Received: 15 May 2023 Accepted: 3 November 2023 DOI: 10.1002/csc2.21143 Crop Science O R I G I N A L A R T I C L E P l a n t G e n e t i c R e s o u r c e s Wild relatives of potato (Solanum L. sec. Petota) poorly sampled and unprotected in Colombia Carlos E. González-Orozco1 Paula H. Reyes-Herrera2 Chrystian C. Sosa3,4 Rosa T. Torres2 Norma C. Manrique-Carpintero5 Zahara Lasso-Paredes2 Ivania Cerón-Souza2 Roxana Yockteng2,6 1Corporación Colombiana de Investigación Agropecuaria- Agrosavia, Centro de Investigación La Libertad- Km 14 vía Villavicencio-Puerto López, Meta, Colombia 2Corporación Colombiana de Investigación Agropecuaria – Agrosavia, Centro de Investigación Tibaitatá, Bogotá, Colombia 3iOMICAS Research Institute, Pontificia Universidad Javeriana, Cali, Colombia 4Grupo de Investigación en Evolución, Ecología y Conservación EECO, Programa de Biología, Facultad de Ciencias Básicas y Tecnologías, Universidad del Quindío, Armenia, Colombia 5Bioversity-Ciat, International Center for Tropical Agriculture (CIAT), Cali, Colombia 6Muséum National d’Histoire Naturelle, UMR-CNRS 7205, Paris, France Correspondence Carlos E. Gonzalez-Orozco, Corporación Abstract Colombiana de Investigación Agropecuaria- Wild potato relatives (Solanum L. sec. Petota) play a vital role in crop improvement, Agrosavia. Centro de Investigación La Libertad- Km 14 vía Villavicencio-Puerto understanding crop evolution, and conserving potato diversity. However, these López, Meta, Colombia. invaluable resources are often neglected and underutilized and are susceptible to Email: cegonzalez@agrosavia.co threats such as climate change, urbanization, and agricultural expansion. Little is Assigned to Associate Editor Laura known about the diversity, conservation status, and distribution of wild potato species Shannon. in Colombia. To address this gap, we assessed the conservation status of five wild potato relatives conserved in the ex situ Colombian Central Collection. Five species Funding information Corporación Colombiana de Investigación were analyzed for their spatial patterns of biodiversity, conservation status, and con- Agropecuaria-Agrosavia, Grant/Award servation gaps. Colombia was found to have six centers of species richness, four Number: 1002442 areas of endemism, and six biogeographical regions. Of the five native species, only one was classified as adequately conserved for ex situ conservation, while the other four were considered low priority. In contrast, for in situ conservation, three species showed high priority, one was classified as medium priority, and one as low Abbreviations: ABZ, agrobiodiversity zones; AGROSAVIA, The Colombian Agricultural Research Corporation; BGVAA, Colombian Plant Germplasm Bank for Food and Agriculture; BIEN, Botanical Information and Ecology Network; CCC, Colombian Central Collection; CE, centers of endemism; CGIAR, Consultative Group of International Agricultural Research; CWE, corrected weighted endemism; CWR, crop wild relatives; ERS, ecological score; FCS, final conservation score; FCSex, final conservation score of ex situ conservation; FCSin, final conservation score of in situ conservation; GRex-in, geographic representativeness score; m.a.s.l., meters above sea level; MaxEnt, maximum entropy; MTSPS, maximum training sensitivity plus specificity; SDM, species distribution models; SRSex-in, sampling representativeness score; WE, weighted endemism; ZRC, Peasant Reserve Zones or Zonas de Reserva Campesina in Spanish. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. © 2023 The Authors. Crop Science published by Wiley Periodicals LLC on behalf of Crop Science Society of America. Crop Science. 2023;1–19. wileyonlinelibrary.com/journal/csc2 1 2 Crop Science GONZÁLEZ-OROZCO ET AL. priority. In light of these findings, we propose three conservation strategies: (1) con- ducting collection missions to increase accessions in the national germplasm bank, prioritizing high-priority species; (2) identifying and protecting unprotected natural habitats and engaging stakeholders to enhance in situ conservation efforts; and (3) establishing regional community genebanks to ensure localized conservation efforts. 1 INTRODUCTION resulting in 186 and 107 tuber-bearing species in the Petota section, respectively. The wild relatives of potatoes play a vital role as a rich source The distribution of environments and the geographic range of biodiversity. Potato (Solanum tuberosum L.) is a global of potato CWR are broader than those of cultivated potatoes. staple crop, ranking fourth in food consumption after rice, According to Hawkes (1988, 1990), potato CWR originated wheat, and maize (Devaux et al., 2020). Conservation of the in Mexico and spread to South America, serving as a main biodiversity of potato crop wild relatives (CWR) is currently center of diversity. According to Hijmans et al. (2002), most a priority (Castañeda-Alvarez et al., 2015; Sotomayor et al., species are concentrated in the Andes region of South Amer- 2023). Potato CWR thrive in diverse and harsh environments, ica, while the highlands of Central America constitute a which makes them valuable sources of naturally evolving secondary center of speciation. Peru has the greatest num- adaptations (Dempewolf et al., 2017). Anthropogenic fac- ber of potato CWR (91), followed by Bolivia and Mexico (36 tors such as urbanization, agricultural expansion, and climate species each). In contrast, Colombia has 11 species, seven of change threaten CWR habitats (Jarvis et al., 2008; Maxted which are endemic or rare. Because of the adjustments in the et al., 2006). Approximately 65% of Colombian ecosystems taxonomic classification, the 11 species reported by Hijmans are threatened (Ayram et al., 2020). The primary culprits are et al. (2002) currently correspond to five species according to the expansion of agricultural and livestock frontiers and land Spooner et al. (2014) (Table S1). The potato CWR species use changes (Ayram et al., 2020; Baptiste et al., 2017; Boron can be found in various habitats ranging from sea level to et al., 2016). Considering the importance of CWR and the 4500 m, including high-altitude Andean grasslands, puna, imminent risk of species loss, it is crucial to prioritize their and paramo ecosystems. Most species are distributed between conservation. Potato CWR merit further research to ensure 2000 and 4000 m and in regions with mean annual temper- their long-term survival and preserve species diversity. atures between 12.7 and 14.1˚C. All species are terrestrial, Furthermore, potato CWR display remarkable diversity, except for Solanum morelliforme Bitter & G. Muench and encompassing over 100 wild tuber-bearing species accord- Solanum clarum Correll., which are epiphytes. Many potato ing to the latest taxonomic classification (Spooner et al., CWR exhibit morphological similarities to cultivated pota- 2014; Spooner et al., 2004). Cultivated potatoes (S. tubero- toes, as tubers grow from stolons (underground stems) that sum L.) and their CWR belong to the section Petota of can reach lengths of a meter or longer. Although most species the Solanum genus within the Solanaceae family (Hardi- are diploids, their ploidy levels can range from 2x to 6x, with gan et al., 2015; Peralta et al., 2021). Various taxonomists 10 species exhibiting several ploidy levels. have influenced the classification of wild potatoes, leading Potato CWR hold great promise as a valuable source of to the worldwide adoption of different taxonomic classifi- traits to address pest and disease problems and new crop- cations. Hawkes (1990) developed the most comprehensive ping conditions resulting from climate change. Species such and widely used taxonomic classification based on mor- as Solanum acaule Bitter., Solanum bulbocastanum Dunal., phological descriptions and interspecific hybridization. This Solanum chacoense Bitter., Solanum demissum Lindl., and classification identified 228 wild potato species, categorized Solanum stoloniferum Schltdl. & Bouchet. have shown resis- into 21 series, with 19 tuber-bearing and two non-tuberous tance to frost and late blight [Phytophthora infestans (Mont.) series (Etuberosa and Juglandifolia). Spooner and Hijmans de Bary] (Jones et al., 2014; Liu & Halterman, 2009; Mattheij (2001) revised this classification, reducing the number of et al., 1992; Smyda et al., 2013; Van der Vossen et al., wild tuber-bearing species to 196 within the Petota section 2003). Additionally, Solanum commersonii and Solanum while reclassifying the non-tuber-bearing species under the berthaultii have demonstrated resistance to bacterial wilt Etuberosum section. Subsequent revisions by Spooner and (Ralstonia solanacearum) and verticillium wilt (Verticillium Salas (2006) and Spooner et al. (2014) further reduced the spp.) (González et al., 2013; Laferriere et al., 1999). The frost number of species based on phylogenetic analysis supported tolerance of Solanum boliviense has been reported (Hawkes by field expeditions and molecular and morphological studies, et al., 2000). Hijmans et al. (2003) and Tucci et al. (1996) also 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GONZÁLEZ-OROZCO ET AL. Crop Science 3 found frost resistance in S. acaule, Solanum albicans (Ochoa) Ochoa., and S. commersonii. Furthermore, a recent study Core Ideas identified species with remarkable adaptability to different environments, highlighting the adaptability of S. colom- ∙ Biodiversity patterns of wild potato species and bianum Bitter. to high temperatures (Fumia et al., 2022). In the their conservation status in Colombia have been face of changing environmental conditions, these potato CWR documented. offer potential solutions to challenges in potato agriculture, ∙ The wild relatives of potato species in Colom- contributing to crop resilience and sustainability. Preserving bia have been insufficiently sampled and remain and utilizing the genetic diversity present in wild potato rel- unprotected. atives are essential for sustaining crop improvement efforts. ∙ Herbarium and genebanks historical data play This genetic diversity can help ensure the long-term resilience critical roles in conserving wild potato relatives. of potato cultivation in the face of changing environmental ∙ Insights for the ex situ and in situ conservation of conditions and emerging challenges. wild potato relatives in Colombia are proposed. Currently, 89 institutions worldwide are engaged in the ex ∙ By utilizing historical data from genebanks, we situ conservation of potato accessions, including four inter- recommended the inclusion of indigenous and national and regional centers in 59 countries, resulting in agrobiodiversity zones. 