Figure 1. Processes (blue) and products (green) developed in the framework of this thesis
The main objective posed in this thesis was to contribute to the conservation-access-utilization continuum of plant genetic resources at the national level, focusing on CWR as a source of novel genetic variation worth to be preserved in the interest of food security, given the limited genetic diversity held by current crops and the challenges brought by climate change. In this sense, not only the taxonomic diversity of CWR was taken into account as a conservation target, but also the genetic diversity and potential adaptations to biotic and abiotic stresses that their populations contain. To that aim, we have prioritized CWR of importance for Spain and applied ecogeographical approaches to estimate the among-population genetic diversity of CWR populations, to contribute to a proposal of sites for in situ conservation and ex situ collection, strengthening the access and, in this manner, the utilization of these valuable plant genetic resources. This discussion section is structured in three subsections relating to the i) identification and prioritization of CWR, ii) conservation of CWR and iii) access and utilization of CWR. The genetic variation of adaptive value component is transversally discussed over the three subsections, as the genetic diversity held by CWR must be the basis for the design of conservation plans that should pursue boosting the use of CWR as gene donors for plant breeding. Figure 1 shows a simplified schema of the processes involved and the products obtained in this thesis, which are the main subjects of this general discussion.
Figure 1. Processes (blue) and products (green) developed in the framework of this thesis
The broad definition of a crop wild relative (CWR) as a wild plant species closely related to a crop provides an ambiguous context for the identification of CWR, sometimes leading to consider as much as 80% of the national Floras as CWR species. This is, for instance, the case of Spain and other countries in the EuroMediterranean region (Kell et al., 2007). However, in other cases, a much lower proportion of the Flora of the countries is considered a CWR species (e.g. 14.8% in The Netherlands (van Treuren et al., 2017), around 10% in Benin (Idohou et al., 2013), 35% in England (Fielder et al., 2015a) or 43% in Scotland (Fielder et al., 2015b)). Accordingly, and accounting for the differences in plant species richness among countries, the number of species in national CWR checklists can be very different. For example, we find checklists with more than 24000, 6500 and 7000 species in China (Kell et al., 2015), Italy (Ciancaleoni et al., 2021) and Turkey (Tas et al., 2019), respectively, and other checklists with less than 500 species (e.g. Zambia (Mwila et al., 2019)), Benin and The Netherlands. Nevertheless, among the published checklists, the final number of species normally ranges between 1200 species (England and Scotland) and 2000 - 3000 species (e.g. Russia (Smekalova, 2008; Chukhina et al., 2020), United Kingdom (Maxted et al., 2007); Portugal (Magos Brehm et al., 2008), Czech Republic (Taylor et al., 2017), Finland (Fitzgerald, 2013), Cyprus (Phillips et al., 2014) or Norway (Phillips et al., 2016), which implies, in every case, larger checklists than the Spanish checklist proposed in this thesis (929 species). Overall, these are large numbers for implementing effective conservation strategies for CWR and all these checklists were subsequently prioritized.
Criteria for prioritization varies among countries, depending on their idiosyncrasy, but there are shared criteria that all countries applied. The two criteria applied in all cases are ease of crossability with crops (except for the United Kingdom) and economic value of related crops. The application of both criteria, whether the approach for the generation of checklists was monographic (selection of crops and then list related wild species) or floristic (list of all CWR in the area using floristic inventories) (Maxted et al., 2011; Magos Brehm et al., 2013), resulted in the definition of different groups of CWR depending on the use of the related crop. In this sense, in Spain we established four categories (Food, Fodder and Forage, Ornamental and Industrial and Other Uses) that were similarly established in all consulted national inventories, with the exception of Venezuela (Berlingeri and Crespo, 2012), Mexico (Contreras-Toledo et al., 2018) and Italy (Ciancaleoni et al., 2021), that only focused on CWR related to human food. Thus, the overall trend followed in the last decade, and opposite to the suggested existence of biases favoring wild food crop relatives against other groups such as ornamentals or forage species in the generation of checklists and inventories (Meilleur and Hodgkin, 2004), is the inclusion of categories not only important for food security, but also for the economic sustainability of the countries. In any case, the criteria applied for the prioritization of CWR in Spain was intentionally biased in favor of food and forage categories in the interest of food security. This preferential treatment is also implemented in other national inventories: for example, Khoury et al., (2013) only prioritized CWR in major agricultural crops for the USA, Fielder et al. (2015a and 2015b) only prioritized species in the human and animal food categories, and Cyprus and Turkey only included these two categories in their inventories (Phillips et al., 2014; Tas et al., 2019).
Following on the main criteria applied for prioritization of checklists, in Spain we considered as a priority those CWR classified in any of the IUCN threat categories or those endemic to the country (excluding Ornamental and Industrial and Other uses categories, as explained above). Regarding relative threat status, it is worth mentioning that it is a common criterion for prioritization of CWR as shown in the processes followed by 10 out of the 18 published national prioritized inventories (Venezuela, Finland, USA, China, Scotland, England, Turkey, The Netherlands, Russia and United Kingdom) and in the prioritization of plant genetic resources for ex situ collection in Israel (Barazani et al., 2008). Furthermore, it is also a widespread criterion for prioritization when following point scoring procedures (i.e., assigning values according to agreed criteria, as first described for CWR prioritization in Portugal (Magos-Brehm et al., 2010) and subsequently applied in the prioritization of inventories of Benin (Idohou et al., 2013), Mexico (Contreras-Toledo et al., 2018) or Zambia (Mwila et al., 2019), increasing to 13 the number of countries the threat status criterion for prioritization. The endemic status is also a common criterion used to select those CWR of particular importance for the country. Except for China or USA, all countries apply the endemicity criterion for prioritization or similar criteria that considers its rarity (e.g. Russia) or national distribution (Mexico, Zambia or Benin) of inventoried CWR.
