et al. 2013). Intraspecific genetic pathways of local adaptation can evolve in sympatric species when there is sufficient time of separate evolution from a common ancestor, environmental heterogeneity in space and reduced environmental variability in time (Jin et al. 2021; Thompson 2020). The divergence times between the target conifers, their diversified demographic and biogeographic histories, and the known diversification in ecological requirements (e.g., different degrees of drought and cold tolerance) are compatible with the evolution of intraspecific local adaptation to both common and diversified Mediterranean bioclimates, as shown by several studies.

• A study of six putative orthologs for drought tolerance in P. hapelensis and P. pinaster revealed a general trend of intraspecific pathways responding to common environmental stresses, which was attributed to the different biogeographic and demographic histories of these species (Grivet et al. 2013). 

• Several genes belonging to the ASR (Abscisic acid, water Stress, Ripening response)  and dehydrin gene families emerged as candidate targets of selection in P. halepensis and P. pinaster for their protective role against drought, suggesting the involvement of similar gene families but separate pathways to overcome common ecological challenges (Grivet et al. 2011, 2013). 

• A core set of 113 out of 1124 genes were found to be over-expressed in roots, stems and needles of P. pinea and P. pinaster in response to drought stress (Perdiguero et al. 2013). These candidates include genes involved in (i) the synthesis of some stress hormones (e.g., ethylene), (ii) carbohydrate metabolism, which can help maintain turgor pressure during desiccation, and (iii) cell rescue, encoding dehydrins that confer tolerance to drought, heat stress proteins that stabilise cell membranes, and ubiquitins that degrade proteins damaged by desiccation. 

• A genomic signature of local adaptation was observed in P. halepensis along independent altitudinal gradients, suggesting the role of a gene (PIN2) involved in the regulation of growth responses to environmental cues (Ruiz Daniels et al. 2019). 

Convergent local adaptation

Convergent local adaptation can be observed when repeated phenotypic evolution occurs in sympatric species due to similar genetic architectures in response to shared ecological challenges (Conte et al. 2012; Stern 2013). This evolutionary outcome has been estimated to affect 10-18% of genes modulating responses to local temperature variation and wintriness in two distantly related conifer species that diverged 140-190 Ma (lodgepole pine and interior spruce; Yeaman et al. 2016), and is predicted to become more likely as phylogenetic proximity increases (Conte et al. 2012). The concomitant occurrence of a rather close phylogeny (see figure above) but million years of separate evolution are compatible with the evolution of both intraspecifc and convergent local adaptation in the conifers under study. Evidence of convergent local adaptation has been suggested for several orthologs.

• The 4-coumarate-CoA ligase (4cl), a gene involved in phenylpropanoid metabolism and in the response to environmental stress, was found to correlate with temperature-related variables, revealing the importance of temperature as a selective driver in Mediterranean pines (Grivet et al. 2013).

• Phylogenetic analysis, gene-temperature associations and neutrality tests candidate the dehydrin gene family as a potential target for convergent local adaptation to desiccation and related stresses such as wounding, cold, salinity in P. pinaster and P. halepensis (Grivet et al. 2011, 2013). 

• The stone pine is a genetically impoverished species with a circum-Mediterranean distribution (Vendramin et al. 2008). Nevertheless, genetic variation was observed for both regulatory and drought stress response genes that are candidates for local adaptation in other conifer species, possibly revealing ongoing convergent adaptation (Jaramillo-Correa et al. 2020). The gene for Metacaspase 1, a protein that regulates cell death in response to abiotic stress, is one such candidate (Grivet et al. 2013). Overall, however, there has been little evidence of convergent evolution in stone pine (Jaramillo-Correa et al. 2020). 

Climate change impacts on forest genomic resources

Forest species are suffering from the effects of climate change, including disruption of local adaptation (maladaptation), increased extinction rates, and modification/loss of species interactions with cascading effects on biotic interactions and ecosystem services (Anderson et al. 2020; Thompson 2020). Plants can cope with climate change through phenotypic plasticity, by adapting, or by following shifts in optimal ecological conditions through dispersal (Aitken et al. 2008). Widespread species with large populations, fecundity, phenotypic plasticity and standing genetic variation are likely to be able to adapt more quickly than fragmented species with small populations, especially if the underlying architecture of adaptation is polygenic and divergent selection is strong (Aitken et al. 2008; Alberto et al. 2013; Anderson et al. 2020). Migration to the leading edge is predicted to be successful if coupled with rapid adaptation through adaptive gene flow from warmer climates (Aitken et al. 2008). 

It can be observed that Mediterranean pines are no exception to this phenomenon, with an increased pressure from pathogens (for example, the Matsucoccus feytaudi attack on eastern P. pinaster populations, as documented by Di Matteo & Voltas 2016), habitat conditions beyond their climatic optima, delayed adaptation to increased temperature and drought in warm/dry margins, and increased precipitation in wet margins (Fréjaville et al. 2020). This situation is expected to worsen over the next few decades, especially for warm margin populations, which will be forced to chase suitable conditions to higher latitudes and altitudes to avoid extirpation (Fréjaville et al. 2020; Mechergui et al. 2021).

