PAPEL DE LA EVOLUCION DE LOS FENOTIPOS INTEGRADOS EN LA RESILIENCIA DE LOS PINOS MEDITERRANEOS FRENTE A UN AMBIENTE CAMBIANTE: CAMBIO GENETICO Y PLASTICIDAD FENOTIPICA
RTI2018-094691-B-C32
•
Nombre agencia financiadora Agencia Estatal de Investigación
Acrónimo agencia financiadora AEI
Programa Programa Estatal de I+D+i Orientado a los Retos de la Sociedad
Convocatoria Proyectos I+D+i Retos de Investigación
Año convocatoria 2018
Unidad de gestión Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020
Centro beneficiario INSTITUTO NACIONAL DE INVESTIGACIÓN Y TECNOLOGÍA AGRARIA Y ALIMENTARIA - CSIC
Identificador persistente http://dx.doi.org/10.13039/501100011033
Resultados relacionados
Resultados totales (Incluyendo duplicados): 17Encontrada(s) 1 página(s)
Artículo científico (JournalArticle). 2020
Intraspecific responses to climate reveal nonintuitive warming impacts on a widespread thermophilic conifer
Recercat. Dipósit de la Recerca de Catalunya
- Patsiou, Theofania
- Shestakova, Tatiana A.
- Klein, Tamir
- Di Matteo, Giovanni
- Sbay, Hassan
- Chambel, Maria Regina
- Zas, Rafael
- Voltas Velasco, Jordi
Summary: Many ecologically important forest trees from dry areas have been insufficiently investigated for their ability to adapt to the challenges posed by climate change, which hampers the implementation of mitigation policies. We analyzed 14 common‐garden experiments across the Mediterranean which studied the widespread thermophilic conifer Pinus halepensis and involved 157 populations categorized into five ecotypes. Ecotype‐specific tree height responses to climate were applied to projected climate change (2071-2100 ad), to project potential growth patterns both locally and across the species' range. We found contrasting ecotypic sensitivities to annual precipitation but comparatively uniform responses to mean temperature, while evidence of local adaptation for tree height was limited to mesic ecotypes. We projected intriguing patterns of response range‐wide, implying either height inhibition or stimulation of up to 75%, and deduced that the ecotype currently experiencing more favorable (wetter) conditions will show the largest inhibition. Extensive height reductions can be expected for coastal areas of France, Greece, Spain and northern Africa. Our findings underline the fact that intraspecific variations in sensitivity to precipitation must be considered when projecting tree height responses of dry forests to future climate. The ecotype‐specific projected performances call for management activities to ensure forest resilience in the Mediterranean through, for example, tailored deployment strategies., This study was funded by the Spanish Government (MCIU/AEI/ coordinated grants AGL2015‐68274‐C3‐3‐R and RTI2018‐094691‐B).
Artículo científico (JournalArticle). 2021
The role of maternal age, growth, and environment in shaping offspring performance in an aerial conifer seed bank
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Callejas Díaz, Marta
- Chambel, Maria Regina
- San-Martín-Lorén, Javier
- Gea-Izquierdo, Guillermo
- Santos-del-Blanco, Luis
- Postma, Erik
- Climent Maldonado, José María
11 Pág., Maternal effects have been demonstrated to affect offspring performance in many organisms, and in plants, seeds are important mediators of these effects. Some woody plant species maintain long-lasting canopy seed banks as an adaptation to wildfires. Importantly, these seeds stored in serotinous cones are produced by the mother plant under varying ontogenetic and physiological conditions., This research was supported by the Spanish Government via the Ministry of Science, Innovation and Universities (MICIU) grants AGL2015-68274-C03-1-R and RTI2018-094691-B-C32 and by a predoctoral research fellowship from the Spanish MICIU (BES-2016-077347)., Peer reviewed
DOI: http://hdl.handle.net/10261/269642, https://api.elsevier.com/content/abstract/scopus_id/85126548164
Artículo científico (JournalArticle). 2022
Adaptation of Mediterranean forest species to climate: Lessons from common garden experiments
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Ramírez Valiente, José Alberto
- Santos-del-Blanco, Luis
- Alía Miranda, Ricardo
- Robledo-Arnuncio, Juan José
- Climent Maldonado, José María
21 Pág.
Centro de Investigación Forestal (CIFOR), Mediterranean ecosystems are biodiversity hotspots located between temperate mesic climates and semi-deserts and deserts. Mediterranean climates are characterized by a drought season but its length and severity can be highly variable across regions. In this review, we explored population genetic variation in functional traits and fitness in Mediterranean oak and pine species. We tested the hypothesis that increased drought tolerance has evolved as an adaptation to xeric and warm areas of the Mediterranean climate while increased competitive abilities have been favoured in more mesic regions, following a productivity-persistence trade-off within species. We first reviewed the literature and performed a meta-analysis of studies on Pinus sp. and Quercus sp. from Mediterranean climates, and then analysed a set of unpublished data from Spanish common garden experiments of species from the Mediterranean Basin, searching for evidence of trait genetic variation among populations, local adaptation and trait–environment associations. The meta-analysis showed that 82.9% (95% CI 75.7–89.4) of traits per study showed significant population genetic differentiation and that 52.5% (35.6–69.2) of traits in studies with two or more Mediterranean environments exhibited population-by-environment interaction. Population differences in traits related to drought tolerance, cold hardiness and fitness were usually correlated with provenance precipitation and temperature gradients, suggesting that adaptation to different climatic regimes is an important process driving intraspecific genetic divergence. Within the Spanish trial network, however, predicted fitness functions based on climatic transfer distance failed to reveal significantly higher fitness of populations at experimental sites with climates closer to their provenances’ ones. Neither the literature review nor the new analyses of the Spanish trial network provided evidence of a negative association between growth- and persistence-related traits at the intraspecific level. Synthesis. Population genetic differentiation in functional traits and fitness is common in Mediterranean species, driven, at least in part, by the adaptation to contrasting temperature and precipitation regimes. Because of experimental constraints or biological reality, our study failed to detect a trade-off between resource-use strategies within species, calling for future studies to investigate further whether intraspecific evolution of stress tolerance occurs at the expense of growth potential in Mediterranean environments or not., This study was funded by the European Union Horizon 2020 research and innovation programme under grant agreement No 773383 (B4EST project), the Spanish Ministry of Agriculture (AEG-17-048) and the Spanish Ministry of Science (RTI2018-094691-B-C32). We are thankful to Maurizio Marchi (CNR-IBBR, Italy) and the B4EST climate downscaling tool for providing climate data. Most data used in this study are integrated in the Spanish Network of Forest Genetic Trials (GENFORED). We thank Ismael Aranda for suggestions and comments on the advanced versions of the manuscript. We also thank José María García del Barrio and Eduardo Notivol for the map. Finally, we thank all persons and institutions involved in establishing and measuring field trials and maintaining the network, Peer reviewed