Last, but not least, the native status of prioritized CWR should be addressed in this discussion, directly linking to genetic diversity of CWR. In this sense, we found different strategies among consulted inventories. Introduced and naturalized taxa are included in most of the inventories (e.g., Portugal, Italy, Zambia, the Czech Republic, Norway, Scotland, England, the USA, Benin, Venezuela), claiming that these genetic resources occurring in the country and linked to important crops should be taken into account. For instance, Bossdorf et al. (2005) argue that the evolution in the country (although short) might have provided these CWR with useful genetic diversity for crop breeding. On the contrary, highly biodiverse countries such as Turkey or China, directly focused on native wild species, as done in the Spanish case. As discussed in Chapter 1, both approaches may entail benefits, however it is expected a higher genetic variation in native CWR, as they are closer to their centers of diversity (Corinto, 2014). In this sense, and despite the inclusion of introduced and naturalized CWR in the inventories, many of them restrict their presence in the prioritized inventories. That is the case for the selected CWR for ex situ collection in Israel or priority CWR in Benin; the case of Scotland and the Czech Republic in which only native or archeophytes were considered for prioritization; the Netherlands which only considered naturalized or introduced species if these naturalization events took place before 1900, or the USA, in which higher priority was given to native taxa.
The assessments of CWR conservation status - both in situ and ex situ- are the starting point to evaluate the preservation of CWR in each country. Remarkably, the conservation status assessment has been traditionally performed independently, separating in situ and ex situ actions. This is partly due to the different responsibilities granted to institutions taking care of conservation actions, assuming that genebanks implement ex situ conservation actions and that protected areas managers take care of the in situ conservation. In most cases, although pursuing the same conservation objective, these different actions are uncoordinated, causing gaps in conservation actions. Furthermore, if particularly focusing on CWR, their in situ conservation is neglected in many cases due to a simplified view that assumes that protected area managers can easily adapt ongoing management plans to include CWR (Hunter et al., 2012). Hunter et al. (2012) also warned about the threats faced by gene banks for the ex situ conservation of CWR, based on the lack of coordinated systems and insecure funding, facts that might compromise the adequate conservation of the accessions. Thus, CWR preservation must involve multiple actors that are expected to coordinate actions to achieve conservation goals (Magos Brehm et al., 2013). The implementation of assessments for CWR conservation must seek the complementary conservation, developing integrated strategies (Maxted et al., 2015) and management plans (Iriondo et al., 2021). In this sense, in this thesis both approaches have been explored searching for complementary conservation: we have evaluated the distribution of priority CWR and their ex situ conservation status (Chapters 1 and 2) and performed gap and complementarity analyses using protected areas in the Natura 2000 network for the identification of suitable sites for the establishment of genetic reserves (Chapters 2 and 3). In line with this, most of the above-mentioned inventories of other countries have also been subject of in situ and ex situ conservation assessments. For instance, in situ conservation status was evaluated for priority CWR of Benin, Portugal, Venezuela, Finland, Cyprus, England, Scotland, Norway, the Czech Republic, Turkey, Zambia, United Kingdom and Russia, including also a regional global assessment (Vincent et al., 2019). The ex situ conservation status was assessed for Portugal, Venezuela, USA, England, Scotland and Norway, plus the global assessment performed by Castañeda-Álvarez et al. (2016). Furthermore, The Netherlands assessed the vulnerability of CWR populations to climate change, in an attempt to clearly direct conservation efforts in a pragmatic manner. The lack of evaluation of the vulnerability of species or sites to climate change in this thesis might be considered as a limitation, as it might compromise the long-term stability of genetic reserves. However, the work on conservation of CWR in Spain has been continued beyond the development of this thesis and these type of analyses are now included in the National Strategy for the Conservation and Use of CWR and wild harvested plants of Spain (Molina Pertíñez et al. in press). In this Strategy, the vulnerability of CWR to climate change is addressed, making this issue one of the objectives to accomplish within the Goal A of the Strategy.
The in situ conservation assessment by any of the methodologies used (i.e. richness analysis, gap analyses against protected areas networks or complementarity analyses using protected areas or cells) is evidently affected by the amount and quality of the available chorological data. In this thesis, the distribution data for in situ evaluation was obtained from the Global Information Facility (GBIF, www.gbif.org) which is, up to date, the most used open access species distribution database. However, this database is also reported to contain biases in the available data due to different sampling efforts, national involvement and funding, and even because of societal and taxonomic preferences (Beck et al., 2014; Troudet et al., 2017; Ronquillo et al., 2020). These biases have been discussed in recent works addressing European CWR complementary conservation, acknowledging also a low participation of certain countries in the GBIF database or restriction on access to sensitive data (i.e., threatened species, narrow endemic taxa) (Rubio Teso et al., 2021). Taking into account these limitations and the overall representation of high priority CWR in protected areas in Spain obtained (74% of target species have at least one population in Natura 2000, Chapter 2), we consider that CWR in Spain are well represented in protected areas, as our findings can be considered as conservative results (i.e., we can expect more CWR species and populations to occur inside protected areas). However, the mere presence of CWR populations within the limits of protected areas does not guarantee their conservation and, much less, the conservation of their genetic diversity.