82,293 accessions (Nagel et al., 2022). These collections were obtained from numerous expeditions to acquire landraces and wild species from Latin America between 1930 and 2020. 2 MATERIALS AND METHODS Most of the accessions consisted of breeding lines (27%), fol- lowed by landraces (23%), improved varieties (25%), and wild 2.1 Wild potato species from Colombia species (20%) (Nagel et al., 2022). In Colombia, the ex situ potato collection, known as Based on the CCC passport data and previous reports the Colombian Central Collection (CCC), is one of 275 (Castañeda-Álvarez et al., 2015; Hijmans et al., 2002; Spooner collections conserved by the Colombian Plant Germplasm et al., 2014), five potato CWR were selected to explore the Bank for Food and Agriculture (BGVAA Spanish acronym biodiversity patterns, conservation gaps, and status of potato of Banco de Germoplasma Vegetal para Alimentación y CWR in Colombia (herbarium samples in Figure 1). From Agricultura) (Cerón-Souza et al., 2023). The responsibility the five species collected in Colombia, two have a distri- for maintaining the BGVAA lies with AGROSAVIA (The bution in the country and neighboring countries (Solanum Colombian Agricultural Research Corporation, in Spanish andreanum Baker. and S. colombianum), and three potato Corporación Colombiana de Investigación Agropecuaria). CWR are endemic (i.e., exclusively distributed) in Colom- The CCC conserves 2504 active ex situ accessions using bia (Solanum flahaultii Bitter. and Solanum garcia-barrigae different conservation systems: field, seed, and in vitro. Ochoa., and Solanum lobbianum Bitter.). According to the taxonomy of Spooner et al. (2014), 89% of Each of the five selected species from the CCC has between the accessions conserved in the CCC correspond to cultivated one and 68 accessions collected in Colombia for a total of species conserved clonally, and 7% (n = 15) correspond to 105 accessions (Table 1; Figure S2). The accessions were potato CWR, conserved as seeds. collected throughout Colombia between 1947 and 1984 but In this study, we address two key questions, focusing on five lacked georeferenced coordinates. To overcome this limita- potato CWR conserved in the CCC that have accessions col- tion, we manually curated the collection books to approximate lected within Colombia: (1) What is the conservation status of geographic coordinates. The CCC also conserves accessions the five potato CWR conserved in the CCC? (2) Where are the from another 10 potato CWR that are not distributed in observed and potential centers of diversity of the five potato Colombia, which correspond to introductions from differ- CWR that could be designated priority sites for conservation ent countries of origin, probably for plant breeding purposes and collection in Colombia? (Table S2). In the process of curating passport coordinates, Based on our findings, we suggest priorities for future we obtained occurrence data for 56 accessions from four research and ex situ and in situ conservation strategies species, 53 of them were collected in Colombia (see map of to safeguard these invaluable potato CWR. These propos- distributions in Figure S1; Supporting Information Data S1). als are intended to guide stakeholders and researchers in The species in the CCC use the taxonomy defined by the protection and conservation of important potato genetic Hawkes (1990), which we updated according to Spooner et al. resources. (2014), to maintain consistency with the latest classification. 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 4 Crop Science GONZÁLEZ-OROZCO ET AL. F I G U R E 1 Herbarium samples of five potato crop wild relatives collected in Colombia and used in this study. The collectors of these samples were L. Lopez, E. Zerda, M. Umaña, A. Forero, O. Montealegre, L. Orozco, and C. Araque. Sample details are as follows: (a) S. andreanum was collected in Nariño, Colombia, in 1980; (b) S. colombianum was collected in Huila, Colombia, in 1982; (c) S. flahualtii was collected in Santander, Colombia in 1981. S. garciacia-barrigae was collected in Norte de Santander, Colombia, in 1981; (d and e) S. lobbianum was collected in Caldas, Colombia, in 1980. Table 1 shows a summary of the five species studied: sea level (m.a.s.l.) in the Sierra Nevada de Santa Marta at the taxonomic classification based on Hawkes (1990) and Pico Bolivar. With its wide range of elevations and the pres- Spooner et al. (2014), the genepool classification (primary or ence of the three Andean mountain ranges, Colombia stands secondary), the number of accessions in the CCC, and spa- out as one of the most remarkable and diverse countries in tial occurrence information obtained from both open-access South America and globally. It possesses major biodiversity databases and CCC passport data. Genepool classification hotspots, including the northwestern part of the Amazon and indicates the ability of wild species to interbreed with cul- the Chocó biogeographic regions (Pérez-Escobar et al., 2022). tivated species (Harlan & de Wet, 1971; Maxted et al., 2006). 2.3 Analyses to diagnose the conservation status of wild potato in Colombia 2.2 Study region We conducted a thorough search for occurrences of five Colombia is part of the Neotropical region known as the species in the passport data from accessions in the CCC of the Northern Andes (Morrone, 2014). According to a biogeo- BGVAA genebank and open-source biodiversity repositories graphical classification by González-Orozco (2021), Colom- (Supporting Information Data S1). With this information, we bia is divided into the Pacific and Boreal Brazilian dominions performed species distribution modelling and a gap analysis to and six provinces named Chocó-Darién, Guajira, Magdalena, identify conservation gaps. The findings from these analyses Páramo-Andes, Sabana-Orinoquía and Imerí-Amazonas. Ele- were then used to propose both in situ and ex situ conservation vations in Colombia range from sea level to 5560 m above strategies (Figure 2). 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GONZÁLEZ-OROZCO ET AL. Crop Science 5 T A B L E 1 List of five wild potato species with geographic distribution in Colombia selected for this study. The table contains the taxonomic classification based on Spooner et al. (2014) and Hawkes (1990), the genepool classification, the ploidy reported by Hijmans et al. (2007), native distributions based on POWO (2023), spatial occurrence information obtained from both open-access databases and in the Colombian Central Collection (CCC) passport data, and the number of accessions in the CCC. Species name No. of spatial No. of spatial according to CCC species name occurrences from occurrences in No. of Spooner et al.’s according to Hawkes’ Potato Native open-access the CCC accessions in (2014) classification (1990) classification genepool Ploidy distribution databases passports the CCC S. andreanum Baker S. andreanum Baker Secondary 2x, 4x Colombia, 110 3 11 S. tuquerrence Hawkes Ecuador S. colombianum S. colombianum Dunal Secondary 4x Colombia, 460 36 68 Dunal S. colombianum Ecuador, Peru, Dunal var. Venezuela guambianum S. colombianum Dunal var. Pubescens S. colombianum var. trianae Bitter S. moscopanum Hawkes S. flahaultii Bitter S. flahaultii Bitter Secondary 4x Colombia 112 13 21 S. garcia-barrigae S. garcia-barrigae Secondary 4x Colombia 5 0 1 Ochoa Ochoa S. lobbianum Bitter S. lobbianum Bitter Secondary 4x Colombia 7 0 4 Total 694 52 105 2.4 Geographic information as defined by Crisp et al. (2001). We then calculated the cor- rected weighted endemism (CWE) metric, which is a measure We compiled 870 species occurrences from various open of the relative endemism that accounts for range restriction, as sources, of which 835 species records were obtained from defined by Laffan et al. (2010, 2013). CWE assesses the extent the Botanical Information and Ecology Network (BIEN) to which species ranges within a grid cell are, on average, version 4.1 database. The records, which included standard- predominantly restricted to that specific cell. ized plant observations derived from herbarium specimens, were extracted using the RBIEN package (Maitner et al., 2018). Additionally, 15 records were sourced from the Virtual 2.6 Biogeographic regions Herbarium of the National University of Colombia, 14 from the Missouri Botanical Garden Herbarium online dataset, and To determine the biogeographic regions of the five wild two from the New York Botanical Garden online herbar- potato species collected in Colombia, we employed the range- ium dataset. Furthermore, we extracted four records from the weighted turnover approach developed by Laffan et al. (2016), supplementary material reported by Castañeda-Álvarez et al. which applied a dissimilarity matrix and agglomerative clus- (2015). After applying a spatial cleaning process, we used 694 tering methods. For the agglomerative