Centro de Investigación Forestal (CIFOR), Mediterranean ecosystems are biodiversity hotspots located between temperate mesic climates and semi-deserts and deserts. Mediterranean climates are characterized by a drought season but its length and severity can be highly variable across regions. In this review, we explored population genetic variation in functional traits and fitness in Mediterranean oak and pine species. We tested the hypothesis that increased drought tolerance has evolved as an adaptation to xeric and warm areas of the Mediterranean climate while increased competitive abilities have been favoured in more mesic regions, following a productivity-persistence trade-off within species. We first reviewed the literature and performed a meta-analysis of studies on Pinus sp. and Quercus sp. from Mediterranean climates, and then analysed a set of unpublished data from Spanish common garden experiments of species from the Mediterranean Basin, searching for evidence of trait genetic variation among populations, local adaptation and trait–environment associations. The meta-analysis showed that 82.9% (95% CI 75.7–89.4) of traits per study showed significant population genetic differentiation and that 52.5% (35.6–69.2) of traits in studies with two or more Mediterranean environments exhibited population-by-environment interaction. Population differences in traits related to drought tolerance, cold hardiness and fitness were usually correlated with provenance precipitation and temperature gradients, suggesting that adaptation to different climatic regimes is an important process driving intraspecific genetic divergence. Within the Spanish trial network, however, predicted fitness functions based on climatic transfer distance failed to reveal significantly higher fitness of populations at experimental sites with climates closer to their provenances’ ones. Neither the literature review nor the new analyses of the Spanish trial network provided evidence of a negative association between growth- and persistence-related traits at the intraspecific level. Synthesis. Population genetic differentiation in functional traits and fitness is common in Mediterranean species, driven, at least in part, by the adaptation to contrasting temperature and precipitation regimes. Because of experimental constraints or biological reality, our study failed to detect a trade-off between resource-use strategies within species, calling for future studies to investigate further whether intraspecific evolution of stress tolerance occurs at the expense of growth potential in Mediterranean environments or not., This study was funded by the European Union Horizon 2020 research and innovation programme under grant agreement No 773383 (B4EST project), the Spanish Ministry of Agriculture (AEG-17-048) and the Spanish Ministry of Science (RTI2018-094691-B-C32). We are thankful to Maurizio Marchi (CNR-IBBR, Italy) and the B4EST climate downscaling tool for providing climate data. Most data used in this study are integrated in the Spanish Network of Forest Genetic Trials (GENFORED). We thank Ismael Aranda for suggestions and comments on the advanced versions of the manuscript. We also thank José María García del Barrio and Eduardo Notivol for the map. Finally, we thank all persons and institutions involved in establishing and measuring field trials and maintaining the network, Peer reviewed
DOI: http://hdl.handle.net/10261/279573, https://api.elsevier.com/content/abstract/scopus_id/85110848497
Artículo científico (JournalArticle). 2022
Straightening the crooked: Intraspecific divergence of stem posture control and associated trade-offs in a model conifer
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Sierra-De-Grado, Rosario
- Pando, Valentín
- Voltas, Jordi
- Zas Arregui, Rafael
- Majada, Juan
- Climent Maldonado, José María
Although the straightening capacity of the stem is key for light capture and mechanical stability in forest trees, little is known about its adaptive implications. Assuming that stem straightening is costly, trade-offs are expected with competing processes such as growth, maintenance, and defence. We established a manipulative experiment in a common garden of Pinus pinaster including provenances typically showing either straight-stemmed or crooked-stemmed phenotypes. We imposed a bending up to 35º on plants aged 9 years of both provenance groups and followed the straightening kinetics and shoot elongation after releasing. Eight months later, we destructively assessed biomass partitioning, reaction wood, wood microdensity, xylem reserve carbohydrates, and phloem secondary metabolites. The experimental bending and release caused significant, complex changes with a marked difference between straight- and crooked-type plants. The straight-type recovered verticality faster and to a higher degree and developed more compression wood, while displaying a transitory delay in shoot elongation, reducing resource allocation to defence and maintaining the levels of non-structural carbohydrates compared with the crooked type. This combination of responses indicates the existence of intraspecific divergence in the reaction to mechanical stresses that may be related to different adaptive phenotypic plasticity., This work was funded by the projects AGL2015-68274-C03 (Spanish Ministry of the Economy, Industry and Competitiveness and by the
European Regional Development Fund), RTI2018-094691-B-C31/C32/C33 (Spanish Ministry of Science, Innovation and Universities, Agencia Estatal de Investigación and European Regional Development Fund), and AGL2007-62335/FOR (Spanish Ministry of Science and Innovation and European Regional Development Fund).
European Regional Development Fund), RTI2018-094691-B-C31/C32/C33 (Spanish Ministry of Science, Innovation and Universities, Agencia Estatal de Investigación and European Regional Development Fund), and AGL2007-62335/FOR (Spanish Ministry of Science and Innovation and European Regional Development Fund).
Set de datos (Dataset). 2021
Datasets from: Adaptation of Mediterranean forest species to climate: lessons from common garden experiments
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Ramírez Valiente, José Alberto
- Santos-del-Blanco, Luis
- Chambel, Maria Regina
- Caño, F.
- Notivol, Eduardo
- Alía Miranda, Ricardo
- Robledo-Arnuncio, Juan José
- Climent Maldonado, José María
We include information (raw Datasets) corresponding to the paper; Adaptation of Mediterranean forest species to climate: lessons from common garden experiments.
Table Journal of Ecology Review.xls. Material used in the metaanalysis
JoE Row data Common garden.xls. Raw data for survival and height used in the study. Multi-environment commong garden data for Pinus canariensis, P. halepensis, P. nigra, P. pinaster, Quercus ilex, and Q. suber.