It is worth mentioning another novel approach used for the conservation assessment of CWR diversity. That is the case of the recent work by González-Orozco et al., (2021) who applied a phylogenetic approach in combination with species distribution modeling to assess the in situ and ex situ conservation status of Colombian CWR. They stress the importance of paying attention not only the taxonomic richness but also to the suitability of the preserved genetic diversity for crop breeding when planning conservation actions for CWR (i.e. take into account genetic compatibility with crops; issue that has been addressed in this thesis by the application of the gene pool and taxon group concept, Chapter 1).
Conservation of genetic diversity is a priority in conservation management and should aim to preserve the evolutionary potential of the species in the long term (Foster Huenneke, 1991). The concern in the conservation of genetic diversity and how to approach it has been largely discussed in the context of both threatened plant species and plant genetic resources conservation. For instance, Brown and Briggs, (1991), already 30 years ago, suggested the sampling of, at least, five populations to adequately cover and ex situ preserve the genetic diversity of endangered species. They argued that endangered species are not widely distributed and normally have few populations. These minimum was further extended to 50 sites by Brown and Marshall in 1995, adducing that distribution restrictions experienced by threatened species are not applicable to non-endangered taxa, and thus a higher number of populations was needed to cover the genetic diversity of these species. Steps forward in the estimation of the genetic diversity of the species, led to the proposal of sampling at least 35% of the known populations of a species, targeting in this way 70% of the genetic diversity - avoiding arbitrary numbers that might not suit each target species - for in situ conservation planning (Whitlock et al., 2016). Up to date, the minimum of five populations is the most common used indicator in the field of CWR to assess their in situ or ex situ conservation status. Both the in situ and ex situ assessments performed in England (Fielder et al., 2015a) and Scotland (Fielder et al., 2015b) proposed the threshold of five populations/accessions to evaluate the conservation status of the targeted CWR. Concerning the ex situ assessments, five accessions were also the minimum threshold settled for Finland (Fitzgerald, 2013), Norway (Phillips et al., 2016) or Zambia (Mwila et al., 2019) and slightly increased to a minimum of ten accessions in the global assessment of the ex situ conservation of CWR by Castañeda-Álvarez et al. (2016). In this thesis, both the minimum five populations/accessions and the 35% threshold of populations have been assessed (Chapter 1 and Chapter 2) as starting point for the evaluation of the conservation of genetic diversity.
Following on the importance of not only the genetic diversity of a species, but also in its potential adaptive value, Brown and Briggs (1991) suggested the interest on sampling diverse ecotypes as a source of potential adaptations, idea that directly links to the ecogeographic approach used in this thesis (Chapter 3 and Chapter 4). The use of Ecogeographic Land Characterization maps (ELC maps) is considered as a step forward in the estimation of genetic variation of adaptive value for plant genetic resources conservation (Parra-Quijano et al., 2020). Having in mind that the main objective for the establishment of a genetic reserve of CWR is the preservation of genetic diversity of the species and the evolutionary potential of their populations (Maxted et al., 2008; Iriondo et al., 2012), the use of ELC maps is widely followed in the conservation assessments of CWR. For instance, Phillips et al. (2016) used the ELC categories for sampling design in Norway, trying to cover the full ecogeographic range of the species’ populations and assessed the ELC categories representation within protected areas. Similar approaches were followed for the conservation assessments in Sweden (Weibull and Phillips, 2020), Mexico (Contreras-Toledo et al., 2019), the Czech Republic (Taylor et al., 2017), in the global in situ assessment carried out by Vincent et al. (2019) and similar maps were used in the global ex situ analyses of Castañeda-Álvarez et al. (2016).
In this thesis, not only ELC maps have been used, but we have also proposed an innovative ELC application by linking populations to ELC categories in which they occur (Chapter 3). We propose a new conservation target unit that is built by joining the populations’ occurrences of CWR to each of the ELC categories in which they occur, putting the focus on the adaptive value of each population of a species. To our knowledge, this is the first time that such combinations are used as conservation target units. Further to current approaches in which ELC representation of in situ CWR populations is assessed (Rubio Teso et al., 2013; Phillips et al., 2016; Taylor et al., 2017; Contreras-Toledo et al., 2019; Vincent et al., 2019; Weibull and Phillips, 2020) or ex situ collections planned or evaluated in their genetic representation according to ELC categories (Parra-Quijano et al., 2012a; Garcia et al., 2017; García et al., 2017) this methodology proposes to conserve at least one population of each of the CWR-Eco combinations and cover in this way the overall potential genetic diversity of the targeted species.
Based on the hypothesis that different environments can exert divergent selective pressures on plant populations, and thus genetic differentiation in genes of adaptive value (Thormann et al, 2014), Parra-Quijano et al. (2012b) provided a conceptual framework supporting the applicability of ELC maps for the design of conservation plans for plant genetic resources. In this way, ELC maps have been reported to show a good performance for predicting phenotype differentiation for Lupinus species in the field according to ELC categories (Parra-Quijano et al., 2012a). Nonetheless, linking the genetic diversity to environmental patterns does not always find a close association. For instance, Foster Huenneke (1991) provided some examples of unsuccessful correlations, citing some works carried out in the decade of the 70’s (mainly with isozymes). In a similar way, Thormann et al. (2016b) did not find a significant correlation among climatic differences and genetic structure in barley using microsatellites markers. However, it should be noted that these works do not estimate genetic diversity of adaptive value, but neutral genetic diversity. Neutral genetic diversity, by definition, does not affect fitness, it is not subjected to selective pressures and, therefore, does not allow to know to which extent the evolutionary and adaptive potential of a species could be affected by environmental conditions (González Campos, 2019).