cluster analysis, we species occurrences in our study, out of the initial 870 records used a pairwise distance matrix and generated a weighted pair (see distributions of native species in Figure 3; Supporting group of hierarchical clusters using arithmetic averages in the Information Data S2). This process involved using only those BIODIVERSE software. These methods to accurately identify records that contained spatial coordinates. and define the biogeographic region were tested in previous studies by Gonzalez-Orozco et al. (2013), Gonzalez-Orozco, Thornhill, et al. (2014), and Gonzalez-Orozco, Ebach, et al. 2.5 Species richness and endemism (2014). The cluster analysis results are presented in a biogeograph- We used the BIODIVERSE software version 0.18 to calcu- ical region map and a dendrogram, illustrating the spatial late two biodiversity metrics for each 10 km × 10 km grid relationship of dissimilarities in species composition among cell. The first metric measured was species richness, which regions. To calculate the weighted endemism (WE), we uti- refers to the number of species present in a single grid cell, lized a portion of the range-weighted turnover calculation, 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 6 Crop Science GONZÁLEZ-OROZCO ET AL. F I G U R E 2 The workflow of geospatial analyses used to assess the conservation status of wild potato relatives in Colombia. The potato Central Collection of Colombia (CCC), crop wild relatives (CWR), area under de curve value (AUC), final score of ex situ conservation (FSCex), final score of in situ conservation (FSCin), final conservation score (FSC), high-priority conservation category (HP), and Potato Crop Wild Relatives (PCWR). specifically the range-weighted richness score. This score 2.7 Species distribution modeling considers the contribution of each taxon, which is propor- tional to the fraction of its range across a set of locations. The first step in conducting the gap analysis is to gener- The methods used in this calculation were based on studies ate species distribution models (SDM) for each species. To by Crisp et al. (2001), Laffan and Crisp (2003), and Laffan accomplish this, we applied the maximum entropy (MaxEnt) et al. (2013). algorithm (Phillips et al., 2006), which produced potential The range-weighted turnover metric quantifies the WE ecogeographic suitability models for the five species that shared between two locations. This dissimilarity metric were originally collected in Colombia and have geographic assigns values of zero when both sites have the same taxa and coordinates. values of one when shared taxa are absent. In the final step, To create the models, we set modeling parameters to their we transformed the distance endemism-weighted dissimilar- default values while randomly excluding 30% of the species ity matrix into clusters of dissimilar taxa proportional to their occurrences for testing purposes. To improve the predictabil- range. ity of each species, five replicates of the SDM were conducted 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GONZÁLEZ-OROZCO ET AL. Crop Science 7 3 km2. We acquired these digital maps from several sources, including Agrosavia (2014), Alzate-Velásquez (2017, 2018), and González-Orozco et al. (2020). To characterize the long-term climate, we considered a minimum of 30 years of climate data from weather stations managed by Colombia’s Institute of Environmental Studies. We labeled suitability values equal to or greater than the maximum training sensitivity plus specificity (MTSPS) logis- tic threshold as one, while values lower than MTSPS were labeled as zero, creating a binary classification required for input to gap analysis software. 2.8 Gap analysis An SDM was generated for the five species (S. andreanum, S. colombianum, S. flahaultii, S. garcia-barrigae, and S. lob- bianum). We then estimated eight metrics to analyze ex situ and in situ conservation systems, using the R package Gap- Analysis (Carver et al., 2021). The calculated indices included the sampling representativeness score (SRSex-in), geographic score (GRex-in), ecological score (ERSex-in), and final con- servation score (FCSex-in). We computed a combined metric known as the FCS-mean, which involves averaging the final ex situ FCSex and in situ FCSin scores. The final combined scores for each species were assigned to specific conservation status categories according to Khoury et al. (2019), which fit in a numeric range between 0 and 100: high priority for further conservation for species where FCS < 25, medium priority where 25 ≤ FCS < 50, low priority where 50 ≤ FCS < 75, and sufficiently conserved for taxa whose FCS ≥ 75. Furthermore, we conducted a predicted species richness analysis for all five species using the ex situ gap analysis. The analysis included summing the binary MaxEnt rasters of the SDM for the five modeled species to calculate the predicted species richness gap. F I G U R E 3 Distribution maps showing species occurrences for 3 RESULTS five species of potato wild relatives with reported geographic distribution in Colombia. 3.1 Species richness and sampling completeness to obtain an average model. A replicate refers to a set of iter- We identified six centers of species richness in Colombia, as ations or repetitions of the modeling process. The criteria to indicated by the labels SR1-6 in Figure 4b. Three of these cen- run the replicates were that their area under the curve values ters are in the middle of the country (SR1-3), while three are in were greater than 0.7. the south (SR3-6). The highest number of species, up to two, For the MaxEnt modeling, we used seven climate variables can be found in the highlands of Nariño, Tolima-Caldas, and that represent the average climatic conditions of Colombia Cundinamarca departments. Our sampling redundancy was from 1980 to 2010. These variables included mean annual 85% per grid cell in most of the Andean region (Figure 4a). precipitation, average temperature, minimum and maximum The most significant species richness hotspot was found in temperature, relative humidity, solar radiation, and wind the Nariño department, which hosts two species (S. colom- speed. The spatial resolution of the climate variable maps was bianum and S. andreanum). This area, known as the “Nudo de 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 8 Crop Science GONZÁLEZ-OROZCO ET AL. Park. While some species occur within a forest reserve called Los Bosques de la Chec, others fall outside of protected areas. The Cundinamarca department in the eastern mountain range is home to species such as S. colombianum and S. flahaultii. These species are found in the northern and cen- tral parts of Cundinamarca, encompassing the municipalities of Pacho, Zipaquira, Cogua, and Tausa. They are well rep- resented within Páramo de Guerrero, part of the protected areas. Other sites with high species richness are in paramo ecosys- tems near Santa Fe de Bogotá, the Colombian district capital, mostly close to the locality of Soacha. Additionally, some cen- ters of richness are scattered across various sites in the paramo ecosystems of Boyacá, Santander, and Norte de Santander departments. Regarding the geographic distribution of species, S. colom- bianum is widely distributed across the three mountain ranges. In contrast, S. lobbianum and S. garcia-barrigae have a nar- row distribution limited to specific mountain areas in the departments of Nariño, Cundinamarca, Boyacá, Bolivar, and Caldas. 3.2 Endemism Four centers of endemism were identified (Figure 4c). How- ever, the results of the randomization showed that three (CE1–E3) out of the four endemism centers (CE) were signif- icantly different from independently randomized samples at a threshold of α= 0.05 (Figure 4d). In the central region, the site shared between Risaralda and Caldas departments (CE3 in Figure 4c) was significantly different and exhibited the high- F I G U R E 4 Spatial patterns of biodiversity of potato crop wild est endemism per grid cell with a value of 0.33. Therefore, the relatives in Colombia. Map of sampling redundancy (a), observed species distribution range is restricted in this area, accounting species richness (b), observed species endemism (c), and endemism significance (d). SR refers to the main hotspots of species richness, and for 33% of its total range. Solanum garcia-barrigae is found CE refers to centers of endemism as indicated by the corrected in endemism centers CE1 and CE2, which are in unprotected weighted endemism metric. Redundancy refers to the number of areas at low elevations (0–3234 m.a.s.l.) in the Magdalena collections per grid cell. department (Caribbean region) and the inter-Andean dry val- leys of Norte de Santander department. Solanum flahaultii is endemic to the eastern mountain range, while S. lobbianum is highly endemic to the central mountain range (CE3 in los Pastos” is located in the southern part of the department Figure 4c). Centers CE3 and CE4 are situated at higher ele- near Ipiales and Laguna de la Cocha. The southern part of vations (2100-3500 m.a.s.l.) in the departments of Risaralda Nariño encompasses Sapuyes, Ospina, Pupiales, Tuquerres, and Tolima, both neighboring the Caldas department. and Cuaspud. The lower slopes of eastern Nariño—bordering the Putumayo department and covering the municipalities of Colon, Santiago, Sibundoy, San Francisco, and El Tablon de 3.3 Biogeographic regions Gomez—remain unprotected and are mostly located outside of paramo ecosystems. Our spatial analysis revealed a clear biogeographical pat- Solanum colombianum and S. lobbianum are found along tern with six clusters, each corresponding to specific Andean the border between the Tolima and Caldas departments. These mountain ranges and isolated sites