JoE Dataset4.xls. Data used for the analysis of local adaptation., Techcnial assitance in Data measurements: del Caño, F, Barba D, Chambel R. Data adquisiton was funded by the Spanish Ministry of Agriculture (AEG-17-048) and the Spanish Ministry of Science (RTI2018-094691-B-C32)., Peer reviewed
Table Journal of Ecology Review.xls. Material used in the metaanalysis
JoE Row data Common garden.xls. Raw data for survival and height used in the study. Multi-environment commong garden data for Pinus canariensis, P. halepensis, P. nigra, P. pinaster, Quercus ilex, and Q. suber.
JoE Dataset4.xls. Data used for the analysis of local adaptation., Techcnial assitance in Data measurements: del Caño, F, Barba D, Chambel R. Data adquisiton was funded by the Spanish Ministry of Agriculture (AEG-17-048) and the Spanish Ministry of Science (RTI2018-094691-B-C32)., Peer reviewed
Artículo científico (JournalArticle). 2021
Do cone age and heating mode determine the opening of serotinous cones during wildfires? A new bench scale approach applied to Pinus halepensis Mill
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Madrigal, Javier
- Martín Jiménez, Ángela
- Chambel, Maria Regina
- Guijarro Guzmán, Mercedes
- Hernando Lara, Carmen
- Calleja, Montserrat
- Espinosa, Juncal
- Climent Maldonado, José María
8 Pág.
Instituto de Ciencias Forestales (ICIFOR), Serotiny is a well-known fire adaptive trait in some species, as the Mediterranean conifer Pinus halepensis. However, information about cone opening mechanisms during wildfires and consequences on post fire dispersal is scarce. In addition, standardized methods allowing a realistic simulation of heating modes at bench-scale are not available. In this study, we address for the first time the interacting effects of radiation, convection and direct flame on the opening and seed release of serotinous cones, following a novel repeatable methodology. Using a Mass Loss Calorimeter (MLC) device and a wide range of heat exposures (between 5 and 75 kW m-2) with or without ignition, we intended to simulate realistic cone heating during surface and crown fires in laboratory conditions. Additionally, we included the effect of contrasting serotinous cone ages interacting with heating mode and considering the random individual variation. The proposed methodology has shown a high potential to simulate the complex process of crown fires in relation to cone opening under controlled conditions, detecting a threshold of heat exposure (25-30 kW m-2) for cone opening. We confirmed that heating mode had a highly significant effect in cone opening, interacting with cone age, while cone age effect on its own was marginal. Particularly, ignition significantly increased the efficacy of cone opening and seed release. Moreover, young and old cones behave differently in seed release, both in surface and crown fire simulations. Implementing and adjusting this methodology in other species will allow more realistic and reliable quantitative comparisons than previously attained., This study was supported by the Spanish R&D projects VIS4FIRE (Integrated Vulnerability of Forest Systems to Wildfire: Implications on Forest Management Tools, RTA2017-00042-C05-01 ) and RESILPINE (Understanding the evolution of integrated phenotypes for the resilience of Mediterranean pines in a changing environment, RTI2018-094691-B-C32 ). VIS4FIRE is co-funded by the EU through the FEDER program., Peer reviewed
Instituto de Ciencias Forestales (ICIFOR), Serotiny is a well-known fire adaptive trait in some species, as the Mediterranean conifer Pinus halepensis. However, information about cone opening mechanisms during wildfires and consequences on post fire dispersal is scarce. In addition, standardized methods allowing a realistic simulation of heating modes at bench-scale are not available. In this study, we address for the first time the interacting effects of radiation, convection and direct flame on the opening and seed release of serotinous cones, following a novel repeatable methodology. Using a Mass Loss Calorimeter (MLC) device and a wide range of heat exposures (between 5 and 75 kW m-2) with or without ignition, we intended to simulate realistic cone heating during surface and crown fires in laboratory conditions. Additionally, we included the effect of contrasting serotinous cone ages interacting with heating mode and considering the random individual variation. The proposed methodology has shown a high potential to simulate the complex process of crown fires in relation to cone opening under controlled conditions, detecting a threshold of heat exposure (25-30 kW m-2) for cone opening. We confirmed that heating mode had a highly significant effect in cone opening, interacting with cone age, while cone age effect on its own was marginal. Particularly, ignition significantly increased the efficacy of cone opening and seed release. Moreover, young and old cones behave differently in seed release, both in surface and crown fire simulations. Implementing and adjusting this methodology in other species will allow more realistic and reliable quantitative comparisons than previously attained., This study was supported by the Spanish R&D projects VIS4FIRE (Integrated Vulnerability of Forest Systems to Wildfire: Implications on Forest Management Tools, RTA2017-00042-C05-01 ) and RESILPINE (Understanding the evolution of integrated phenotypes for the resilience of Mediterranean pines in a changing environment, RTI2018-094691-B-C32 ). VIS4FIRE is co-funded by the EU through the FEDER program., Peer reviewed
DOI: http://hdl.handle.net/10261/287879, https://api.elsevier.com/content/abstract/scopus_id/85098167487
Artículo científico (JournalArticle). 2022
Local seed sourcing for sustainable forestry
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Alía Miranda, Ricardo
- Notivol, Eduardo
- Climent Maldonado, José María
- Pérez, Felipe
- Barba, Diana
- Majada, Juan
- García Del Barrio, José Manuel
16 Pág., Seed sourcing strategies are the basis for identifying genetic material meeting the requirements of future climatic conditions and social demands. Specifically, local seed sourcing has been extensively promoted, based on the expected adaptation of the populations to local conditions, but there are some limitations for the application. We analyzed Strict-sense local and Wide-sense local (based on climatic similarity) seed sourcing strategies. We determined species and genetic pools based on these strategies for 40 species and deployment zones in Spain. We also obtained the total number of seed sources and stands for these species in the EU countries. We analyzed the richness of the pools, the relationship with variables related to the use of the species in afforestation, and the availability of seed production areas approved for the production of reproductive material destined to be marketed. This study confirms the existence of extensive species and genetic local pools. Also, that the importance of these pools differs for different species, limitations being derived from the use of forest reproductive material and the existence of approved basic materials. Strategies derived from local seed sourcing approaches are the basis for the use of forest reproductive material because a large number of the species in the area considered in the study are under regulation. However, despite the extensive work done to approve basic materials, limitations based on the availability of seed production areas to provide local material for sustainable forestry are found in those species. Considering a Wide-sense local seed sourcing strategy we provide alternative pools in order to meet social demands under the actual regulations on marketing of reproductive materials., This research was supported by the Project AEG 17-048 established in the frame of the measure 15.2“support to the conservation and use of forest genetic resources” and under Regulation (EU) No 1305/2013 of the European Parliament and of the Council of 17 December 2013 on support for rural development by the European Agricultural Fund for Rural Development (EAFRD) with 75% co-financing (FP). This study was funded by the European Union Horizon 2020 research and innovation programme under grant agreement No 773383 (B4EST project) (RA), and the Ministry of Science (RTI2018-094691-B-C32) (JC). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript., Peer reviewed
DOI: http://hdl.handle.net/10261/304998, https://api.elsevier.com/content/abstract/scopus_id/85144129895
Artículo científico (JournalArticle). 2023
Diversity and enrichment of breeding material for resilience in European forests
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Olsson, Sanna
- Dauphin, Benjamin
- Jorge, Véronique
- Grivet, Delphine
- Farsakoglou, Anna Maria
- Climent Maldonado, José María
- Alizoti, Paraskevi
- Faivre-Rampant, Patricia
- Pinosio, S.