More recently, and using data from sequenced regions that are neutral and also under selection, Reeves and Richards (2018) claimed that geographic and environmental distances are not good proxies for the estimation of functional genetic diversity, finding biases in haplotypic representation in Populus and Soighum species. However, García Sánchez (2020) provided some limitations to the findings of Reeves and Richards (2018), pointing to the lack of edaphic variables in the populations characterization and also that they did not take into account environmental variables’ contribution to the distribution of the species, contrary to what is done for the generation of ELC maps. In addition, Di Santo and Hamilton (2020) tested the neutral, adaptive and functional genetic diversity of 15 plant species using geographic and environmental distances as predictors for such diversity, providing strong arguments (close to 71% of adaptive variation and 45% of functional diversity captured) for the use of environmental distances in the design of ex situ collecting plans.
Most published works related to CWR conservation consider multi-species approaches to increase the efficiency of in situ conservation. For example, richness analyses are applied in the collecting strategy of 98 CWR to cereal crops in Spain (García et al., 2017), also in the proposal of 150 sites for global conservation of CWR (Vincent et al., 2019) or for the proposal of sites for the establishment of genetic reserves in the UK (Maxted et al., 2007). Complementarity analyses, iterative processes that maximize the number of species in the minimum number of places (Rebelo, 1994), are also a methodology that intends to protect multiple species at the minimum cost. Complementarity analyses have been applied in the conservation assessments of Norway, Cyprus, Zambia or Turkey, just to cite some. Both richness and complementarity analyses have been implemented in this thesis (Chapter 1, Chapter 2 and Chapter 3), and results show that they are an excellent approach to conserve CWR in situ and ex situ in Spain. However, the increment in the number of target conservation units, resulting when the combination of CWR with ELC categories is used, may considerably increase the resources needed to implement in situ and ex situ conservation actions. Therefore, there is an urgency to implement more efficient approaches based on multiple-species conservation. The integration of phytosociological approaches may be helpful in this regard. Results obtained in Chapter 3 highlight the usefulness of phytosociological associations to combine multiple-species conservation along with the potential genetic diversity their populations might contain. Since this methodology has been implemented to a reduced group of CWR, its application to other groups of CWR must be tested. This approach might be useful to enhance the already established genetic reserves of specific CWR with allied CWR species. This could be the case for the established network of Apium genetic reserves in Germany (Bonisch et al., 2015) or the proposed genetic reserves of Beta relatives (Frese et al., 2017).
The establishment of genetic reserves should contemplate the current and future utilization of the genetic diversity preserved, making it available for potential users (Maxted et al., 1997). Besides, one of the aims of the ex situ conservation is to make available the material both to reinforce natural populations or to be used in scientific essays, among others (Bacchetta et al., 2008). In this way, the access to genetic diversity to be used would be linking the conservation efforts to the sustainable use of these genetic resources, as suggested by Maxted et al. (2008). However, an enhanced access to plant material whether from the in situ genetic reserves or from the ex situ collections, needs a previous characterization of the contained diversity, both in the genotypic and the phenotypic component. In this way, potential users could orientate sampling and trials efforts; otherwise, the effective access to genetic variation of adaptive value would be impractical. The genotypic characterization of all populations that are part of a genetic reserve network or in a gene bank collection is a costly and time-consuming process (Dulloo et al., 2008). Thus, the implementation of methodologies that may help the characterization of genetic variation of adaptive value is a key element when designing conservation plans aimed also to facilitate the access to such variation.
Falconer (1952) already proposed the selection of populations under the same environment in which the improved breed is destined to live. That is the principle applied to the selection of CWR for crop breeding through the predictive characterization methodology (Thormann et al., 2014a, 2016a) and the Focused Identification of Germplasm Strategy (FIGS) (Mackay and Street, 2004). Heterogeneous environmental conditions, by generating different types of limitations to living organisms, are likely to promote divergent selection in the populations of a given species and lead to phenotypic differentiation through local adaptation. Predictive characterization aims to help in the selection of germplasm for breeding and pre-breeding purposes, identifying CWR populations with higher probabilities of containing trait adaptations than if randomly chosen. To reach this objective, the incorporation of indicators helping in the discrimination of genetic variation of adaptive value is required. In this regard, predictive characterization techniques involve the use of ecogeographic information, including bioclimatic, edaphic, geophysic and other environmental variables to characterize populations. Furthermore, implications of phenotypic plasticity (i.e., the capacity of some genotypes to produce different phenotypic responses depending on the environmental pressures) are not tested in these works.
FIGS and predictive characterization techniques have been shown useful for the identification of germplasm with adaptive traits for crop breeding, by using climatic and environmental variables in the search of adaptive diversity. Regarding the FIGS approach (used with landraces and cultivated diversity), and just to cite some examples, Khazaei et al. (2013) found ecotypic differentiation due to drought pressures in faba bean, Bari et al. (2012) reported resistance to wheat stem rust associated to certain environments and Endresen et al. (2011) tested the subset selections for wheat stem rust and barley net blotch resistances, successfully finding correlations between resistance and certain climate variables. On the other hand, although predictive characterization is becoming popular in the search for adaptive traits in CWR (Thormann et al., 2014b; Garcia et al., 2017; Rubio Teso et al., 2020), works validating the results of predictive characterization subsets are still scarce. García Sánchez et al., (2019) experimentally validated the results obtained through this methodology, finding a significant association between the ecogeographic variables used and the acyanogenic status of white clover. Although further experimental studies are needed to validate the results of this approach, based on the successful results of the FIGS methodology with landraces, we expect similar or even higher performance of predictive characterization techniques with CWR. That is because, contrary to landraces, CWR have only evolved under natural selective pressures and thus, one would expect to find stronger correlations between adaptive traits and the type of environment. Nonetheless, experimental essays and quantitative genetic studies to assess the wide applicability and appropriate scale of these methodologies are unavoidable steps to adequately assess the benefits of predictive characterization.