similar to the Sierra sites are situated within the central Andean mountain range Nevada de Santa Marta (Figure 5). Cluster 1 (red) encom- on the northern slopes, adjacent to the Los Nevados National passes the central and eastern subregions, including the 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GONZÁLEZ-OROZCO ET AL. Crop Science 9 F I G U R E 5 Geographic regions of wild relatives of potatoes in Colombia, showing (a) six geographic clusters, by color code (red, blue, green, purple, orange, and yellow) indicating species occurrence in the clusters, and (b) the dendrogram based on geographic distances. The colors in the map and dendrogram refer to the six different clusters. highlands of Cundinamarca-Boyacá. Cluster 2 (green) is 3.5 Gap analysis endemic to the departments of Nariño and Cauca. Cluster 3 (blue) covers the region between the Caldas and Tolima The ex situ gap analysis identified four species as having a low departments and clustering in the foothills of Los Nevados priority for conservation, while one species was considered National Park. Cluster 4 (yellow) is endemic to the upper to be sufficiently conserved (Table 2). This result indicates a plateaus near Bogotá’s eastern mountain range. Cluster 5 (pur- satisfactory representation of diversity for ex situ conservation ple) is specific to the northern Caribbean region. Finally, efforts. On the other hand, the in situ gap analysis designated Cluster 6 (yellow) corresponds to the southern and eastern three species as high priority, one as medium priority, and one parts of Cauca. as low priority, suggesting the need for further investigation and implementation of measures for both in situ and ex situ conservation (Table 2). 3.4 Species distribution modeling The highest predicted species richness is observed in areas with four species (Figure 6a). Significant regions of potential We generated SDM for five species (Figure S1). All species species diversity include the Macizo Colombiano and Nudo showed niche climate preferences for high elevations across de los Pastos, located in the departments of Cauca and Nar- the three Andean mountain ranges. For the species S. lob- iño, as well as the high elevations of Valle del Cauca, Tolima, bianum and S. colombianum, maximum temperature played a Huila, and Caldas in the central Andean range. Addition- predominant role in the niche models, contributing more than ally, several scattered centers are found in the central Andean 75% to the prediction of niche suitability at high elevations in mountain range, including the Los Nevados region, Choachi, the southern and central Andean regions. Conversely, precip- and Ubaque on the eastern Andean range of Cundinamarca. itation significantly influenced the predicted distribution of S. Other centers of the highest species richness are found in var- garcia-barrigae, particularly at lower elevations and northern ious municipalities in the east of Boyacá highlands and the latitudes in Colombia. high peaks of the Sierra Nevada de Santa Marta. 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 10 Crop Science GONZÁLEZ-OROZCO ET AL. T A B L E 2 Results of ex situ and in situ conservation gap analysis for five wild potato species distributed in Colombia. Species name FCSex (%) FCSex_class FCSin (%) FCSin_class FCSc_mean (%) FCSc_class S. andreanum 54.79 LP 14.65 HP 34.72 MP S. colombianum 78.18 SC 24.25 HP 51.21 LP S. flahaultii 66.35 LP 34.38 MP 50.36 LP S. garcia-barrigae 54.83 LP 21.76 HP 38.29 MP S. lobbianum 67.55 LP 58.95 LP 63.25 LP Note: The percentages indicate the final conservation score (FCS) for ex situ (FCSex) and in situ (FCSin) conservation efforts. The conservation categories assigned to the species are as follows: low priority (LP), sufficiently conserved (SC), high priority (HP), and medium priority (MP). It is important to note that all five species fall within the secondary genepool of cultivated potato. Furthermore, other centers are identified in the northern as a strategic measure to mitigate the loss of agrobiodiversity part of the western Andean Mountain range, covering the (Gonzalez-Orozco et al., 2021). highlands of Antioquia, Risaralda, and Valle del Cauca, as This study highlights the significance of linking agriculture well as the Serranía of Perijá in the department of Cesar. Sig- and biodiversity through public information, underscoring nificant collecting gaps were identified in areas such as the the value of historical collections such as herbariums and Sierra Nevada de Santa Marta, El Cocuy National Park, the genebanks. Using these potato datasets, we were able to central Andean range in Cauca, Huila, and Tolima depart- determine the present conservation status of five wild potato ments, and the western Andean range of Valle del Cauca, species with distributions in Colombia, identifying both the Risaralda, and Chocó. observed and potential centers of diversity for these species. Additional conservation information was also provided for the germplasm collections stored in the CCC. This information 3.6 Priority sites for conservation supports the development of strategies and the establishment of priority sites for both in situ and ex situ conservation and sampling. To enhance conservation efforts, we have identified a list of municipalities (second administrative level) and veredas (third administrative level) that we propose as priority sites 4.1 What is the current conservation status for further collection missions (Table 3; refer to predicted of wild potato species in Colombia? gap species richness value of four in Figure 6b). These sites have been selected based on species gaps and endemism The results of this study showed that in general, there is hotspots. Among the regions with the largest number of a good representation of the five native species of Colom- species with high-priority conservation gaps in Colombia are bia in ex situ conservation. Therefore, the seed genebanks Cauca, Boyacá, and Tolima departments, with a maximum play a crucial role in conserving wild potato species in of 65 unexplored localities in Cauca and 73 in Boyacá. The Colombia. Our results differ from a previous global analy- proposed list of high-priority sites for further collecting is sis of potato CWR. At the species level, Castañeda-Álvarez comprehensive, encompassing a wide range of elevations and et al. (2015) reported S. garcia-barrigae and S. lobbianum as latitudes from north to south of the country. high priority for ex situ conservation, S. andreanum and S. flahaultii as medium priority, and S. colombianum as low pri- ority. However, our regional ex situ analysis categorized all 4 DISCUSSION species as low priority, except S. colombianum categorized as sufficiently conserved. This discrepancy highlights how con- CWR are an untapped reservoir of genetic diversity and play servation status outputs can differ between regional and global a crucial role in addressing food security and climate-related scales. Based on the current state of germplasm of potato challenges. They offer valuable genetic traits that are often CWR at the CCC in Colombia, we propose upgrading the ex absent in the cultivated species. CWR have the potential to situ conservation status to high priority for S. garcia-barrigae enhance pest and disease resistance, stress tolerance, nutri- and S. lobbianum owing to the limited number of accessions tional profile, and other traits that are vital for improving in the CCC. Solanum lobbianum has a highly restricted cli- productivity, quality, and sustainability in agriculture (Bohra mate niche suitability. Therefore, any event that threatens et al., 2022). The initial step in harnessing the potential the niche area could increase the probability of extinction of CWR is to assess their conservation status and identify of this species. Solanum garcia-barrigae has a broader niche hotspots of genetic resource diversity. This approach serves breadth than S. lobbianum, making it less vulnerable but still 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GONZÁLEZ-OROZCO ET AL. Crop Science 11 T A B L E 3 Priority sites for further collecting selected based on the largest number of species with high-priority conservation gaps of wild relatives of potato in as shown in Figure 6b. Department Municipalities Veredas Elevational range Bioregion (first administrative level) (second administrative level) (third administrative level) (m.a.s.l.) Andean Nariño Ipiales, Funes, San Pedro de Granja Agrícola La Paz, Villa de Leyva, San Julian, Llanitos, Ospina Perez, 3580–3900 Pasto Santa Barbara, El Encanto Cauca Santa Rosa, Inza, Silvia, San Andres, La Soledad, Chontillal, Bombonal, Tarabita, La Agencia, Santo 2400–3400 Jambalo, Páez, Toribio, Domingo, Chichuque, Coscuro, Tumbichucue, Suin, Lame, La Troja, Corinto, Miranda Cuartel, Mosoco, Santa Martha, San Jose, Botatierra, Amoladero, El Trebol, Chuluambo, Santa Clara, Media Loma, Santiago, Delicias, Michambe, Pueblito, Pena del Corazón, Cumbre Nueva, San Pedro, Alto Real, Alto de los Troches, Guambia, Las Tapias, Bujios, Villa Nueva, Salado, El Tengo, Tranal, Alpes, Golondrina, Buenavista, Las Dantas, Chulluambo, El Robla, Quizgo, Alto de la Palma, Altamira, Asnenga, La Ovejera, La Esperanza, Mendes, Puente Quemado, La Primicia, Llanobuco, Yusayu, Caloto Huila, Santo Domingo, La Playa, El Silencio, Las Violetas, La Calera, Cajones Huila San Agustín, La Plata, Baraya, La Maria, Dos Aguas, El Líbano, La Trinidad, La Ribera, Villa Viciosa, Filo 1800–3800 Tello de Salazar, Betania, La Esmeralda, Nevado del Huila, Tolima Planadas, Rio Blanco, El Silencio, Parque Nacional, San José de las Hermosas, Cucuanita, El 2800–4000 Chaparral, Roncesavalles, Coco, Yerbabuena, Orisol, El Paraíso, Los Alpes, El Salado, Alpujarra, Alpujarra La Mielecita, La