- Milesi, Pascal
- Scalabrin, Simone
- Bagnoli, Francesca
- Scotti, I.
- Vendramin, Giovanni G.
- González-Martínez, Santiago C.
- Fady, Bruno
- Aravanopoulos, Filippos A.
- Bastien, Catherine
- Alía Miranda, Ricardo
11 Pág., Delivering material selected for breeding purposes into the wild in the context of sustainable forest management might reduce the levels of genetic diversity of future forests in comparison to that of natural populations. Another consequence might be a reduction of their resilience under uncertain future climatic and socio-economic conditions if these new populations lack adaptability. Despite the long tradition of breeding activities in Europe, there is still a need to assess the impact of genetically enriched material on forests’ resilience. In this study, we address (1) the genetic diversity of selected material compared to its wild ancestors, and (2) how to enrich breeding material to support forests’ resilience under changing socio-environmental conditions. We analysed 16 study cases of selected material delivered from breeding activities in four European forest tree species (Pinus halepensis Mill., Pinus nigra J.F. Arnold, Pinus pinaster Ait. and Populus nigra L.) with different levels of breeding. To answer these two questions, we first assessed and compared the genetic diversity of selected material versus natural populations using both putatively neutral and adaptive (based on diverging selection) Single Nucleotide Polymorphisms (SNPs). We then suggest how to enrich these populations for resilience under future climatic conditions by defining a core collection for each species including material from populations that will likely disappear under future conditions. Thanks to the large SNP datasets available for our focal species, we were able to detect some trends in our data. Expected and observed heterozygosity values for selected populations were almost always identical. The selected material showed small but significant genetic differentiation from their original population and their inbreeding coefficient was generally lower. However, the level of genetic improvement (i.e. low vs high) was not correlated with the observed genetic differences between selected material and natural populations.The genetic characterization of natural populations distributed across the species range, and the future projection of their range stability, made it possible to identify core-collections that would significantly enrich breeding populations under uncertain future environmental conditions., This work was supported by the European Union’s Horizon 2020 research and innovation programme under grant agreement No 676876-Gentree “Optimizing the management and sustainable use of forest genetic resources in Europe”; the Spanish Ministry of Science [Grant No RTI2018-094691-B-C32]., Peer reviewed
DOI: http://hdl.handle.net/10261/308293, https://api.elsevier.com/content/abstract/scopus_id/85145971679
Artículo científico (JournalArticle). 2020
Seed sourcing strategies considering climate change forecasts: A practical test in scots pine
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Notivol, Eduardo
- Santos-del-Blanco, Luis
- Chambel, Maria Regina
- Climent Maldonado, José María
- Alía Miranda, Ricardo
17 Pág., Research Highlights: We experimentally tested different seed sourcing strategies (local, predictive, climate-predictive, climate-adjusted, composite and admixture) under a climate change high emissions scenario using a Scots pine multi-site provenance test. Background and Objectives: There is an urgent need to conserve genetic resources and to support resilience of conifer species facing expected changes and threats. Seed sourcing strategies have been proposed to maximize the future adaptation and resilience of our forests. However, these proposals are yet to be tested, especially in long-lived organisms as forest trees, due to methodological constraints. In addition, some methods rely on the transfer of material from populations matching the future conditions of the sites. However, at the rear edge of the species, some specific problems (high fragmentation, high genetic differentiation, role of genetic drift) challenge the theoretical expectations of some of these methods. Materials and Methods: We used a Scots pine multi-site provenance test, consisting of seventeen provenances covering the distribution range of the species in Spain tested in five representative sites. We measured height, diameter and survival at 5, 10 and 15 years after planting. We simulated populations of 50 trees by bootstrapping material of the provenance test after removing the intra-site environmental effects, simulating different seed sourcing strategies. Results: We found that local and predictive methods behaved better than methods based on the selection of future climate-matching strategies (predictive-climate and climate-adjusted) and those combining several seed sources (composite and admixture seed sourcing strategies). Conclusions: Despite the theoretical expectations, for Scots pine, a forest tree species at its rear edge of its distribution, seed-sourcing methods based on climate matching or a combination of seed sources do not perform better than traditional local or predictive methods or they are not feasible because of the lack of future climate-matching populations., This research was supported by the Project AEG 17-048 established in the frame of the measure 15.2 “support to the conservation and use of forest genetic resources” and under Regulation (EU) No 1305/2013 of the European Parliament and of the Council of 17 December 2013 on support for rural development by the European Agricultural Fund for Rural Development (EAFRD) with 75% co-financing. This study was funded by the European Union Horizon 2020 research and innovation programme under grant agreement No 773383 (B4EST project), and the Ministry of Science (RTI2018-094691-B-C32)., Peer reviewed
DOI: http://hdl.handle.net/10261/337650, https://api.elsevier.com/content/abstract/scopus_id/85096803588
Artículo científico (JournalArticle). 2024
Adaptive potential of maritime pine under contrasting environments
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Alía Miranda, Ricardo
- Climent Maldonado, José María
- Santos-del-Blanco, Luis
- Gonzalez-Arrojo, Amelia
- Feito, Isabel
- Grivet, Delphine
- Majada, Juan
11 Pág., Predicting the adaptability of forest tree populations under future climates requires a better knowledge of both the adaptive significance and evolvability of measurable key traits. Phenotypic plasticity, standing genetic variation and degree of phenotypic integration shape the actual and future population genetic structure, but empirical estimations in forest tree species are still extremely scarce. We analysed 11 maritime pine populations covering the distribution range of the species (119 families and 8 trees/family, ca. 1300 trees) in a common garden experiment planted at two sites with contrasting productivity. We used plant height as a surrogate of fitness and measured five traits (mean and plasticity of carbon isotope discrimination, specific leaf area, needle biomass, Phenology growth index) related to four different strategies (acquisitive economics, photosynthetic organ size, growth allocation and avoidance of water stress)., Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. This study was funded by European Union’s Horizon 2020 research and innovation program (grant agreement no 773383 B4EST), MITECO2023-AF. 20234TE003, and grant RTI2018-094691-B-C32), and by Junta de Castilla y León (project “CLU-2019-01, co-financed by the European Union (ERDF)., Peer reviewed
DOI: http://hdl.handle.net/10261/349973, https://api.elsevier.com/content/abstract/scopus_id/85181691332
Artículo científico (JournalArticle). 2024
Trade-offs and Trait Integration in Tree Phenotypes: Consequences for the Sustainable Use of Genetic Resources
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Climent Maldonado, José María
- Alía Miranda, Ricardo
- Kärkkäinen, Katri
- Bastien, Catherine
- Benito-Garzón, M.