In conclusion, the link between conservation and access to the genetic diversity of adaptive value of CWR is approached in this thesis through the identification of priority CWR of interest for Spain (Chapter 1), the identification of high-priority CWR that are in urgent need of conservation (Chapter 2), the proposal of establishment of multispecies genetic reserves considering adaptive genetic variation - through the use of ELC maps - (Chapter 3) and the proposal of populations for collecting germplasm of wild lentil as candidates in their tolerance to drought, soil salinity and waterlogging and their resistance to lentil rust (Chapter 4), taking into account environmental variables for the selection of subsets.
Bacchetta, G., Bueno Sánchez, A., Fenu, G., Jiménez-Alfaro, B., Mattana, E., Piotto, B., et al. eds. (2008). Conservación ex situ de plantas silvestres. Principado de Asturias / La Caixa.
Barazani, O., Perevolotsky, A., and Hadas, R. (2008). A problem of the rich: Prioritizing local plant genetic resources for ex situ conservation in Israel. Biol. Conserv. doi:10.1016/j.biocon.2007.10.014.
Bari, A., Street, K., Mackay, M., Endresen, D. T. F., de Pauw, E., and Amri, A. (2012). Focused identification of germplasm strategy (FIGS) detects wheat stem rust resistance linked to environmental variables. Genet. Resour. Crop Evol. 59, 1465-1481. doi:10.1007/s10722-011-9775-5.
Beck, J., Boller, M., Erhardt, A., and Schwanghart, W. (2014). Spatial bias in the GBIF database and its effect on modeling species’ geographic distributions. Ecol. Inform. 19, 10-15. doi:10.1016/j.ecoinf.2013.11.002.
Berlingeri, C., and Crespo, M. B. (2012). Inventory of related wild species of priority crops in Venezuela. Genet. Resour. Crop Evol. doi:10.1007/s10722-011-9709-2.
Bonisch, M., Herden, T., Nachtigall, M., Friesen, N., Zander, M., and Frese, L. (2015). Establishment of Genetic Reserves for Crop Wild Relatives. poster. doi:10.13140/RG.2.2.15771.67363.
Bossdorf, O., Auge, H., Lafuma, L., Rogers, W. E., Siemann, E., and Prati, D. (2005). Phenotypic and genetic differentiation between native and introduced plant populations. Oecologia 144, 1-11. doi:10.1007/s00442-005-0070-z.
Brown, A. H. D., and Briggs, J. D. (1991). “Sampling strategies for genetic variation in ex situ collectoins of endagered plant species,” in Genetics and conservation of rare plants, eds. D. A. I. Falk and K. E. Holsinger (New York; Oxford: Oxford University Press), 99-119.
Brown, A. H. D., and Marshall, D. R. (1995). “A basic sampling strategy: theory and practice,” in Collectingplant genetic diversity: Technical guidelines, eds. L. Guarino, R. V Ramanantha, and R. Reid (Wallingford, UK: CAB International), 75-91.
Castañeda-Álvarez, N. P., Khoury, C. K., Achicanoy, H. A., Bernau, V., Dempewolf, H., Eastwood, R. J., et al. (2016). Global conservation priorities for crop wild relatives. Nat. Plants 2, 1-6. doi:https://doi.org/10.1038/nplants.2016.22.
Chukhina, I., Shipilina, L., Bagmet, L., Talovina, G., and Smekalova, T. (2020). Results of studying wild relatives of the cultivated plants of Russia. Biol. Commun. 65, 41-52. doi:https://doi.org/10.21638/spbu03.2020.104.
Ciancaleoni, S., Raggi, L., Barone, G., Donnini, D., Gigante, D., Domina, G., et al. (2021). A new list and prioritization of wild plants of socioeconomic interest in Italy: toward a conservation strategy. Agroecol. Sustain. Food fyst. doi:https://doi.org/10.1080/21683565.2021.1917469.
Contreras-Toledo, A. R., Cortés-Cruz, M. A., Costich, D., Rico-Arce, M. L., Magos Brehm, J., and Maxted, N. (2018). A crop wild relative inventory for Mexico. Crop Sci. 58, 1292-1305. doi:10.2135/cropsci2017.07.0452.
Contreras-Toledo, A. R., Cortés-Cruz, M., Costich, D. E., Rico-Arce, M. D. L., Magos Brehm, J., and Maxted, N. (2019). Diversity and conservation priorities of crop wild relatives in Mexico. Plant Genet. Resour. Characterisation Util. 17, 140150. doi:10.1017/S1479262118000540.
Corinto, G. L. (2014). Nikolai Vavilov ’ s Centers of Origin of Cultivated Plants With a View to Conserving Agricultural Biodiversity. Hum. Evol. 29, 1-17.
Di Santo, L. N., and Hamilton, J. A. (2020). Using environmental and geographic data to optimize ex situ collections and preseve evolutionary potential. Conserv. Biol. 35, 733-744. doi:10.1111/cobi13568.
Dulloo, M. E., Labokas, J., Iriondo, J. M., Maxted, N., Lane, E., Laguna, E., et al. (2008). “Genetic Reserve Location and Design,” in Conserving Plant Genetic Diversity in Protected Areas. Population Management of Crop Wild Relatives, eds. J. M. Iriondo, N. Maxted, and M. E. Dulloo (Oxfordshire, UK), 23-64.
Endresen, D. T. F., Street, K., Mackay, M., Bari, A., and de Pauw, E. (2011). Predictive association between biotic stress traits and eco-geographic data for wheat and barley landraces. Crop Sci. 51, 2036-2055. doi:10.2135/cropsci2010.12.0717.
