Received: 22 February 2021 Revised: 1 September 2021 Accepted: 6 September 2021 DOI: 10.1002/ppp3.10233 OPINION Crop archaeogenomics: A powerful resource in need of a well-defined regulation framework Alice Iob | Laura Botigué Centre for Research in Agricultural Genomics (CRAG), CSIC-IRTA-UAB-UB, Barcelona, Spain Societal Impact Statement Crop archaeogenomics has rapidly flourished in recent years, leading to a new way of Correspondence Laura Botigué, Centre for Research in understanding the past and bringing answers to important questions about human Agricultural Genomics (CRAG), CSIC-IRTA- history in relation to plant management and food production. Furthermore, the UAB-UB, CRAG building, campus UAB, 08193 Cerdanyola, Barcelona, Spain. knowledge derived from the analysis of ancient crops can contribute to the develop- Email: laura.botigue@cragenomica.es ment of a more sustainable future. However, the extant legal framework presents a number of challenges when applied to this research field, particularly in the current scenario of disparities in scientific outcomes between countries. We expose the uncertainties of the legal framework and the factors that maintain or exacerbate these inequalities, as well as possible solutions. Summary Crop archaeogenomics is a flourishing field that has greatly benefited from next- generation sequencing technologies. Ancient and historical plant remains are currently considered genetic resources and as such are subject to legal frameworks like those implemented by the Nagoya Protocol. In addition to the challenges in complying with genetic resource regulations that crop archaeogenomics share with other basic plant research disciplines, there are additional difficulties specific to this interdisciplinary field that includes science and humanities, namely, the need to comply with two different legislations before accessing the samples (one for genetic resources and one for cul- tural heritage), along with a high risk of not obtaining DNA. As a result, most studies to date have been done on samples for which the laws regulating genetic resources did not apply, sometimes avoiding the need of reaching Access and Benefit Sharing agree- ments with the country that originally provided the samples. This phenomenon is likely to worsen in the future, as the archaeological record is a limited resource and competi- tion between laboratories will only widen the gap between developed and developing economies. Because crop archaeogenomics is a new and promising scientific field, it is desirable to begin a dialogue with other basic biological research fields to facilitate the implementation of these agreements so that basic sciences can easily utilize these biological samples while ensuring the rights of all parties involved. KEYWORDS access and benefit sharing, crop archaeogenomics, genetic resources, Nagoya protocol, policy This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited and is not used for commercial purposes. © 2021 The Authors. Plants, People, Planet published by John Wiley & Sons Ltd on behalf of New Phytologist Foundation. 44 wileyonlinelibrary.com/journal/ppp3 Plants People Planet. 2022;4:44–50. 25722611, 2022, 1, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10233 by Readcube (Labtiva Inc.), Wiley Online Library on [25/05/2023]. 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  IOB AND BOTIGUE 45 1 | I N T RO DU CT I O N BOX 1 Assessing the value of archaeobotanical The field of archaeogenomics has come a long way since the publica- samples. Examples from (Zohary et al., 2012) tion of a mitochondrial sequence from a museum-preserved quagga in 1. Uneven geographic distribution of the archaeological record: 1984 (Higuchi et al., 1984) and has recently flourished thanks to the The abundance of archaeological sites is uneven across the development of genomic sequencing technologies. globe. Although the archaeological record provides an over- Although most archaeogenomic studies have so far been per- all reliable overview of crop domestication in Europe, South- formed in animals (including hominins), plant archaeogenomics has west Asia and the Mediterranean basin, other regions have gained increasing attention in the last decade, because few samples not been as explored, such as South Asia or in Africa, south are a powerful resource to investigate important events such as plant of the Sahara. domestication. Processes like selection, local adaptation and early dis- 2. Type of sample: Seeds are, together with microscopic pol- persal of domestic forms have been investigated in major crops, such len, the more resilient parts of the plants and thus represent as barley (Mascher et al., 2016; Palmer et al., 2009), bread wheat (Li the most abundant form of crop remains from early farming et al., 2011), cotton (Palmer et al., 2012), maize (da Fonseca villages in the old world. On the contrary, horticultural vege- et al., 2015), emmer wheat (Scott et al., 2019) and bean (Trucchi tables that furthermore may undergo different food et al., 2021). Plant ancient DNA analyses study both past human– processing techniques are very rare because they have environment interactions and the evolutionary forces that shaped fewer chances to survive as archaeological remains. modern crops. Furthermore, knowledge obtained from crop 3. Conservation