- Bouffier, L.
- de Dato, Giovanbattista
- Delzon, Sylvain
- Dowkiw, Arnaud
- Elvira-Recuenco, Margarita
- Grivet, Delphine
- González-Martínez, Santiago C.
- Hayatgheibi, Haleh
- Kujala, Sonja T.
- Leplé, J. C.
- Martin-Sanz, Ruth C.
- de Miguel, Marina
- Monteverdi, M. Cristina
- Mutke, Sven
- Plomion, Christophe
- Ramírez Valiente, José Alberto
- Sánchez, Leopoldo
- Solé-Medina, Aida
- Soularue, Jean Paul
- Steffenrem, Arne
- Teani, Angela
- Westin, Johan
- Whittet, Richard
- Wu, Harry
- Zas Arregui, Rafael
- Cavers, Stephen
27 Pág., Purpose of Review: In this review, we synthesise current knowledge on trade-offs among traits in key fitness dimensions and identify major research gaps with the intention of laying the groundwork for a rapid advance in tree breeding for multiple objectives as a key contribution to the sustainability of planted forests in the future. Recent Findings: Trade-offs among growth, reproduction, defence, stress tolerance and product quality predicted theoretically have been reported experimentally in many breeding programmes. Among these trade-offs, the genetic linkage between resistance against biotic threats and growth (or other relevant traits) is particularly critical for the current and future management of forest genetic resources. Maintaining tree growth and wood quality in the novel environments of the future requires the assessment of genetic correlations of target traits with phenology, closely linked to survival to temperature extremes. Improving our current knowledge on the genetic trade-offs of drought tolerance as a breeding objective in forest trees obligates a more precise definition of both the specific traits and the experimental conditions. Published evidence suggests that common target traits in breeding programmes may trade-off with reproductive success and fire-adaptation, and the simultaneous improvement of growth and wood quality traits still remains as a constraint in traditional tree breeding. Summary: Changing environments combined with pests and diseases are challenging plantation forestry worldwide, which implies an urgent need to develop new improvement strategies to build the resilience of forestry for our future environments. It is essential to have a better understanding of how traits interact, especially those important for production, climate and biotic threat resilience, but much of the information is still missing. Since many key trade-offs are affected by the environment, we need new studies under novel environments to forecast levels of multi-trait integration in breeding populations., Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. H2020 773383 (B4EST), RTI2018-094691-B-C32 and C33 (RESILPINE), University of Bordeaux’s France 2030 programme ‘GPR Bordeaux Plant Sciences’., Peer reviewed
DOI: http://hdl.handle.net/10261/357929, https://api.elsevier.com/content/abstract/scopus_id/85188184183
Artículo científico (JournalArticle). 2024
Phylogeography and climate shape the quantitative genetic landscape and range-wide plasticity of a prevalent conifer
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Voltas, Jordi
- Amigó, Ramón
- Shestakova, Tatiana A.
- di Matteo, Giovanni
- Díaz, Raquel
- Zas Arregui, Rafael
21 páginas, 6 figuras, 2 tablas.