Falconer, D. S. (1952). The problem of environment and selection. Am. Nat. LXXXVI, 293-298.
Fielder, H., Brotherton, P., Hosking, J., Hopkins, J. J., Ford-Lloyd, B., and Maxted, N. (2015a). Enhancing the Conservation of Crop Wild Relatives in England. PLoS One 10, e0130804. doi:10.1371/journal.pone.0130804.
Fielder, H., Smith, C., Ford-Lloyd, B., and Maxted, N. (2015b). Enhancing the conservation of crop wild relatives in Scotland. J. Nat. Conserv. 29, 51-61. doi:10.1016/j.jnc.2015.11.002.
Fitzgerald, H. (2013). The National Crop Wild Relative Strategy Report for Finland.
Foster Huenneke, L. (1991). “Ecological Implications of Genetic Variation in Plant Populations,” in Genetic and Conservation of Rare Plants, eds. D. A. I. Falk and K. E. Holsinger (New York; Oxford: Oxford University Press), 31-44.
Frese, L., Bülow, L., Castro, S., Duarte, M. C., Iriondo, J. M., Lohwasser, U., et al. (2017). ECPGR Activity Grant Scheme - First Call, 2014 Final Activity Report: Genetic diversity of Patellifolia species (GeDiPa).
Garcia, R. M., Parra-Quijano, M., and Iriondo, J. M. (2017). Identification of ecogeographical gaps in the Spanish Aegilops collections with potential tolerance to drought and salinity. PeerJ 2017. doi:10.7717/peerj.3494.
García, R. M., Parra-Quijano, M., and Iriondo, J. M. (2017). A multispecies collecting strategy for crop wild relatives based on complementary areas with a high density of ecogeographical gaps. Crop Sci. 57, 1059-1069. doi:10.2135/cropsci2016.10.0860.
García Sánchez, R. M. (2020). Conservation of plant genetic resources: a spatial and ecogeographical approach. PhD thesis.
García Sánchez, R. M., Parra-Quijano, M., Greene, S., and Iriondo, J. M. (2019). Predictive characterisation identifies global sources of acyanogenic germplasm of a key forage species. Crop Pasture Sci. 70, 546-554.
González-Orozco, C. E., Sosa, C. C., Thornhill, A. H., and Laffan, S. W. (2021). Phylogenetic diversity and conservation of crop wild relatives in Colombia. Evol. Appl. 14, 2603-2617. doi:10.1111/eva.13295.
González Campos, J. M. (2019). Diversidad genética neutral y adaptativa, una simple explicación. Cienc. Investig. For. 25, 8198. doi:10.52904/0718-4646.2019.512.
Hunter, D., Guarino, L., Khoury, C. K., and Dempewolf, H. (2012). “A community divided: Lessons from the conservation of crop wild relatives around the world,” in Agrobiodiversity Conservation: Securing the diversity of crop wild relatives and landraces2, eds. N. Maxted, M. E. Dulloo, B. V. Ford-Lloyd, L. Frese, J. M. Iriondo, and M. A. A. Pinheiro de Carvalho (Wallingford, Oxfordshire, UK: CAB International), 298-304.
Idohou, R., Assogbadjo, A. E., Fandohan, B., Gouwakinnou, G. N., Glele Kakai, R. L., Sinsin, B., et al. (2013). National inventory and prioritization of crop wild relatives: Case study for Benin. Genet. Resour. Crop Evol. 60, 1337-1352. doi:https://doi.org/10.1007/s10722-012-9923-6.
Iriondo, J. M., Magos-Brehm, J., Dulloo, M. E., and Maxted, N. eds. (2021). Crop Wild Relative Population Management Guidelines. Farmer’s Pride: Networking, partnerships and tools to enhance in situ conservation of European plant genetic resources. Available at: https://more.bham.ac.uk/farmerspride/wp-content/uploads/sites/19/2021/07/Crop_Wild_Relative_Population_Management_Guideli.
Iriondo, J. M., Maxted, N., Kell, S. P., Ford-Lloyd, B. V., Lara-Romero, C., Labokas, J., et al. (2012). “Quality standards for genetic reserve conservation of crop wild relatives,” in Agrobiodiversity Conservation: Securing the diversity of crop wild relatives and landraces, eds. N. Maxted, M. E. Dulloo, B. V. Ford-Lloyd, L. Frese, J. M. Iriondo, and M. A. A. Pinheiro de Carvalho (Oxfordshire, UK: CAB International), 72-77.
Kell, S. P., Knupffer, H., Jury, S. L., Ford-Lloyd, B. V., and Maxted, N. (2007). “Crops and wild relatives of the Euro-Mediterranean region: making and using a conservation catalogue,” in Crop Wild Relative Conservation and Use, eds. N. Maxted, B. V. Ford-Lloyd, S. P. Kell, J. M. Iriondo, M. E. Dulloo, and J. Turok (CAB International), 69-109. Available at: http://centaur.reading.ac.uk/10030/.
Kell, S., Qin, H., Chen, B., Ford-Lloyd, B., Wei, W., Kang, D., et al. (2015). China’s crop wild relatives: Diversity for agriculture and food security. Agric. Ecosyst. Environ. 209, 138-154. doi:10.1016/j.agee.2015.02.012.
Khazaei, H., Street, K., Bari, A., Mackay, M., and Stoddard, F. L. (2013). The FIGS (focused identification of germplasm strategy) approach identifies traits related to drought adaptation in Vicia faba genetic resources. PLoS One 8, e63107. doi:10.1371/journal.pone.0063107.