status: The conservation status will also archaeogenomics holds great potential to aid in the development of affect the value of the sample. Samples are usually charred, new conservation strategies, breeding programmes and agricultural less commonly desiccated (when located in conditions of practices in response to climate change and human pressure on the extreme dryness such as desertic areas), or waterlogged environment (Di Donato et al., 2018; Estrada et al., 2018; Hofman (e.g., in lakes or wells in anaerobic conditions). They can also et al., 2015; Pont et al., 2019; Przelomska et al., 2020). be mineralized, in phytolites and coprolites. Desiccated With the advent of ancient DNA analysis, legal and ethical issues remains have so far proven to be more likely to contain have arisen. These include the ethical implications of undertaking the ancient DNA than charred remains do. genetic analysis of ancient humans, their cultural bonds with present- 4. Uneven temporal distribution of the archaeological record: day communities, competition between research groups, hoarding of Within a given archaeological site the abundance of samples material from the Global South, and limits in experiment replication can vary between historical periods or sections excavated. due to the intrinsic value of the sample coupled with their finite avail- This happens for instance at the site of Troy; although it is ability, both for human (Bardill et al., 2018; Elliott, 2009; Paradise & rich in plant remains in sections dated to the Middle Bronze Andrews, 2007; Wagner et al., 2020) and archaeofaunal remains Age, only a few specimens belonging to the Early Bronze  ttir et al., 2019). (Pálsdo age and Neolithic have been recovered. In the case of crop archaeogenomics, many factors (including 5. Additional value: some specimens have an added cultural stochasticity) play a very important role in determining the preserva- value. The material used to make artefacts (e.g., necklaces tion and the cultural value of the remains (see Box 1 for more details). made of seeds and baskets made of leaves) is not only infor- Usually, the most promising samples consist of seeds or leaves (small mative about the plants themselves but also about the cul- amounts of material), and DNA extraction is most often a destructive ture that fabricated those artefacts, trade networks, etc. experimental procedure that effectively impoverishes the Another example would be for plant remains found in exca- archaeobotanical record. Moreover, it is not possible to know what vations or burials of historical characters notorious to soci- fraction of the archaeobotanical record contains DNA, but so far it ety. Results from these studies would have higher chances seems to be modest, especially for charred remains (Nistelberger to be disseminated by the media because of their capacity et al., 2016). The relative abundance of ancient material has shielded to engage society, rather than the strictly scientific findings this field from the competition and hoarding that have occurred in from those studies. human archaeogenomics (Makarewicz & Nimrod Marom, 2017; Morris, 2017). However, the growing interest in the discoveries from crop archaeogenomics, coupled with the constant technical research for improvements (e.g., Brown et al., 2014; Gamba et al., 2016; Lendvay et al., 2018), could rapidly change that. We discuss here aspects of this research field under the Conven- which include (1) the obligation to abide by both heritage and genetic tion on Biological Diversity (CBD) and Nagoya Protocol regulation and the inadequacies of CBD definitions when it comes to (NP) international framework. The field of ancient crop genomics archaeobotanical remains; (2) limitations of the current legal frame- shares many aspects with other basic research disciplines, such as the work for Access and Benefit Sharing (ABS) agreements, and (3) possi- non-monetary nature of the results, but it has also some peculiarities, ble solutions to improve the current situation. 25722611, 2022, 1, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10233 by Readcube (Labtiva Inc.), Wiley Online Library on [25/05/2023]. 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 46  IOB AND BOTIGUE This opinion piece focuses on archaeobotanical macroremains act upon the increasing globalization and environmental degradation, of crops because of their important role in human development while promoting the wellness of humanity. and history. However, we note that plant archaeogenomics includes the analysis of many kinds of remains, among others plant DNA in ancient sediments, coprolites and wood remains. For a 3 | I N A DE Q U A C I E S O F T H E C B D more detailed read on plant archaeogenomics, a review DE F I N I T I O N S A N D T H E N P F RA M E W O R K covering this topic has been recently published elsewhere (Kistler FO R A R C H A E O B O T A N I C A L R E M A I N S et al., 2020). The CBD defines genetic material as “any material of plant, animal, microbial or other origin containing functional units of heredity”, and 2 | THE L EGAL FRA M EW ORK defines genetic resources as “genetic material of actual or potential value” (Cooper & Noonan-Mooney, 2013). In addition, under the NP, Geneticists can access archaeobotanical remains either by establishing authorization