Data (Voltas et al., 2023) supporting the results of thisstudy are available in the CORA open repository athttps://doi.org/10.34810/data871. Data (Voltas, 2023)describing the characteristics of populations are availablein Zenodo at https://doi.org/10.5281/zenodo.8079551, The contribution of genetic adaptation and plasticity to intraspecific phenotypic variability remains insufficiently studied in long-lived plants, as well as the relevance of neutral versus adaptive processes determining such divergence. We examined the importance of phylogeographic structure and climate in modulating genetic and plastic changes and their interdependence in fitness-related traits of a widespread Mediterranean conifer (Pinus pinaster). Four marker-based, previously defined neutral classifications along with two ad hoc climate-based categorizations of 123 range-wide populations were analyzed for their capacity to summarize genetic and plastic effects of height growth and survival (age 20) in 15 common gardens. The plasticity of tree height and differential survival were interpreted through mixed modeling accounting for heteroscedasticity in the genotype-by-environment dataset. The analysis revealed a slight superiority of phylogeographic classifications over climate categorizations on the explanation of genetic and plastic effects, which suggests that neutral processes can be at least as important as isolation by climate as a driving factor of evolutionary divergence in a prevalent pine. The best phylogeographic classification involved eight geographically discrete genetic groups, which explained 92% (height) and 52% (survival) of phenotypic variability, including between-group mean differentiation and differential expression across trials. For height growth, there was high predictability of plastic group responses described by different reaction norm slopes, which were unrelated to between-group mean differentiation. The latter differences (amounting to ca. 40% among groups) dominated intraspecific performance across trials. Local adaptation was evident for genetic groups tested in their native environments in terms of tree height and, especially, survival. This finding was supported by Q > F estimates. Additionally, our range-wide evaluation did not support a general adaptive syndrome by which less reactive groups to ameliorated conditions would be associated with high survival and low growth. In fact, a lack of relationship between mean group differentiation, indicative of genetic adaptation, and predictable group plasticity for height growth suggests different evolutionary trajectories of these mechanisms of phenotypic divergence. Altogether, the existence of predictable adaptive-trait phenotypic variation for the species, involving both genetic differentiation and plastic effects, should facilitate integrating genomics and environment into decision-making tools to assist forests in coping with climate change., This study was funded by the Spanish Government, grants RTI2018-094691-B (“RESILPINE,” MCIU/AEI/UE, subprojects C31 and C32) and PID2022-140521OB (“PLASTICPINE, MCIU/AEI/UE, subprojects C31 and C33). We acknowledge the collaboration of the Spanish network of forest genetic trials (GENFORED) for technical cooperation, and F. Righi, L. Ricciotti and E. Fusaro (CREA) for their contributions in gathering data of the Italian trials. Tatiana A. Shestakova acknowledges the support received by the Beatriu de Pinós Programme and the Ministry of Research and Universities of the Government of Catalonia (2020 BP 00126)., Peer reviewed
Data (Voltas et al., 2023) supporting the results of thisstudy are available in the CORA open repository athttps://doi.org/10.34810/data871. Data (Voltas, 2023)describing the characteristics of populations are availablein Zenodo at https://doi.org/10.5281/zenodo.8079551, The contribution of genetic adaptation and plasticity to intraspecific phenotypic variability remains insufficiently studied in long-lived plants, as well as the relevance of neutral versus adaptive processes determining such divergence. We examined the importance of phylogeographic structure and climate in modulating genetic and plastic changes and their interdependence in fitness-related traits of a widespread Mediterranean conifer (Pinus pinaster). Four marker-based, previously defined neutral classifications along with two ad hoc climate-based categorizations of 123 range-wide populations were analyzed for their capacity to summarize genetic and plastic effects of height growth and survival (age 20) in 15 common gardens. The plasticity of tree height and differential survival were interpreted through mixed modeling accounting for heteroscedasticity in the genotype-by-environment dataset. The analysis revealed a slight superiority of phylogeographic classifications over climate categorizations on the explanation of genetic and plastic effects, which suggests that neutral processes can be at least as important as isolation by climate as a driving factor of evolutionary divergence in a prevalent pine. The best phylogeographic classification involved eight geographically discrete genetic groups, which explained 92% (height) and 52% (survival) of phenotypic variability, including between-group mean differentiation and differential expression across trials. For height growth, there was high predictability of plastic group responses described by different reaction norm slopes, which were unrelated to between-group mean differentiation. The latter differences (amounting to ca. 40% among groups) dominated intraspecific performance across trials. Local adaptation was evident for genetic groups tested in their native environments in terms of tree height and, especially, survival. This finding was supported by Q > F estimates. Additionally, our range-wide evaluation did not support a general adaptive syndrome by which less reactive groups to ameliorated conditions would be associated with high survival and low growth. In fact, a lack of relationship between mean group differentiation, indicative of genetic adaptation, and predictable group plasticity for height growth suggests different evolutionary trajectories of these mechanisms of phenotypic divergence. Altogether, the existence of predictable adaptive-trait phenotypic variation for the species, involving both genetic differentiation and plastic effects, should facilitate integrating genomics and environment into decision-making tools to assist forests in coping with climate change., This study was funded by the Spanish Government, grants RTI2018-094691-B (“RESILPINE,” MCIU/AEI/UE, subprojects C31 and C32) and PID2022-140521OB (“PLASTICPINE, MCIU/AEI/UE, subprojects C31 and C33). We acknowledge the collaboration of the Spanish network of forest genetic trials (GENFORED) for technical cooperation, and F. Righi, L. Ricciotti and E. Fusaro (CREA) for their contributions in gathering data of the Italian trials. Tatiana A. Shestakova acknowledges the support received by the Beatriu de Pinós Programme and the Ministry of Research and Universities of the Government of Catalonia (2020 BP 00126)., Peer reviewed
Artículo científico (JournalArticle). 2024
A decade of genetic makeup in the aerial seed bank of a fire-evader tree
DIGITAL.CSIC. Repositorio Institucional del CSIC
- Callejas Díaz, Marta
- Climent Maldonado, José María
- Grivet, Delphine
[EN] Background Aerial seed banks occur in plants that postpone the release of viable seeds, thereby providing a mechanism for population maintenance in unpredictable environments. Seeds retained on the mother trees offer a reservoir of genetic diversity across years, but the pattern and evolutionary consequences of such accumulated diversity are poorly understood. We characterize the genetic layout of an aerial seed bank composed of serotinous cones formed in 2003 and in 2014 in a historically fire‑prone area. Our hypothesis is that within this timeframe, recurrent fires could have modified the genetic makeup of the seed bank. Results Our results did not reveal any genetic difference along the 12‑year period, but indicated a significant genetic variation (13%) of seed banks among trees within the same year. Moreover, progeny from the seed bank showed a 4% increase of observed heterozygosity, together with 14 new alleles, compared to mother trees. Finally, a strong homogenization effect of pollen flow on the genetic diversity was detected, with a very high effective number of fathers in 2003 and 2014. Conclusions Our results highlight the temporal stability of the genetic makeup of aerial seed banks in this fire‑prone area. The maternal genetic differences and an increase of genetic diversity (linked to effective pollen flow) in new generations compared to their maternal progenitors are also noteworthy. Together, these characteristics represent key assets for serotinous forest adaptation and persistence in the face of increasing wildfire activity., [ES] Antecedentes Los bancos de semillas aéreos ocurren en plantas que posponen la liberación de semillas viables, proveyendo de esa manera de un mecanismo de mantenimiento de sus poblaciones en ambientes impredecibles. Las semillas retenidas en árboles madres ofrecen un reservorio de diversidad genética a lo largo de los años, aunque el patrón y consecuencias evolutivas de este mecanismo de diversidad acumulada es poco conocido. Caracterizamos la disposición genética de un banco de semillas aéreo compuesto de conos serótinos formados en 2003 y 2014 en un área históricamente propensa a incendios. Nuestra hipótesis fue que dentro de esta crono‑secuencia, los fuegos recurrentes pueden haber modificado la constitución de este banco de semillas. Resultados Nuestros resultados no revelaron ninguna diferencia genética en los 12 años de estudio, aunque indicaron una variación genética (13%) del banco de semillas entre árboles en un mismo año. Además, la progenie del banco de semillas mostró un 4% de incremento en la heterocigosis, junto con 14 nuevos alelos comparados con los árboles madres. Finalmente, fue detectada una fuerte homogenización, efecto del flujo de polen en la diversidad genética, con un muy efectivo número de padres en 2003 y 2014. Conclusiones Nuestros resultados resaltan la estabilidad temporal de la constitución genética de los bancos de semillas aéreos en esta área de propensa a incendios. Las diferencias genéticas maternales y un incremento en la diversidad genética (ligada al flujo efectivo del polen) en nuevas generaciones, comparados con sus progenitores maternales son también notables. Juntos, esas características representan activos claves para la adaptación y persistencia de bosques serótinos que afrontan una actividad incremental de incendios., Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature., This research was supported by the Spanish Government via the Ministry of Science, Innovation and Universities (MICIU) grants AGL2015-68274-C03-1-R, RTI2018-094691-B-C32 and PID2022-1405210B-C32, as well as by a predoctoral research fellowship from the Spanish MICIU (BES-2016–077347)., Peer reviewed
Artículo científico (JournalArticle). 2020
Seed sourcing strategies considering climate change forecasts: A practical test in scots pine
Zaguán. Repositorio Digital de la Universidad de Zaragoza
- Notivol, E.