Lindosa, Valle del Cauca Florida, Pradera, Palmira, El Las Brisas, Pueblo Nuevo, La Rivera, Los Calenos, La Feria, Bolo Azul, 1700–3800 Cerrito, Ginebra, Guadalajara Bolo Blanco, Tenjo, Toche, Combia, Tenerife, El Rosario, El Salado, El de Buga, Tuluá, Sevilla, Placer, Juntas, Rio Loro, Santa Lucia, Barragan, Penas Blancas, Yotoco, Calima Miraflores, Tibi, San Juan, Maulen, San Juan Alto, Cumaral Alto, San Juan Alto, El Boleo, El Diamante, La Florida, La Colonia, El Caney, La Cecilia, La Primavera, La Unión, El Remolino, Jiguales, Vegel, Embalse Calima, San Jose, Paramillo Cundinamarca Chuachi, Ubaque La Victoria, San Roque, Cerezos Grandes, Mongue, Rondalla, Cruz Verde 2800–3350 Boyacá Miraflores, Zetaquira, La Vega, Centro, La Mesa, Pena Blanca, Muceno, Bancos de Páramo, 1700–4870 Ramiriqui, Tibana, Umbita, Resguardo Machilero, Quicua arriba, Cunica Molino, Cienaga Valvanera, Pachavita, Garagoa, Guanata, Mundo nuevo, Zanja arriba, Chinavita, Escobal, Suna arriba, Aquitania, Labranzagrande, Estancia y Tablón, Matarredonda arriba, Buenos Aires, Morro arriba, Socota, Chita, Jerico, Sativa Hormigas, Patanco, La Esperanza, Guarumal, Quebradas, Cardoso, norte, Susacon, El Cocuy, San Mombita, Sisvaca, Hibra, Magavita centro y sector Golconda, Charanga, Mateo, Covarachia, Chiscas, Corinto, Toquilla, Hato viejo, Usaza, Ochita, Correjimiento Chipaviejo, Guican El Cardon, Corral de Piedra, El Moral, El Verde, Pueblo Nuevo, Chusvita, Guaquira, Bacota, Socotacito, Ticuaquita, Tiza, Tequita, Hato, Ocavita, Batan, Topachoque, Zaracuta, Tobachia, Cardonal, Laurelal, Parroquita, Rechniga, Cortadera, Casagui, Carrisal, Primavera, Palchacual, Cañaveral, La Cueva, El Tabor, Tapias, El Pueblo, El Calvario, Gucan. (Continues) 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 12 Crop Science GONZÁLEZ-OROZCO ET AL. T A B L E 3 (Continued) Department Municipalities Veredas Elevational range Bioregion (first administrative level) (second administrative level) (third administrative level) (m.a.s.l.) Antioquia Belmira, Dabeiba, Urrao La Candelaria, Río arriba, El Chuscal, El Salado- La Honda, Chaque, La 3100–3400 Florida, La Magdalena, Orobugo alto, El Hato Santander Cerrito, Concepción, San Volcan, Tuli, Carabobo, Babega, Carcasi, Humala, El Chucharal, Laguna de 2100–2780 Miguel, Macaravita, Ortices Mologavita Norte de Santander Salazar de las Palmas, Villa Caro Galvanez, Ramirez 2800–3100 Pacific Choco Novita, San José del Palmar, El El Pino 2000–2500 Carmen de Atrato Caribbean Magdalena Santa Marta, Ciénaga, Resguardo Indígena Kogui-Malayo-Arahuaco, Nabusimake, Costa Rica 2100–4400 Aracataca, Fundación Cesar Valledupar, Pueblo Bello Chemesquemena, San Sebastian 3400–3900 Guajira Dibulla, Rioacha, San Juan del Palomino, Inspecciones de Policía Potre 4000–4200 Cesar, Rio Ancho Orinoquía Arauca Tame Cocouy 4300 Meta Cubarral, Lejanías, La Uribe El Triunfo, Parque Sumapaz, Sonora 3100–3700 Amazon Putumayo San Francisco Los Monos, La Siberia, Minchoy 3000–3300 Caquetá Florencia NA 1900–2490 Note: Elevation in meters above the sea level (m.a.s.l.) units. 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GONZÁLEZ-OROZCO ET AL. Crop Science 13 critical for conservation. Based on the Genesys database (https://www.genesys-pgr.org/), 50 accessions collected in Colombia for the five studied species in this analysis are reported in other worldwide genebanks (Table S1) in Perú (International Potato Center) and the Netherlands (Centre for Genetic Resources). In the international genebanks, there is a higher representation of S. colombianum accessions (30), followed by S. flahaultii (11) and fewer numbers for S. andreanum (4), S. lobbianum (4), and S. garcia-barrigae (1). Lower numbers of accessions but similar patterns are found in the CCC. The in situ diversity of wild potatoes in the country is inadequately sampled and predominantly occurs outside of protected areas (Figure 6a). There is still a need to complete in situ conservation efforts for reported and potentially undis- covered species. Even species such as S. andreanum and S. colombianum, which have adapted to various environments across the Andes in Colombia, present scores indicating the need for in situ conservation. The low levels of in situ conser- vation among widespread species underscores the significant conservation gap that still exists. Many actions are required to identify and promote com- plementary conservation processes at both ex situ and in situ levels (Castañeda-Álvarez et al., 2016). These actions may include collecting new accessions based on genetic diversity analysis. Conservationists should also consider establishing community genebanks, food conservation reserves, species conservation parcels, and new protected areas. The overall final conservation score (FCS) showed that potato CWR are relatively well conserved in Colombia, but actions must be taken mainly for in situ conservation. Vélez et al. (2016) reported their field expeditions for herbarium sampling and evaluation of the conservation status of S. andreanum, S. flahaultii, and S. colombianum in different areas of the center and south of Colombia. Wild populations were found for all three species. According to the parameters established by the IUCN (2003), the authors categorized the conservation status of S. andreanum and S. colombianum as less concerning, while S. flahaultii is considered vulnerable. However, the authors reported that the genetic diversity of S. colombianum and S. flahautii is being lost in some local areas due to agriculture expansion and livestock production. For S. colombianum, they found populations in only two of six areas explored in the past. In our current study, S. andreanum, S. colombianum, and S. garcia-barrigae were categorized as high priority for in situ conservation. F I G U R E 6 Maps of predicted species richness and predicted A global initiative called “Adapting agriculture to cli- distribution of hotspots for conservation of wild potato relatives in Colombia based on gap analysis. (a) The predicted species richness mate change” aims to collect, conserve, and promote the overlapped with protected areas; (b) the predicted hotspots areas with use of CWR of major crops for food security (Dempewolf high species gaps, indicating the overlap with indigenous reserves. The et al., 2014). The Norwegian government funds this 10-year scale denotes the number of species from 1 (blue) to 4 (red) for species project, which was initiated in 2013. The Millenium Seed richness or number of high-priority species with gaps for conservation. Bank of the Royal Botanical Garden, Kew Gardens, and the Global Crop Diversity Trust lead the project in close 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 14 Crop Science GONZÁLEZ-OROZCO ET AL. collaboration with national agricultural research programs in situ reserves of wild potato species. Many unprotected areas developing countries. The project also includes the interna- and conservation gap hotspot sites coincide with areas that tional agricultural research centers of the Consultative Group are high priority for in situ conservation of S. colombianum, of International Agricultural Research (CGIAR) and other S. andreanum, and S. garcia-barrigae. crop expert institutions. Activities of the project include The degree of endemism can help define even more spe- inventory and prioritization of CWR, gap analysis to diag- cific locations for conservation. Our data showed that the nose the state of ex situ and in situ conservation of CWR endemism hotspots (Figure 4c,d) and gap hotspots differed at the global and national levels, and collection missions in in the Caribbean and central Andes regions. Where there 25 countries (Eastwood et al., 2022). Successful collections are discrepancies, sites should be revisited to conduct new of CWR under threat were carried out in Peru and Brazil, collections with highly localized value. Unexplored sites of in some cases collecting germplasm without previous repre- range-restricted species, such as S. garcia-barrigae, S. lob- sentation in the genebanks (Medeiros et al., 2021; Sotomayor bianum, and S. andreanum, are insufficiently conserved in et al., 2023). Conservationists developed effective sampling situ and should be considered primary locations for investi- strategies and collection plans based on gap analysis, expert gating and collecting priority endemic taxa. The endemism experience, reports of earlier collections, herbarium speci- hotspots in the northern and central parts of the Andean region mens, and passport data from genebanks. Cadima et al. (2014) are mainly between 2900 and 3200 m.a.s.l., whereas in the showed how the project provided guidelines to prioritize areas northern latitudes, they are distributed below 2000 m.a.s.l. of in situ conservation and target areas for germplasm collec- Interestingly, hotspots of species richness do not neces- tion of species with less than five accessions conserved in the sarily spatially coincide with the sites of high endemism. national genebank of Bolivia. Similar actions could be imple- They should be treated as different kinds of hotspots mented in Colombia, where extensive and up-to-date field and managed separately, requiring appropriate conservation collections of potato CWR have not been carried out since strategies. 