References

Aitken, S. N., Yeaman, S., Holliday, J. A., Wang, T., & Curtis‐McLane, S. (2008). Adaptation, migration or extirpation: climate change outcomes for tree populations. Evolutionary applications, 1(1), 95-111. 

Alberto, F. J., Aitken, S. N., Alía, R., González‐Martínez, S. C., Hänninen, H., Kremer, A., ... & Savolainen, O. (2013). Potential for evolutionary responses to climate change–evidence from tree populations. Global change biology, 19(6), 1645-1661. 

Anderson, J. T., & Song, B. H. (2020). Plant adaptation to climate change—Where are we?. Journal of Systematics and Evolution, 58(5), 533-545. 

Conte, G. L., Arnegard, M. E., Peichel, C. L., & Schluter, D. (2012). The probability of genetic parallelism and convergence in natural populations. Proceedings of the Royal Society B: Biological Sciences, 279(1749), 5039-5047.

del Río, M., et al. (2017). Mediterranean Pine Forests: Management Effects on Carbon Stocks in Managing Forest Ecosystems: The Challenge of Climate Change, Managing Forest Ecosystems 34, DOI 10.1007/978-3-319-28250-3_15 

Di Matteo, G., & Voltas, J. (2016). Multienvironment evaluation of Pinus pinaster provenances: evidence of genetic trade-offs between adaptation to optimal conditions and resistance to the maritime pine bast scale (Matsucoccus feytaudi). Forest Science, 62(5), 553-563. 

Fréjaville, T., Vizcaíno‐Palomar, N., Fady, B., Kremer, A., & Benito Garzón, M. (2020). Range margin populations show high climate adaptation lags in European trees. Global Change Biology, 26(2), 484-495. 

Grivet, D., Sebastiani, F., Alía, R., Bataillon, T., Torre, S., Zabal-Aguirre, M., ... & González-Martínez, S. C. (2011). Molecular footprints of local adaptation in two Mediterranean conifers. Molecular biology and evolution, 28(1), 101-116. 

Grivet, D., Climent, J., Zabal-Aguirre, M., Neale, D. B., Vendramin, G. G., & González-Martínez, S. C. (2013). Adaptive evolution of Mediterranean pines. Molecular Phylogenetics and Evolution, 68(3), 555-566. 

Jaramillo‐Correa, J. P., Bagnoli, F., Grivet, D., Fady, B., Aravanopoulos, F. A., Vendramin, G. G., & González‐Martínez, S. C. (2020). Evolutionary rate and genetic load in an emblematic Mediterranean tree following an ancient and prolonged population collapse. Molecular Ecology, 29(24), 4797-4811. 

Jin, W. T., Gernandt, D. S., Wehenkel, C., Xia, X. M., Wei, X. X., & Wang, X. Q. (2021). Phylogenomic and ecological analyses reveal the spatiotemporal evolution of global pines. Proceedings of the National Academy of Sciences, 118(20), e2022302118. 

Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology letters, 7(12), 1225-1241. 

Mechergui, K., Saleh Altamimi, A., Jaouadi, W., & Naghmouchi, S. (2021). Climate change impacts on spatial distribution, tree-ring growth, and water use of stone pine (Pinus pinea L.) forests in the Mediterranean region and silvicultural practices to limit those impacts. iForest-Biogeosciences and Forestry, 14(2), 104. 

Perdiguero, P., del Carmen Barbero, M., Cervera, M. T., Collada, C., & Soto, Á. (2013). Molecular response to water stress in two contrasting Mediterranean pines (Pinus pinaster and Pinus pinea). Plant physiology and biochemistry, 67, 199-208. 

Ramírez‐Valiente, J. A., Santos del Blanco, L., Alía, R., Robledo‐Arnuncio, J. J., & Climent, J. (2022). Adaptation of Mediterranean forest species to climate: Lessons from common garden experiments. Journal of Ecology, 110(5), 1022-1042. 

Ruiz Daniels, R., Taylor, R. S., González-Martínez, S. C., Vendramin, G. G., Fady, B., Oddou-Muratorio, S., ... & Beaumont, M. A. (2019). Looking for local adaptation: convergent microevolution in Aleppo pine (Pinus halepensis). Genes, 10(9), 673. 

Savolainen, O., Lascoux, M., & Merilä, J. (2013). Ecological genomics of local adaptation. Nature Reviews Genetics, 14(11), 807-820. 

Stern, D. L. (2013). The genetic causes of convergent evolution. Nature Reviews Genetics, 14(11), 751-764. 

Thompson, J. D. (2020). Plant evolution in the Mediterranean: insights for conservation. Oxford University Press, USA. 

Yeaman, S., Hodgins, K. A., Lotterhos, K. E., Suren, H., Nadeau, S., Degner, J. C., ... & Aitken, S. N. (2016). Convergent local adaptation to climate in distantly related conifers. Science, 353(6306), 1431-1433.