- Santos-Del-blanco, L.
- Chambel, R.
- Climent, J.
- Alía, R.
Research Highlights: We experimentally tested different seed sourcing strategies (local, predictive, climate-predictive, climate-adjusted, composite and admixture) under a climate change high emissions scenario using a Scots pine multi-site provenance test.
Background and Objectives: There is an urgent need to conserve genetic resources and to support resilience of conifer species facing expected changes and threats. Seed sourcing strategies have been proposed to maximize the future adaptation and resilience of our forests. However, these proposals are yet to be tested, especially in long-lived organisms as forest trees, due to methodological constraints. In addition, some methods rely on the transfer of material from populations matching the future conditions of the sites. However, at the rear edge of the species, some specific problems (high fragmentation, high genetic differentiation, role of genetic drift) challenge the theoretical expectations of some of these methods.
Materials and Methods: We used a Scots pine multi-site provenance test, consisting of seventeen provenances covering the distribution range of the species in Spain tested in five representative sites. We measured height, diameter and survival at 5, 10 and 15 years after planting. We simulated populations of 50 trees by bootstrapping material of the provenance test after removing the intra-site environmental effects, simulating different seed sourcing strategies.
Results: We found that local and predictive methods behaved better than methods based on the selection of future climate-matching strategies (predictive-climate and climate-adjusted) and those combining several seed sources (composite and admixture seed sourcing strategies).
Conclusions: Despite the theoretical expectations, for Scots pine, a forest tree species at its rear edge of its distribution, seed-sourcing methods based on climate matching or a combination of seed sources do not perform better than traditional local or predictive methods or they are not feasible because of the lack of future climate-matching populations.
Background and Objectives: There is an urgent need to conserve genetic resources and to support resilience of conifer species facing expected changes and threats. Seed sourcing strategies have been proposed to maximize the future adaptation and resilience of our forests. However, these proposals are yet to be tested, especially in long-lived organisms as forest trees, due to methodological constraints. In addition, some methods rely on the transfer of material from populations matching the future conditions of the sites. However, at the rear edge of the species, some specific problems (high fragmentation, high genetic differentiation, role of genetic drift) challenge the theoretical expectations of some of these methods.
Materials and Methods: We used a Scots pine multi-site provenance test, consisting of seventeen provenances covering the distribution range of the species in Spain tested in five representative sites. We measured height, diameter and survival at 5, 10 and 15 years after planting. We simulated populations of 50 trees by bootstrapping material of the provenance test after removing the intra-site environmental effects, simulating different seed sourcing strategies.
Results: We found that local and predictive methods behaved better than methods based on the selection of future climate-matching strategies (predictive-climate and climate-adjusted) and those combining several seed sources (composite and admixture seed sourcing strategies).
Conclusions: Despite the theoretical expectations, for Scots pine, a forest tree species at its rear edge of its distribution, seed-sourcing methods based on climate matching or a combination of seed sources do not perform better than traditional local or predictive methods or they are not feasible because of the lack of future climate-matching populations.
Artículo científico (JournalArticle). 2023
Phylogeography and climate shape the quantitative genetic landscape and range-wide plasticity of a prevalent conifer
Recercat. Dipósit de la Recerca de Catalunya
- Voltas Velasco, Jordi
- Amigó, Ramon
- Shestakova, Tatiana A.