Khoury, C. K., Greene, S., Wiersema, J., Maxted, N., Jarvis, A., and Struik, P. C. (2013). An inventory of crop wild relatives of the United States. Crop Sci. 53, 1496-1508. doi:https://doi.org/10.2135/cropsci2012.10.0585.
Mackay, M. C., and Street, K. (2004). Focused identification of germplasm strategy – FIGS. in Proceedings of the 54th Australian Cereal Chemistry Conference and the 11th Wheat Breeders’ Assembly. (Melbourne: Royal Australian Chemical Institute), 138141.
Magos-Brehm, J., Maxed, N., Martins-Loução, M. A., and Ford-Lloyd, B. V. (2010). New approaches for establishing conservation priorities for socioeconomically important plant species. Biodivers. Conserv. 19, 2715-2740. doi:https://doi.org/10.1007/s10531-010-9871-4.
Magos Brehm, J., Kell, S., Thormann, I., Gaisberger, H., Dulloo, E., and Maxted, N. (2013). INTERACTIVE TOOLKIT FOR CROP WILD RELATIVE CONSERVATION PLANNING version 1.0. Resource Book for the Preparation of National Plans of Crop Wild Relatives and Landraces. Food and Agriculture Organization of the In Situ Conservation and Use of Crop Wild Rela.
Magos Brehm, J., Maxted, N., Ford-Lloyd, B. V., and Martins-Lou9ao, M. A. (2008). National inventories of crop wild relatives and wild harvested plants: Case-study for Portugal. Genet. Resour. Crop Evol. 55, 779-796. doi:https://doi.org/10.1007/s10722-007-9283-9.
Maxted, N., Avagyan, A., Frese, L., Iriondo, J., Brehm, J. M., Singer, A., et al. (2015). ECPGR Concept for in situ conservation of crop wild relatives in Europe. Wild Species Conservation in Genetic Reserves Working Group. European Cooperative Programme for Plant Genetic Resources. Rome, Italy. Available at: www.ecpgr.cgiar.org/fileadmin/temp. 21. Available at: www.ecpgr.cgiar.org/fileadmin/templates/ecpgr.org/upload/WG_UPLOADS_PHASE_IX/WILD_SPECIES/%0AConcept_for_in__situ_conservation_of_CWR_in_Europe.pdf%0A.
Maxted, N., Hawkes, J. G., Ford-Lloyd, B. V., and Williams, J. T. (1997). “A practical model for in situ genetic conservation,” in Plant Genetic Conservation: The In Situ Approach, eds. N. Maxted, B. V. Ford-Lloyd, and J. G. Hawkes (Dordrecht, The Netherlands: Kluwer Academic Publishers), 339-367.
Maxted, N., Iriondo, J. M., de Hond, L., Dulloo, M. E., Lefevre, F., Asdal, A., et al. (2008). Genetic reserve management. Conserv. plant Genet. Divers. Prot. areas, 65-78.
Maxted, N., Kell, S., and Brehm, J. M. (2011). Options to Promote Food Security: On-Farm Management and In Situ Conservation of Plant Genetic Resources for Food and Agriculture. Commission Genet. Resour. Food Agric., 25. Available at: http://www.fao.org/docrep/meeting/022/am489e.pdf.
Maxted, N., Scholten, M., Codd, R., and Ford-Lloyd, B. (2007). Creation and use of a national inventory of crop wild relatives. Biol. Conserv. doi:https://doi.org/10.1016/j.biocon.2007.08.006.
MeiUeur, B. a., and Hodgkin, T. (2004). In situ conservation of crop wild relatives: Status and trends. Biodivers. Conserv. 13, 663-684. doi:https://doi.org/10.1023/B:BIOC.0000011719.03230.17.
Molina Pertíñez, A., Torres Lamas, E., Rubio Teso, M. L., Álvarez-Muñiz, C., de la Rosa, L., Tardío Pato, J., et al. Estrategia Nacional de Conservación y Utilización de Parientes Silvestres de los Cultivos (PSC) y Plantas Silvestres de Uso Alimentario (PSUA). 114 pp.
Mwila, G., Gaisberger, H., International, B., Brehm, J. M., and Kell, S. (2019). Spatial analyses of occurrence data of crop wild relatives (CWR) taxa as tools for selection of sites for conservation of priority CWR in Zambia. Plant Genet. Resour., 1-12. doi:https://doi.org/10.1017/S1479262118000497.
Parra-Quijano, M., Iriondo, J. M., and Torres, E. (2012a). Improving representativeness of genebank collections through species distribution models, gap analysis and ecogeographical maps. Biodivers. Conserv. 21, 79-96. doi:https://doi.org/10.1007/s10531-011-0167-0.
Parra-Quijano, M., Iriondo, J. M., and Torres, E. (2012b). Review. Applications of ecogeography and geographic information systems in conservation and utilization of plant genetic resources. Spanish J. Agric. Res. 10, 419-429. doi: https://doi.org/10.5424/sjar/2012102-303-11.
Parra-Quijano, M., Iriondo, J. M., Torres, M. E., López, F., Maxted, N., and Kell, S. (2020). CAPFITOGEN 3. Una caja de herramientas para la conservación y promoción del uso de la biodiversidad agrícola. Manual de usuario. 1-5. Available at: http://www.etitudela.com/entrenadorcomunicaciones/downloads/gsmmanualsmsconfiguratorl.pdf.
Phillips, J., Asdal, A., Magos Brehm, J., Rasmussen, M., and Maxted, N. (2016). In situ and ex situ diversity analysis of priority crop wild relatives in Norway. Divers. Distrib. 22, 1112-1126. doi:https://doi.org/10.1111/ddi.12470.