1992 (Vélez et al., 2016). Not only are single sites essential for conservation, but entire regions as well. In our study, we identified geographic areas that contain dissimilar and range-restricted species, 4.2 Where are the observed and potential which we propose as priority regions for the conservation centers of diversity for wild potato species that of wild potato species assemblages (Figure 5). Therefore, can help define priority sites for conservation we consider the southwestern corner of the country to be a and collection? high-priority region for conservation, as it harbors the largest narrowly distributed assemblage of taxa, isolated in the high Our results provide new information compared to the results peaks of the Macizo Colombiano and Nudo de los Pastos from a global analysis (Castañeda et al., 2015). We propose (Figure 5, green). Similarly, we found assemblages of unique the southern Andean region of Nariño as the primary diversity taxa in the northern regions of Colombia and the central hotspot for species richness. This region contains the largest Andean mountain ranges. In contrast, a more extensive clus- accumulation of sites with high species richness for wild pota- ter (red in Figure 5) is widespread and common in the western toes in Colombia. Second, the main gap in species richness is and eastern Andean mountain ranges. found in the central Andean areas of the Cauca, the Cundina- marca high plains, and the Los Nevados region between the Risaralda, Caldas, and Tolima departments. These regions are 4.3 Conservation strategies fundamental for future conservation plans because they have high potential for wild potato species yet are poorly explored Our study suggests strategies for in situ and ex situ conserva- and undersampled. tion. One of the ideas discussed here as a potential strategy The most unexplored regions—those with the greatest is the establishment of agrobiodiversity zones (ABZ). ABZs number of species with conservation gaps and a limited num- correspond to territories where local communities develop, ber of collections—are in the southwest of Tolima, northeast manage, and conserve the richness and diversity of native of Huila, southeast of Boyacá, and the Sierra Nevada de Santa natural resources (Ruiz Muller, 2009). Establishing commu- Marta. Protected areas can also guide decisions regarding pri- nity genebanks that promote in situ and local conservation ority sites for the establishment of reserves. Cauca, Valle del of the area’s traditional crops and their wild relatives is one Cauca, and Tolima departments in the southwest of the coun- of the principles for agrobiodiversity conservation. The crite- try, as well as Guajira, Magdalena, and Cesar in the northern ria for designating ABZs are high species diversity of native part of Colombia, have the most significant gap areas that resources, high socio-cultural diversity, the presence of culti- are currently unprotected (Figure 6a). These regions could vated and wild relatives, agroecosystems for conserving and be targeted to improve conservation efforts by stabilizing in sustaining native agrobiodiversity, and community land rights 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GONZÁLEZ-OROZCO ET AL. Crop Science 15 F I G U R E 7 Proposal for establishing agrobiodiversity zones (ABZs) and peasant reserve zones (ZRCs) in southwest Colombia’s center of wild potato diversity. The red and orange areas are sites of high predicted species and richness gaps. over the ABZ. This community-based agrobiodiversity strat- servation and the establishment of new ABZs. Our findings egy has great potential in Colombia. Unfortunately, ABZs are could help to delineate new ABZs and ZRCs for potatoes in still not included in Colombia’s environmental legislation. Colombia, particularly in Nudo de Los Pastos and Macizo The cultivated varieties of potatoes in Colombia originated Colombiano regions (Figure 7), where no ABZs or ZRCs cur- from areas that coincide with the high diversity of their wild rently exist. However, their definition is still an ongoing topic counterparts. Importantly, for the establishment of ABZs, of political discussion. By considering the overlapping zones regions with potential species diversity should overlap with of protected areas, paramo ecosystems, indigenous reserves, the settlements of indigenous peoples in those territories. and zones of wild potato species diversity, we have identified a We found that the Macizo Colombiano and the Nudo de los vast area that we propose as potential ABZs or ZRCs (see map Pastos in the departments of Cauca and Nariño (Figure 7) per regions in Figure 7). However, these areas should be care- comprise more than 10% of the country’s indigenous pop- fully selected given the sensitivity of boundaries of protected ulations, comprising 16 ethnic groups and 144 indigenous areas, paramo ecosystems, and indigenous reserves. reservations. According to WWF (2021) and other conserva- Moreover, the results of this study highlight the impor- tion organizations, 91% of indigenous territories are in good tance of ex situ conservation as exemplified by the CCC. ecological condition, and at least 36% are key biodiversity Genebanks play a critical role in ensuring the preservation areas. These data reinforce the significance of indigenous of wild materials, which entails monitoring and regenera- reserves (in Spanish Resguardo indígena) as remarkable legal tion efforts. Additionally, the CCC can serve as a platform and sociopolitical institutions. for repatriating Colombian wild potato relatives conserved In addition, the mentioned regions are characterized by a in genebanks abroad, thus enhancing their representativeness diversity of actors who come together in the territory, includ- within the country. ing farming communities actively engaged in agroecological Research projects could use these findings to formu- practices and conservation efforts. According to Colom- late conservation strategies for wild crop relatives and bian legislation, peasant reserve zones (Zonas de Reserva support the sustainable use of agrobiodiversity in the Campesina or ZRC in Spanish) are located in areas of American tropics. An example of such an initiative is exceptional environmental richness, typically situated on the the project “Nature-Positive Solutions for Shifting Agri- borders of paramo ecosystems and tropical dry forests (see food Systems to More Resilient and Sustainable Pathways” National Association of Peasant Reserve Zones and Hum- (https://bit.ly/3XEBS7S), led by CGIAR in collaboration with boldt Institute definition of ZRCs; Osejo et al., 2018). Both AGROSAVIA. The rich diversity uncovered in this study indigenous territories and ZRCs can contribute to in situ con- has already contributed to developing new potato varieties 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 16 Crop Science GONZÁLEZ-OROZCO ET AL. currently employed by farming communities (http://bitly.ws/ Conceptualization; investigation; writing—original draft; EsNt). writing—review and editing. A C K N O W L E D G M E N T S 5 CONCLUSION The authors would like to thank the Corporación Colombiana de Investigación Agropecuaria (AGROSAVIA) for providing The wild relatives of potato in Colombia are insufficiently funding under project 1002442 (2023 BGA Documentación sampled, both in situ and ex situ. They are highly vulnerable to BG Vegetal). We thank the OMICAS program for providing degradation due to the ongoing expansion of the agricultural research support (Grant ID: FP44842-212-2018 and OMI- frontier and to habitat loss in the Andes. Our study iden- CAS award ID: 792–61187). We would like to thank Clara tified several regions in Colombia as centers of endemism Inés Medina Cano and Andres Cortes Vera for helping us with (i.e., northern and central Andes regions) and species richness the discussion at the beginning of this study. We thank the (i.e., southwest region) for these wild relatives. We propose Genebank staff for their commitment to collecting and main- these priority areas for conservation, designated as poten- taining the CCC. We would like to thank the AGROSAVIA tial ABZs or ZRCs. Furthermore, we identified significant researchers who work as part of the support team at the sampling gaps in the western and central Andean mountain National Germplasm Bank Collection in Tibaitata, Colom- ranges, as well as in the Sierra Nevada de Santa Marta. These bia. We thank Glenn Hyman, Science Writer, and Editor of areas of high diversity often lack adequate protection. Their the Alliance Science Writing Service (Alliance of Bioversity conservation status varies, ranging from high to medium in International and CIAT) for English and copy editing of this terms of in situ diversity. manuscript. We also recommend conducting additional collecting cam- paigns to enhance ex situ collections, especially for species C O N F L I C T O F I N T E R E S T S T AT E M E N T confined to specific environments that may face a greater risk The authors declare no conflicts of interest. of extinction or loss of unique diversity. In particular, our study highlighted the inadequate representation of S. garcia- D AT A AVA I L A B I L I T Y S T AT E M E N T barrigae and S. lobbianum in the national BGVAA genebank, The species occurrences datasets (Supporting Information underscoring the need for focused ex situ conservation efforts. Data S1 and S2) and Figure S1 are directly available in the Although S. colombianum is sufficiently conserved in situ, supplementary information. ex situ collections need evaluations of genetic diversity to understand priority gap hotspots. Additionally, we suggest O R C I D further research to prioritize areas with conservation gaps. Carlos E. González-Orozco https://orcid.org/0000-0002- Ultimately, this study showed the critical role of genebanks 4593-9113 and historical data in guiding conservation efforts and future Chrystian C. Sosa https://orcid.org/0000-0002-3734-3248 research on native plant genetic resources. R E F E R E N C E S AU T H O R C O N T R I B U T I O N S Agrosavia. (2014). Establecimiento de la base de datos para Carlos E. González-Orozco: Conceptualization; data cura- caracterización de la variabilidad climática con fines agro- tion; formal