- Matteo, Giovanni
- Díaz, Raquel
- Zas, Rafael
The contribution of genetic adaptation and plasticity to intraspecific phenotypic variability remains insufficiently studied in long-lived plants, as well as the relevance of neutral versusadaptive processes determining such divergence. We examined the importance of phylogeographic structure and climate modulating genetic and plastic changes and their interdependence in fitness-related traits of a widespread Mediterranean conifer(Pinus pinaster). Four marker-based, previously defined neutral classifications along with two ad hoc climate-based categorizations of 123 range-wide populations were analyzed for their capacity to summarize genetic and plastic effects of height growth and survival (age 20) in 15 common gardens. Plasticity of tree height and differential survival were interpreted through mixed modeling accounting for heteroscedasticity in the genotype-by-environment dataset. The analysis revealed a slight superiority of phylogeographic classifications over climate categorizations on the explanation of genetic and plastic effects, which suggests that neutral processes can be at least as important as isolation by climate as driving factor of evolutionary divergence in a prevalent pine. The best phylogeographic classification involved eight geographically discrete genetic groups which explained 92% (height) and 52% (survival) of phenotypic variability, including between-group mean differentiation and differential expression across trials. For height growth, there was predictability of plastic group responses described by different reaction norm slopes, which were unrelated to between-group mean differentiation. The latter differences (amounting to ca. 40% among groups) dominated intraspecific performance across trials. Local adaptation was evident for genetic groups tested in their native environments in terms of tree height and, especially, survival. This finding was supported by QST > FST estimates. Additionally, our range-wide evaluation did not support a general adaptive syndrome by which less reactive groups to ameliorated conditions would be associated with high survival and low growth. In fact, a lack of relationship between mean group differentiation, indicative of genetic adaptation, and predictable group plasticity for height growth suggests different evolutionary trajectories of these mechanisms of phenotypic divergence. Altogether, the existence of predictable adaptive-trait phenotypic variation for the species, involving both genetic differentiation and plastic effects, should facilitate integrating genomics and environment into decision-making tools to assist forests to cope with climate change., This study was funded by the Spanish Government, grants RTI2018-094691-B (“RESILPINE”, MCIU / AEI / UE, subprojects C31 and C32) and PID2022-140521OB (“PLASTICPINE, MCIU / AEI / UE, subprojects C31 and C33). We acknowledge the collaboration of the Spanish network of forest genetic trials (GENFORED) for technical cooperation, and F. Righi, L. Ricciotti and E. Fusaro (CREA) for their contributions in gathering data of the Italian trials. T atiana A. Shestakova acknowledges the support received by the Beatriu de Pinós Programme and the Ministry of Research and Universities of the Government of Catalonia (2020 BP 00126)
Artículo científico (JournalArticle). 2023
Phylogeography and climate shape the quantitative genetic landscape and range-wide plasticity of a prevalent conifer
Repositori Obert UdL
- Voltas Velasco, Jordi
- Amigó, Ramon
- Shestakova, Tatiana A.
- Matteo, Giovanni
- Díaz, Raquel
- Zas, Rafael
The contribution of genetic adaptation and plasticity to intraspecific phenotypic variability remains insufficiently studied in long-lived plants, as well as the relevance of neutral versusadaptive processes determining such divergence. We examined the importance of phylogeographic structure and climate modulating genetic and plastic changes and their interdependence in fitness-related traits of a widespread Mediterranean conifer(Pinus pinaster). Four marker-based, previously defined neutral classifications along with two ad hoc climate-based categorizations of 123 range-wide populations were analyzed for their capacity to summarize genetic and plastic effects of height growth and survival (age 20) in 15 common gardens. Plasticity of tree height and differential survival were interpreted through mixed modeling accounting for heteroscedasticity in the genotype-by-environment dataset. The analysis revealed a slight superiority of phylogeographic classifications over climate categorizations on the explanation of genetic and plastic effects, which suggests that neutral processes can be at least as important as isolation by climate as driving factor of evolutionary divergence in a prevalent pine. The best phylogeographic classification involved eight geographically discrete genetic groups which explained 92% (height) and 52% (survival) of phenotypic variability, including between-group mean differentiation and differential expression across trials. For height growth, there was predictability of plastic group responses described by different reaction norm slopes, which were unrelated to between-group mean differentiation. The latter differences (amounting to ca. 40% among groups) dominated intraspecific performance across trials. Local adaptation was evident for genetic groups tested in their native environments in terms of tree height and, especially, survival. This finding was supported by QST > FST estimates. Additionally, our range-wide evaluation did not support a general adaptive syndrome by which less reactive groups to ameliorated conditions would be associated with high survival and low growth. In fact, a lack of relationship between mean group differentiation, indicative of genetic adaptation, and predictable group plasticity for height growth suggests different evolutionary trajectories of these mechanisms of phenotypic divergence. Altogether, the existence of predictable adaptive-trait phenotypic variation for the species, involving both genetic differentiation and plastic effects, should facilitate integrating genomics and environment into decision-making tools to assist forests to cope with climate change., This study was funded by the Spanish Government, grants RTI2018-094691-B (“RESILPINE”, MCIU / AEI / UE, subprojects C31 and C32) and PID2022-140521OB (“PLASTICPINE, MCIU / AEI / UE, subprojects C31 and C33). We acknowledge the collaboration of the Spanish network of forest genetic trials (GENFORED) for technical cooperation, and F. Righi, L. Ricciotti and E. Fusaro (CREA) for their contributions in gathering data of the Italian trials. T atiana A. Shestakova acknowledges the support received by the Beatriu de Pinós Programme and the Ministry of Research and Universities of the Government of Catalonia (2020 BP 00126)
Artículo científico (JournalArticle). 2020
Intraspecific responses to climate reveal nonintuitive warming impacts on a widespread thermophilic conifer
Repositori Obert UdL
- Patsiou, Theofania
- Shestakova, Tatiana A.
- Klein, Tamir
- Di Matteo, Giovanni
- Sbay, Hassan
- Chambel, Maria Regina
- Zas, Rafael
- Voltas Velasco, Jordi
Summary: Many ecologically important forest trees from dry areas have been insufficiently investigated for their ability to adapt to the challenges posed by climate change, which hampers the implementation of mitigation policies. We analyzed 14 common‐garden experiments across the Mediterranean which studied the widespread thermophilic conifer Pinus halepensis and involved 157 populations categorized into five ecotypes. Ecotype‐specific tree height responses to climate were applied to projected climate change (2071-2100 ad), to project potential growth patterns both locally and across the species' range. We found contrasting ecotypic sensitivities to annual precipitation but comparatively uniform responses to mean temperature, while evidence of local adaptation for tree height was limited to mesic ecotypes. We projected intriguing patterns of response range‐wide, implying either height inhibition or stimulation of up to 75%, and deduced that the ecotype currently experiencing more favorable (wetter) conditions will show the largest inhibition. Extensive height reductions can be expected for coastal areas of France, Greece, Spain and northern Africa. Our findings underline the fact that intraspecific variations in sensitivity to precipitation must be considered when projecting tree height responses of dry forests to future climate. The ecotype‐specific projected performances call for management activities to ensure forest resilience in the Mediterranean through, for example, tailored deployment strategies., This study was funded by the Spanish Government (MCIU/AEI/ coordinated grants AGL2015‐68274‐C3‐3‐R and RTI2018‐094691‐B).