to use the genetic resources must be obtained before a collaboration with an archaeobotanist or, when the samples have accessing them. In the study of crop archaeogenomics, this is particu- already been deposited, with a curator of a museum or an herbarium. larly daunting because it is not possible to know whether the sample In the first case, the decision to collaborate will depend on the archae- of interest contains DNA without processing it first. Indeed, it is not ological project, its director or the archaeobotanist, depending on the at all clear if ancient plant remains should be considered genetic institutions involved. In the case of museum or herbarium collections, resources. Foremost, ancient biological samples include a long list of the decision process varies, but usually involves, an internal or exter- remains as well as archaeological artefacts, most of which do not con- nal evaluation of the request as per general disciplinary standards: sci- tain endogenous DNA at all. Second, if endogenous DNA is still pre- entific need, nature of the project and research potential against the sent inside the sample, it is highly fragmented and degraded need to preserve the collections.  nsson et al., 2013; Pääbo et al., 2004), containing numerous (e.g., Jo In cases where the collaboration is established between multiple nucleotide misincorporations which prevent its functionality (only two countries, the movement of the samples must be granted following notable exceptions have been described so far; Sallon et al., 2008; two national laws: that covering archaeological material and, if they Shen-Miller et al., 1995). exist, that of genetic resources. For the former, export permits have Under the present legal framework, the intention to undertake a to be requested and accepted by Antiquity Authorities or Heritage genetic analysis on an ancient plant specimen turns this sample into a Institutions, even though exceptions exist (e.g., Egypt restricts the genetic resource. Archaeological plant material is regulated only by export of all materials). Agreements usually last for a known time, dur- Cultural and Heritage laws up until the time a researcher wants to do ing which researchers can study the archaeological material. If the a genetic analysis on this material. At this point, the sample acquires a analyses entail the destruction of the samples, it is usually harder to potential value that turns it into genetic resources according to the obtain the authorization. CBD terms. Nevertheless, most likely the sample cannot be consid- Regarding the genetic nature of the material, two international ered to be genetic material because it does not contain DNA, espe- agreements have also been established. The United Nations cially if defined as functional units of heredity. This high risk of not (UN) CBD entered into force in 1993 with the goals of conserving bio- obtaining DNA from archaeobotanical remains and the additional logical diversity, promoting the sustainable use of its components, and bureaucratic burden to comply with genetic, cultural and heritage reg- the fair and equitable ABS arising from their utilization. So far, it has ulations has led to the avoidance of NP-regulated archaeobotanical been signed by 196 Parties, with the notable absence of the remains. The main downside of this legal framework is the require- United States, among other countries (Cooper & Noonan- ment to enter into agreements before accessing the sample and thus Mooney, 2013). The NP emerged to provide a legal framework to be allowed to test the feasibility of the research project (i.e., the pres- implement the third objective of the CBD, entered into force in 2014 ence of analysable DNA in the sample). As a result, at times, the coun- and has 128 Parties. Briefly, the NP sets out core obligations for its try of origin of the sample, provider country henceforth, is not contracting parties through mutually agreed terms concerning access considered at all in the study. This prevents the involvement of to genetic resources, benefit sharing and compliance. It also covers researchers from this country and promotes the unfair distribution of traditional knowledge associated with genetic resources, taking into benefits arising from the use of resources that the very NP was account the role of indigenous people and local communities established to avoid. (UN CBD, 2011). Each country implements NP with its own national ABS policies and laws, as the CBD recognizes each country's sover- eignty over its own genetic resources. 4 | TH E NE E D TO P R O M OTE A N A BS The ultimate intent of these international agreements is to avoid AGRE EM ENT undue appropriation of natural resources and unfair distribution of ben- efits arising from their exploitation. Thus, these agreements were born Although crop archaeogenomics is a basic science field and no mone- out of the necessity for international legal and ethical standards that tary profit can be envisioned out of it, it is still necessary to ensure 25722611, 2022, 1, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10233 by Readcube (Labtiva Inc.), Wiley Online Library on [25/05/2023]. 