analysis; investigation; methodology; writing— climáticos, Mosquera (Cundinamarca): s.n. https://www.agrosavia. original draft; writing—review and editing. Paula H. Reyes- co/productos-y-servicios/oferta-tecnol%C3%B3gica/l%C3%ADnea- Herrera: Conceptualization; data curation; investigation; agr%C3%ADcola/cultivos-transitorios-y-agroindustriales/sistemas- de-informaci%C3%B3n/723-sistema-experto-mapa visualization; writing—original draft; writing—review and Alzate-Velásquez, D. F. (2017). RegRAIN: Method RegRAIN (MLR, editing. Chrystian C. Sosa: Conceptualization; formal anal- Spline and IDW) for spatial interpolation of daily rainfall and air ysis; investigation; methodology; writing—original draft; temperature data from climate stations. R package version 0.1.0. writing—review and editing. Rosa T. Torres: Concep- https://github.com/Diegoa16/RegRAIN tualization; data curation; investigation; writing—original Alzate-Velásquez, D. F. (2018). Interpolación Regnie para lluvia y draft; writing—review and editing. Norma C. Manrique- temperatura en las regiones Andina, Caribe y Pacífica de Colom- Carpintero: Conceptualization; data curation; investigation; bia. Colombia Forestal, 21, 102–118. https://doi.org/10.14483/ writing—original draft; writing—review and editing. Zahara 2256201X.11601 Ayram, C. A. C., Etter, A., Díaz-Timoté, J., Buriticá, S. R., Ramírez, W., Lasso-Paredes: Conceptualization; investigation; writing— & Corzo, G. (2020). Spatiotemporal evaluation of the human footprint original draft; writing—review and editing. Ivania Cerón- in Colombia: Four decades of anthropic impact in highly biodiverse Souza: Conceptualization; investigation; writing—original ecosystems. Ecological Indicators, 117, 106630. https://doi.org/10. draft; writing—review and editing. Roxana Yockteng: 1016/j.ecolind.2020.106630 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GONZÁLEZ-OROZCO ET AL. Crop Science 17 Baptiste, B., Pinedo-Vasquez, M., Gutierrez-Velez, V. H., Andrade, G. I., K., Magos Brehm, J., Breidy, J., Breman, E., Brenes Angulo, A., . . . Vieira, P., Estupiñán-Suárez, L. M., Londoño, M. C., Laurance, W., Kilian, B. (2022). Adapting agriculture to climate change: A synopsis & Lee, T. M. (2017). Greening peace in Colombia. Nature Ecology & of coordinated national crop wild relative seed collecting programs Evolution, 1(4), 0102. across five continents. Plants, 11(14), 1840. https://doi.org/10.3390/ Bohra, A., Kilian, B., Sivasankar, S., Caccamo, M., Mba, C., McCouch, plants11141840 S. R., & Varshney, R. K. (2022). Reap the crop wild relatives for Fumia, N., Pironon, S., Rubinoff, D., Khoury, C. K., Gore, M. A., & breeding future crops. Trends in Biotechnology, 40(4), 412–431. Kantar, M. B. (2022). Wild relatives of potato may bolster its adapta- https://doi.org/10.1016/j.tibtech.2021.08.009 tion to new niches under future climate scenarios. Food and Energy Borón, V., Payán, E., MacMillan, D., & Tzanopoulos, J. (2016). Achiev- Security, 11, e360. https://doi.org/10.1002/fes3.360 ing sustainable development in rural areas in Colombia: Future González, M., Galván, G., Siri, M. I., Borges, A., & Vilaró, F. (2013). scenarios for biodiversity conservation under land use change. Land Resistencia a la marchitez bacteriana de la papa en Solanum com- Use Policy, 59, 27–37. https://doi.org/10.1016/j.landusepol.2016.08. mersonii. Agrociencia Uruguay, 7, 45–54. https://doi.org/10.31285/ 017 AGRO.17.513 Cadima, X., van Zonneveld, M., Scheldeman, X., Castañeda, N., Patiño, González-Orozco, C. E. (2021). Biogeographical regionalisation of F., Beltran, M., & Van Damme, P. (2014). Endemic wild potato Colombia: A revised area taxonomy. Phytotaxa, 484, 247–260. (Solanum spp.) biodiversity status in Bolivia: Reasons for conserva- https://doi.org/10.11646/phytotaxa.484.3.1 tion concerns. Journal for Nature Conservation, 22, 113–131. Gonzalez-Orozco, C. E., Ebach, M. C., Laffan, S. W., Thornhill, A. Carver, D., Sosa, C. C., Khoury, C. K., Achicanoy, H. A., Diaz, M. V., H., Knerr, N., Schmidt-Lebuhn, A., Cargill, C. C., Clements, M., Sotelo, S., Castañeda-Álvarez, N. P., & Ramirez-Villegas, J. (2021). Nagalingum, N. S., Mishler, B. D., & Miller, J. T. (2014). Quantify- GapAnalysis: An R package to calculate conservation indicators using ing phytogeographical regions of Australia using geospatial turnover spatial information. Ecography, 44, 1000–1009. in species composition. PLoS One, 9, e92558 https://doi.org/10.1371/ Castañeda-Álvarez, N. P., de Haan, S., Juárez, H., Khoury, C. K., journal.pone.0092558 Achicanoy, H. A., Sosa, C. C., Heider, B., Simon, R., Maxted, N., & Gonzalez-Orozco, C. E., Laffan, S. W., Knerr, N., & Miller, J. T. Spooner, D. M. (2015). Ex situ conservation priorities for the wild (2013). A biogeographic regionalisation of Australian Acacia species. relatives of potato (Solanum L. Section Petota). PLoS One, 10(4), Journal of Biogeography, 40, 2156–2166. https://doi.org/10.1111/jbi. e0122599. https://doi.org/10.1371/journal.pone.0122599 12153 Castañeda-Álvarez, N. P., Khoury, C., Achicanoy, H., Bernau, V., González-Orozco, C. E., Porcel, M., Alzate-Velásquez, D. F., & Orduz, Dempewolf, H., Eastwood, R. J., Guarino, L., Harker, R. H., Jarvis, J. (2020). Extreme climate variability weakens a major tropical agri- A., Maxted, N., Müller, J. V., Ramirez-Villegas, J., Sosa, C. C., Struik, cultural hub. Ecological Indicators, 111, 106015. https://doi.org/10. P. C., Vincent, H., & Toll, J. (2016). Global conservation priorities for 1016/j.ecolind.2019.106015 crop wild relatives. Nature Plants, 2, 16022. https://doi.org/10.1038/ González-Orozco, C. E., Sosa, C., Thronhill, A., & Laffan, S. W. (2021). nplants.2016.22 Phylogenetic diversity and conservation of crop wild relatives in Cerón-Souza, I., Delgadillo-Duran, D., Polo-Murcia, S. M., Sarmiento- Colombia. Evolutionary Applications, 14(11), 2603–2617. https:// Naizaque, Z. X., & Reyes-Herrer, P. H. (2023). Prioritizing Colom- doi.org/10.1111/eva.13295 bian plant genetic resources for investment in research using indi- Gonzalez-Orozco, C. E., Thornhill, A. H., Knerr, N., Laffan, S. W., & cators about the geographic origin, vulnerability status, economic Miller, J. T. (2014). Biogeographical regions and phytogeography of benefits, and food security importance. Biodiversity and Conser- the eucalypts. Diversity and Distributions, 20, 46–58. https://doi.org/ vation, 32, 2221–2261. https://doi.org/10.1007/s10531-023-02599- 10.1111/ddi.12129 7 Hardigan, M. A., Bamberg, J., Buell, C. R., & Douches, D. S. (2015). Crisp, M. D., Laffan, S., Linder, H. P., & Munro, A. (2001). Endemism Taxonomy and genetic differentiation among wild and cultivated in the Australian flora. Journal of Biogeography, 28, 183–198. https:// germplasm of Solanum sect. Petota. The Plant Genome, 8(1), 1–16. doi.org/10.1046/j.1365-2699.2001.00524.x https://doi.org/10.3835/plantgenome2014.06.0025 Dempewolf, H., Baute, G., Anderson, J., Kilian, B., Smith, C., & Harlan, J. R., & de Wet, J. M. (1971). Toward a rational classification Guarino, L. (2017). Past and future use of wild relatives in crop of cultivated plants. Taxon, 20(4), 509–517. https://doi.org/10.2307/ breeding. Crop Science, 57(3), 1070–1082. https://doi.org/10.2135/ 1218252 cropsci2016.10.0885 Hawkes, J. G. (1988). The evolution of cultivated potatoes and their Dempewolf, H., Eastwood, R. J., Guarino, L., Khoury, C. K., Müller, J. tuber-bearing wild relatives. Kulturpflanze, 36, 489–492. https://doi. V., & Toll, J. (2014). Adapting agriculture to climate change: A global org/10.1007/BF01986960 initiative to collect, conserve, and use crop wild relatives. Agroecol- ogy and Sustainable Food Systems, 38 Hawkes, J. G. (1990). The potato: Evolution, biodiversity, and genetic (4), 369–377. https://doi.org/ resources. Smithsonian Institution Press. 10.1080/21683565.2013.870629 Hawkes, J. G., Maxted, N., & Ford-Lloyd, B. V. (2000). The ex Devaux, A., Goffart, J. P., Petsakos, A., Kromann, P., Gatto, M., Okello, situ conservation of plant genetic resources. Kluwer Academic J., Suarez, V., & Hareau, G. (2020). Global food security, contribu- Publishers. tions from sustainable potato agri-food systems. In H. Campos, & O., Ortiz (Eds.), The potato crop. Springer. https://doi.org/10.1007/978- Hijmans, R. J., Gavrilenko, T., Stephenson, S., Bamberg, J., Salas, A., & 3-030-28683-5_1 Spooner, D. M. (2007). Geographical and environmental range expan- Eastwood, R. J., Tambam, B. B., Aboagye, L. M., Akparov, Z. I., Aladele, sion through polyploidy in wild potatoes (Solanum section Petota). S. E., Allen, R., Amri, A., Anglin, N. L., Araya, R., Arrieta-Espinoza, Global Ecology and Biogeography, 16(4), 485–495. https://doi.org/ G., Asgerov, A., Awang, K., Awas, T., Barata, A. M., Boateng, S. 10.1111/j.1466-8238.2007.00308.x 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License 18 Crop Science GONZÁLEZ-OROZCO ET AL. Hijmans, R. J., Jacobs, M., Bamberg, J. B., & Spooner, D. M. (2003). Enquist, B. J. (2018). The BIEN r package: A tool to access the Botan- Frost tolerance in wild potato species: Assessing the predictivity of ical Information and Ecology Network (BIEN) database. Methods in taxonomic, geographic, and ecological factors. Euphytica, 130, 47– Ecology and Evolution, 9, 373–379. 