Phillips, J., Kyratzis, A., Christoudoulou, C., Kell, S., and Maxted, N. (2014). Development of a national crop wild relative conservation strategy for Cyprus. Genet. Resour. Crop Evol. 61, 817-827. doi:https://doi.org/10.1007/s10722-013-0076-z.
Rebelo, A. G. (1994). “Iterative selection procedures: Centres of endemism and optimal placement of reserves,” in Botanica/ Diversity in Southern Africa, ed. B. J. Huntley (Pretoria: National Botanical Institute), 231-257.
Reeves, P. A., and Richards, C. M. (2018). Biases induced by using geography and environment to guide ex situ conservation. Conserv. Genet. 19, 1281-1293. doi:https://doi.org/10.1007/s10592-018-1098-z.
Ronquillo, C., Alves-Martins, F., Mazimpaka, V., Sobral-Souza, T., Vilela-Silva, B., Medina, N. G., et al. (2020). Assessing spatial and temporal biases and gaps in the publicly available distributional information of Iberian mosses. Biodivers. Data J. 8. doi:https://doi.org/10.3897/BDJ.8.E53474.
Rubio Teso, M. L., Álvarez-Muñiz, C., Gaisberger, H., Kell, S. P., Lara-Romero, C., Magos Brehm, J., et al. (2021). European crop wild relative diversity: towards the development of a complementary conservation strategy. 100.
Rubio Teso, M. L., Álvarez-Muñiz, C., Raggi, L., Negri, V., García, R., Parra-Quijano, M., et al. (2020). Farmer’s Pride: Identifying in situ areas with useful adaptive traits.
Rubio Teso, M. L., Iriondo, J. M., Parra-Quijano, M., and Torres, E. (2013). Report for National Strategy for the Conservation of Crop Wild Relatives of Spain.
Smekalova, T. N. (2008). “National Crop Wild Relative In Situ conservation Strategy for Russia,” in Crop Wild Relative Conservation and Use, eds. N. Maxted, B. V. Ford-Lloyd, S. P. Kell, J. M. Iriondo, M. E. Dulloo, and J. Turok (Oxfordshire, UK: CAB International), 143-151.
Tas, N., West, G., Kircalioglu, G., Topaloglu, S. B., Phillips, J., Kell, S., et al. (2019). Conservation gap analysis of crop wild relatives in Turkey. Plant Genet. Resour. Characterisation Util. 17, 164-173. doi:https://doi.org/10.1017/S1479262118000564.
Taylor, N. G., Kell, S. P., Holubec, V., Parra-Quijano, M., Chobot, K., and Maxted, N. (2017). A systematic conservation strategy for crop wild relatives in the Czech Republic. Divers. Distrib., 1-15. doi:https://doi.org/10.1111/ddi.12539.
Thormann, I., Parra-Quijano, M., Endresen, D. T. F., Rubio-Teso, M. L., Iriondo, J. M., and Maxted, N. (2014a). Predictive characterization of crop wild relatives and landraces. Bioversiy Int, 40.
Thormann, I., Parra-Quijano, M., Iriondo, J. M., Rubio-Teso, M. L., Endresen, D. T. F., Dias, S., et al. (2014b). New predictive characterization methods for accessing and using CWR diversity. in International Conference on ENHANCED GENEPOOL UTILIZATION - Capturing wild relative and landrace diversityfor crop improvement, Cambridge, United Kingdom, 16-20 June 2014. Book of Abstracts.
Thormann, I., Parra-Quijano, M., Rubio Teso, M. L., Endresen, D. T. F., Dias, S., Iriondo, J. M., et al. (2016a). “Predictive Characterization Methods for Accessing and Using CWR Diversity,” in Enhancing Crop Genepool Use: Capturing Wild Relative and Landrace Diversity for Crop Improvement, eds. N. Maxted, M. E. Dulloo, and B. Ford-Loyd (CAB International), 64-77.
Thormann, I., Reeves, P., Reilley, A., Engels, J. M. M., Lohwasser, U., B??rner, A., et al. (2016b). Geography of genetic structure in barley wild relative Hordeum vulgare subsp. Spontaneum in Jordan. PLoS One 11, 1-19. doi:https://doi.org/10.1371/journal.pone.0160745.
Troudet, J., Grandcolas, P., Blin, A., Vignes-Lebbe, R., and Legendre, F. (2017). Taxonomic bias in biodiversity data and societal preferences. Sci. Rep. 7, 1-14. doi:https://doi.org/10.1038/s41598-017-09084-6.
van Treuren, R., Hoekstra, R., and van Hintum, T. J. L. (2017). Inventory and prioritization for the conservation of crop wild relatives in The Netherlands under climate change. Biol. Conserv. 216, 123-139. doi:https://doi.org/10.1016/j.biocon.2017.10.003.
Vincent, H., Amri, A., Castañeda-Álvarez, N. P., Dempewolf, H., Dulloo, E., Guarino, L., et al. (2019). Modeling of crop wild relative species identifies areas globally for in situ conservation. Commun. Biol. 2, 136. doi:https://doi.org/10.1038/s42003-019-0372-z.
Weibull, J., and Phillips, J. (2020). Swedish Crop Wild Relatives : towards a national strategy for in situ conservation of CWR. Genet. Resour. 1, 17-23. doi:https://doi.org/10.46265/genresj.2020.1.17-23.
Whitlock, R., Hipperson, H., Thompson, D. B. A., Butlin, R. K., and Burke, T. (2016). Consequences of in-situ strategies for the conservation of plant genetic diversity. Biol. Conserv. 203, 134-142. doi:https://doi.org/10.1016/j.biocon.2016.08.006.