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  IOB AND BOTIGUE 47 that research and scientific collaborations follow fundamental ethical hinders the data analysis process. International initiatives such as eIFL principles. All parties involved in a given study should share intellec- (eILF - Open Access Programme), INASP (Inasp - Homepage) and tual and technological benefits, consistent with the intent of the NP Research4Life (Research4life Organization) have incentivized access to to promote developing economies' technical capacities and science science and scientific advancement in the so-called Global South, building. The field of crop archaeogenomics is usually led by even if extant inequalities remain difficult to overcome (Powell researchers from the Global North even though many plant remains et al., 2020). originate from the Global South. There are various reasons embedded The ultimate consequence of these factors is a movement of in the research area that explain this: First, the generation of the data ancient biological samples from the Global South to the Global North. is a very expensive process. It requires the construction of an exclu- Samples are then processed and analysed by researchers in countries sively dedicated laboratory facility and continuous expense in that do have the infrastructures to do so (Morris, 2017; Prendergast & laboratory material to minimize the risk of contamination Sawchuk, 2018) (Figure 1). Without an ABS agreement, Global South from external sources and cross-contamination between samples countries that provided the samples risk having a mere testimonial (e.g., Krause, 2010; Pääbo et al., 2004). It also requires investment for role in the study, if they are represented at all. Considering the studies sequencing and bioinformatic analyses. All these factors, along with mentioned in Figure 1 in at least 70% of the cases (8 of 12) where the intrinsic uncertainty of obtaining (good amounts of) target DNA, samples were originally excavated in a country of the Global South, leave developing economies out of the race of leading no author is affiliated with an institution of a developing economy. archaeogenomic studies, even those that have a rich archaeological When present, authors from institutions in developing economies did record. not play a major role in the research, as reflected in the affiliation of Second, the data to analyse consist of digital sequence informa- the first and last authors. tion (DSI) to be processed along with other DSI available in public databases. Currently though, many institutions in developing econo- mies cannot afford the subscription fees for many scientific journals 5 | S O L U T I O N S WI T HI N T H E N P where the information to locate the DSI in repositories is found, hin- dering their access to new knowledge and the genomic data Recently, a new concept has been coined to refer to the colonialist (Djikeng, 2012; Helmy et al., 2016). Besides, the lack of basic infra- practices that still occur in science, the helicopter research (Minasny structures, such as fast and stable internet connection to download et al., 2020). More and more voices are being raised about the need the DSI, as well as access to high-performance computers further to maintain certain ethical rules when performing research involving F I G U R E 1 Movement of crop macroremains from country of origin to ancient DNA facilities up to 2019. The movement of samples from country of origin to the country where they were processed. The dimension of the dots depends on the number of the resulting scientific publications. This map has a per country resolution, the location of dots/triangles is not related to exact archaeological sites/labs coordinates inside the country. The number of samples analysed is reported on the left panel, next to the country where the analysis took place. The genomic studies considered in this figure are those included in (Kistler et al., 2020), hence reflecting studies published up to December 2019, not a complete survey of ancient DNA studies on plants. Studies about wood have been excluded, not being about crops 25722611, 2022, 1, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10233 by Readcube (Labtiva Inc.), Wiley Online Library on [25/05/2023]. 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 48  IOB AND BOTIGUE countries in the Global South. The NP, through the implementation of parties should ensure the active participation of researchers from the ABS agreement, is the perfect venue to ensure that these non- that country in the study. Indeed, we think that standardization of an monetary benefits are included when planning a research project. ABS agreement for non-monetary benefits focused on avoiding heli- However, in the specific case of archaeogenomics, there are a large copter research practices would have a very positive impact on that number of samples that were collected before the NP entered into regard. This standard ABS form could even exist beyond the force and therefore escape this regulation. In addition, the need to framework of the NP and be used more broadly by researchers from draft an agreement before accessing samples combined with the high the Global North and South before undertaking international risk of not obtaining DNA from them has a deterrent effect that collaborations. results in avoiding the selection of NP-regulated specimens. Given that crop archaeogenomics is a novel field, which can and As other authors pointed out, one