59. https://doi.org/10.1023/A:1022344327669 Mattheij, W. M., Eijlander, R., de Koning, J. R., & Louwes, K. M. Hijmans, R. J., Spooner, D. M., Salas, A. R., Guarino, L., & (1992). Interspecific hybridization between the cultivated potato de la Cruz, J. (2002). Atlas of wild potatoes. International Solanum tuberosum subspecies tuberosum L. and the wild species Plant Genetic Resources Institute. https://hdl.handle.net/10568/10 S. circaeifolium subsp. circaeifolium Bitter exhibiting resistance to 5275 Phytophthora infestans (Mont.) de Bary and Globodera pallida. The- IUCN. (2003). Directrices para emplear los criterios de la Lista Roja oretical and Applied Genetics, 83, 459–646. https://doi.org/10.1007/ de la UICN a nivel nacional y regional, versioťn 3.0, Preparadas BF00226534 por la comisión de supervivencia de especies la UICN. UICN- Maxted, N., Ford-Lloyd, B. V., Jury, S., Kell, S., & Scholten, M. Unión Mundial para la Naturaleza. www.iucnredlist.org/technical- (2006). Towards a definition of a crop wild relative. Biodiversity & documents/categories-and-criteria Conservation, 15, 2673–2685. Jarvis, A., Lane, A., & Hijmans, R. J. (2008). The effect of climate change Medeiros, M. B., Valls, J. F. M., Abreu, A. G., Heiden, G., Ribeiro-Silva, on crop wild relatives. Agriculture, Ecosystems & Environment, 126, S., José, S., Santos, I. R. I., Passos, A. M. A., & Burle, M. L. (2021). 13–23. https://doi.org/10.1016/j.agee.2008.01.013 Status of the ex situ and in situ conservation of Brazilian crop wild Jones, J. D. G., Witek, K., Verweij, W., Jupe, F., Cooke, D., Dorling, S., relatives of rice, potato, sweet potato, and finger millet: Filling the Tomlinson, L., Smoker, M., Perkins, S., & Foster, S. (2014). Elevating gaps of germplasm collections. Agronomy, 11, 638. https://doi.org/ crop disease resistance with cloned genes. Philosophical Transactions 10.3390/agronomy11040638 of the Royal Society B, 369, 20130087. https://doi.org/10.1098/rstb. Morrone, J. J. (2014). Biogeographical regionalisation of the Neotrop- 2013.0087 ical region. Zootaxa, 3782, 1–110. https://doi.org/10.11646/zootaxa. Khoury, C. K., Amariles, D., Soto, J. S., Diaz, M. V., Sotelo, S., Sosa, 3782.1.1 C. C., Ramírez-Villegas, J., Achicanoy, H. A., Velásquez-Tibatá, J., Nagel, M., Dulloo, M. E., Bissessur, P., Gavrilenko, T., Bamberg, Guarino, L., León, B., Navarro-Racines, C., Castañeda-Álvarez, N. J., Ellis, D., & Giovannini, P. (2022). Global strategy for the P., Dempewolf, H., Wiersema, J. H., & Jarvis, A. (2019). Compre- conservation of potato. Global Crop Diversity Trust. https://www. hensiveness of conservation of useful wild plants: An operational croptrust.org/fileadmin/uploads/croptrust/Documents/Ex_Situ_ indicator for biodiversity and sustainable development targets. Eco- Crop_Conservation_Strategies/Potato_Conservation_Strategy_ logical Indicators, 98, 420–429. https://doi.org/10.1016/j.ecolind. 2022_LR.pdf 2018.11.016 Osejo Varona, A., Marín Marín, W. J., Posada Molina, V., Sánchez, S. Laferriere, L. T., Helgeson, J. P., & Allen, C. (1999). Fertile Solanum A., & Torres Quijano, S. C. (2018). Zonas de reserva campesina tuberosum + S. commersonii somatic hybrids as sources of resis- en el escenario del posconflicto: Una estrategia comunitaria para tance to bacterial wilt caused by Ralstonia solanacearum. Theoret- el manejo de la biodiversidad. In L. A. Moreno, C. Rueda, & ical and Applied Genetics, 98, 1272–1278. https://doi.org/10.1007/ G. I. Andrade (Eds.), Biodiversidad 2017 (pp. 1–10). Estado y s001220051193 tendencias de la biodiversidad continental de Colombia. Insti- Laffan, S. W., & Crisp, M. D. (2003). Assessing endemism at mul- tuto de Investigación de Recursos Biológicos Alexander von tiple spatial scales, with an example from the Australian vascular Humboldt. flora. Journal of Biogeography, 30, 511–520. https://doi.org/10.1046/ Peralta, I. E., Clausen, A. M., Zorrilla, C., Ames, M., Digilio, A., & j.1365-2699.2003.00875.x Rodriguez, F. (2021). Wild and cultivated potato species diversity, Laffan, S. W., Lubarsky, E., & Rosauer, D. F. (2010). Biodiverse, a tool taxonomy and conservation. In D. Carputo, R. Aversano, & M. R. for the spatial analysis of biological and related diversity. Ecography, Ercolano (Eds.), The wild Solanum genomes (pp. 51–94). Springer. 33, 643–647. https://doi.org/10.1111/j.1600-0587.2010.06237.x https://doi.org/10.1007/978-3-030-30343-3_4 Laffan, S. W., Ramp, D., & Roger, E. (2013). Using endemism to Pérez-Escobar, O. A., Zizka, A., Bermúdez, M. A., Meseguer, A. S., assess representation of protected areas—The family Myrtaceae Condamine, F. L., Hoorn, C., Hooghiemstra, H., Pu, Y., Bogarín, in the Greater Blue Mountains World Heritage Area. Journal of D., Boschman, L. M., Pennington, R. T., Antonelli, A., & Chomicki, Biogeography, 40, 570–578. https://doi.org/10.1111/jbi.12001 G. (2022). The Andes through time: Evolution and distribution of Laffan, S. W., Rosauer, D. F., Di Virgilio, G., Miller, J. T., Gonzales- Andean floras. Trends in Plant Science, 27, 364–378. https://doi.org/ Orozco, C., Knerr, N., Thornhill, A., & Mishler, B. D. (2016). 10.1016/j.tplants.2021.09.010 Range-weighted metrics of species and phylogenetic turnover can Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum better resolve biogeographic breaks and boundaries. Methods in Ecol- entropy modelling of species geographic distributions. Ecological ogy and Evolution, 7, 580–588. https://doi.org/10.1111/2041-210X. Modelling, 190, 231–259. https://doi.org/10.1016/j.ecolmodel.2005. 12513 03.026 Liu, Z., & Halterman, D. (2009). Different genetic mechanisms control POWO. (2023). Plants of the world online. Royal Botanic Gardens, Kew. foliar and tuber resistance to Phytophthora infestans in wild potato http://www.plantsoftheworldonline.org/ Solanum verrucosum. American Journal of Potato Research, 86, 476– Rahaman, W., Magos Brehm, J., Maxted, N., Phillips, J., 480. https://doi.org/10.1007/s12230-009-9103-1 ContrerasToledo, A. R., Faraji, M., & Parra-Quijano, M. (2021). Maitner, B. S., Boyle, B., Casler, N., Condit, R., Donoghue II, J., Durán, Gap analyses of priority wild relatives of food crop in current ex situ S. M., Guaderrama, D., Hinchliff, C. E., Jørgensen, P. M., Kraft, N. J. and in situ conservation in Indonesia. Biodiversity & Conservation, B., McGill, B., Merow, C., Morueta-Holme, N., Peet, R. K., Sandel, 30, 2827–2855. http://reporte.humboldt.org.co/biodiversidad/2017/ B., Schildhauer, M., Stephen, A., Smith, S. A., Svenning, J-C., . . . cap4/404/#seccion9 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License GONZÁLEZ-OROZCO ET AL. Crop Science 19 Ruiz Muller, M. (2009). Las zonas de agrobiodiversidad y el registro Van der Vossen, E., Sikkema, A., Hekkert, B. t. L., Gros, J., Stevens, de cultivos nativos: Aprendiendo de nosotros mismos. Lerma-Gomez P., Muskens, M., Wouters, D., Pereira, A., Stiekema, W., & Allefs, Editores-Peru. S. (2003). An ancient R gene from the wild potato species Solanum Smyda, P., Jakuczun, H., Dębski, K., Sliwka, J., Thieme, R., Nachtigall, bulbocastanum confers broad-spectrum resistance to Phytophthora M., Wasilewicz-Flis, I., & Zimnoch-Guzowska, E. (2013). Develop- infestans in cultivated potato and tomato. Plant Journal, 36, 867–882. ment of somatic hy brids Solanum × michoacanum Bitter. (Rydb.) https://doi.org/10.1046/j.1365-313X.2003.01934.x (+) S. tuberosum L. and autofused 4x S. × michoacanum plants as Vélez, J. M., Pineda, R., Galindo, L., Arango, R., & Morales, potential sources of late blight resistance for potato breeding. Plant J. G. (2016). Current situation of wild Solanum spp. L. sect. Cell Reports, 32, 1231–1241. https://doi.org/10.1007/s00299-013- Petota (Solanum, Solanaceae) in some Colombian regions. Genetic 1422-5 Resources and Crop Evolution, 63, 47–54. https://doi.org/10.1007/ Sotomayor, D. A., Ellis, D., Salas, A., Gomez, R., Sanchez, R. A., s10722-015-0234-6 Carrillo, F., Giron, C., Quispe, V., Manrique-Carpintero, N. C., WWF. (2021). The state of indigenous peoples’ and local commu- Anglin, N. L., & Zorrilla, C. (2023). Collecting wild potato species nities’ lands and territories. World Wildlife Foundation. https:// (Solanum sect. Petota) in Peru to enhance genetic representation and wwfint.awsassets.panda.org/downloads/report_the_state_of_the_ fill gaps in ex situ collections. Frontiers in Plant Science, 14, 1044718. indigenous_peoples_and_local_communities_lands_and_territor. https://doi.org/10.3389/fpls.2023.1044718 pdf Spooner, D. M., Ghislain, M., Simon, R., Jansky, S. H., & Gavrilenko, T. (2014). Systematics, diversity, genetics, and evolution of wild and cultivated potatoes. The Botanical Review, 80, 283–383. https://doi. org/10.1007/s12229-014-9146-y S U P P O R T I N G I N F O R M AT I O N Spooner, D. M., & Hijmans, R. J. (2001). Potato systematics and Additional supporting information can be found online in the germplasm collecting, 1989–2000. American Journal of Potato Supporting Information section at the end of this article. Research, 78, 237–268. https://doi.org/10.1007/BF02875691 Spooner, D. M., & Salas, A. (2006). Structure, biosystematics, and genetic resources. In J. Gopal & S. M. P. Khurana (Eds.), Handbook of potato production, improvement, and post-harvest management (pp. How to cite this article: González-Orozco, C. E., 1–39). Haworth’s Press. Reyes-Herrera, P. H., Sosa, C. C., Torres, R. T., Spooner, D. M., van den Berg, R. G., Rodríguez, A., Bamberg, J., Manrique-Carpintero, N. C., Lasso-Paredes, Z., Hijmans, R. J., & Lara Cabrera, S. I. (2004). Wild potatoes (Solanum Cerón-Souza, I., & Yockteng, R. (2023). Wild section Petota; Solanaceae) of North and Central America. Systematic relatives of potato (Solanum L. sec. Petota) poorly Botany Monographs, 68, 1–209. https://doi.org/10.2307/25027915 Tucci, M., Carputo, D., Bile, G., & Frusciante, F. (1996). Male fertil- sampled and unprotected in Colombia. Crop Science, ity and freezing tolerance of hybrids involving Solanum tuberosum 1–19. https://doi.org/10.1002/csc2.21143 haploids and diploid Solanum species. Potato Research, 39, 345–353. https://doi.org/10.1007/BF02357938 14350653, 0, Downloaded from https://acsess.onlinelibrary.wiley.com/doi/10.1002/csc2.21143 by CochraneItalia, Wiley Online Library on [14/12/2023]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License