solution would be to have spe- likely will grow in the future, we think this is the right time to open a cific regulations for ancient (and historical) plant material within the dialogue about possible options to aid easy access to resources for NP. However, this is hard to accomplish, at least in the near future scientists while preserving the archaeological record and granting ben- (Sherman & Henry, 2020). A more interdisciplinary strategy is more efit sharing and inclusion of research institutions in developing econo- likely to succeed. There is an ongoing debate around the bureaucratic mies. Standards in accessing the samples coupled with active sharing burden that basic plant research faces to comply with ABS of the benefits deriving from the research could help to take away dis- (e.g., Kursar, 2011; Schindel, 2010; Watanabe, 2015). Certain solu- parities between scientific communities in different countries and tions have been proposed, such as mechanisms that would allow dif- support the development of this field worldwide. Even if CBD and NP ferentiating between monetary and non-monetary benefits were drafted to recognize the sovereignty of each country over its (Rourke, 2018). We also advocate a solution that goes beyond the genetic resources, we strongly believe that in the end all of us should specific case of non-modern plant specimens and unites all basic bio- gain benefit from the reconstruction of past phenomena such as plant logical research. domestication, which can be seen as a form of collective heritage of We propose two actions that would have a positive impact in the humankind. present circumstances. First, add a clause in the NP for all basic sci- ence disciplines that do not entail monetary benefits, allowing explor- AC KNOW LEDG EME NT S atory analyses on the samples for a short time frame to determine the We would like to thank Dr. Amaia Arranz-Otaegui and Dr. Alex Weide feasibility of the proposed project. This is similar to the regulations for helpful suggestions regarding archaeobotanical samples, the team applied in social sciences, where samples are allowed to be studied for n Protocolo de Nagoya for their insights on the legal of the Buzo a restricted period. Second, a standardized ABS agreement, designed aspects of the NP and CBD international agreements, and Elizabeth to avoid helicopter research detailing the participation and recognition Rovere for graphical suggestions. of all the members involved in the project. The standardization will facilitate the process of sample acquisition for researchers while AUTHOR CONTRIBU TIONS ensuring intellectual contribution, recognition and transfer of techni- L.B. planned and designed the research. A.I. and L.B. revised the scien- cal and scientific expertise to researchers in the provider country of tific literature and conducted the research of the current international the samples. An example of access standardization is provided by the agreements. A.I. and L.B. wrote the manuscript. multilateral ABS system and standard material transfer agreements of the International Treaty on Plant Genetic Resources for Food and FUNDING INF ORMATI ON Agriculture (2001) (Rourke, 2018).  n y Cajal A.I. is a FPI fellow (PRE2018-083529). L. B is a Ramo Fellow. (RYC2018-024770-I) both fellowships funded by the n—Agencia Estatal de Investigacio Ministerio de Ciencia e Innovacio n/ 6 | C O N CL U S I O N S Fondo Social Europeo. We acknowledge financial support from the Spanish Ministry of Science and Innovation-State Research Agency An appropriate legal framework for crop archaeogenomic studies is of (AEI), through the “Severo Ochoa Programme for Centres of particular importance because the current situation promotes the use Excellence in R&D” SEV-2015-0533 and CEX2019-000902-S. This of plant remains that are not subject to the NP or a national law regu- work was also supported by the CERCA programme by the lating genetic resources. This is even more true because the distribu- Generalitat de Catalunya. tion of archaeological remains is unbalanced between the Global North and the Global South, the former counting on extensive collec- DATA AVAILABILITY STAT EMEN T tions of foreign specimens that predate international agreements. In Data sharing not applicable - no new data generated, or the article some instances, this implies the total exclusion of the provider coun- describes entirely theoretical research try in the research study, and therefore the impossibility of sharing the benefits of the ongoing research. OR CID Care must be taken, however, to avoid mere testimonial participa- Alice Iob https://orcid.org/0000-0002-7505-3612 tion by the provider country, and agreements made between the Laura Botigué https://orcid.org/0000-0001-7114-5168 25722611, 2022, 1, Downloaded from https://nph.onlinelibrary.wiley.com/doi/10.1002/ppp3.10233 by Readcube (Labtiva Inc.), Wiley Online Library on [25/05/2023]. 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  IOB AND BOTIGUE 49 RE FE R ENC E S Improved recovery of ancient DNA from subfossil wood—Application Bardill, B. J., Bader, A. C., Garrison, N. A., Bolnick, D. A., Raff, J. A., & to the world's oldest late glacial pine forest. The New Phytologist, Walker, A. (2018). Advancing the ethics of palaeogenomics. 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