Low degree of domestication can be an indicator of high potential of biological invasion

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Dechoum, Carolina Levis, Gustavo Lemes, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-5362570/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract The degree of domestication can influence the ability of introduced species to survive and reproduce. Species with higher degrees of domestication are highly dependent on humans for survival and reproduction. On the other hand, lower degrees may result in lower survival rates and reproduction output. However, the interrelationship between degrees of domestication and plant invasion remains underexplored. We focused our study on plant species native to the Americas with distinct degrees of domestication, with fruits used for human consumption, to test the hypothesis that plants with intermediate degrees of domestication show higher invasion potential than plants with lower or higher degrees of domestication. We calculated an invasion potential index as the ratio between the number of checklists where an introduced species was recorded as invasive and the total number of checklists where it was registered as introduced. Our results show a negative non-linear relationship between the degree of domestication and invasion potential. While species with intermediate degrees of domestication show higher invasion potential than those fully domesticated, species with the lowest degrees of domestication showed the highest invasion potential. These findings suggest that full domestication does not eliminate invasion risk, highlighting the complexity of the relationship between domestication and invasion. Our results provide valuable insights to support public policies, inform future studies on plant invasions, and the need for management strategies that consider different degrees of domestication. invasive species management non-native species domestication syndrome human-mediated dispersal invasiveness Figures Figure 1 Figure 2 1 Introduction The domestication of plants is a complex mutualistic and co-evolutionary process that has selected and transformed populations of wild species into populations highly adapted to human habitats (Purugganan 2019 ; Clement et al. 2021 ). Over time, humans have utilized and transported these valuable plants, intensifying the selection of desirable phenotypic traits (Van Kleunen et al. 2018 ; Fuller et al. 2023 ). With globalization, the scale of this movement has exponentially increased, leading to the introduction of numerous non-native species into new environments (Meyerson and Mooney 2007 ). This marks a critical point in the history of biodiversity and biological invasions, especially considering that biological invasions constitute one of the greatest threats to global biodiversity and human well-being (Roy et al. 2024 ). However, the interrelationship between domestication and plant invasion remains underexplored, particularly considering the correlation between invasion potential and different degrees of domestication. There are several barriers that introduced species need to overcome before they become invasive, including the capacity to survive in new environmental conditions and to disperse and establish new self-sustainable populations (Blackburn et al. 2011 ). The changes caused by the domestication process can facilitate or hinder different steps of the invasion process (Petri et al. 2021 ). The introduction of domesticated species is usually intentional, with the species being pre-adapted to human-made environments due to human selection. The faster transport of a greater number of propagules facilitates biological invasions (Petri et al., 2021 ). Furthermore, traits such as high dispersal ability, adaptation to a wide range of environmental conditions (phenotypic plasticity), and resistance to pests and pathogens can enhance invasion risk (Petri et al. 2021 ). On the other hand, some studies have assumed that domestication reduces the risk of invasion (Gordon et al. 2010 ; Petri et al. 2021 ). This is based on several domesticated plants that lose their reproduction ability without interaction with humans and become highly dependent on human management in human-made environments (Clement et al. 2017 ). This dependency can reduce invasion potential by limiting dispersal and establishment in new environments (Petri et al. 2021 ). Although there has been an inconclusive discussion about the relationship between domestication and invasion, the degrees of domestication have not been considered so far. Compared to wild populations, artificially selected populations may vary in a domestication gradient from wild to fully domesticated plant populations, with some intermediate degrees of domestication (Clement 1999a ). Degrees of domestication can also be assessed as a domestication gradient in a quantitative way (Lemes 2021 ). These degrees significantly influence the ability of plant populations to establish in areas outside cultivation (Clement et al. 2017 ). While fully domesticated plants are highly dependent on human care, which makes it difficult to establish individuals/populations outside cultivation, plants with lower degrees of domestication (wild, incipient, and semi-domesticated) can establish new plants outside cultivated areas. This ability to establish new individuals/populations may be due to the retention of the capacity of ecological adaptation (Clement 1999a ) but also due to hybridization with local wild plants (Miller and Gross 2011 ). In this sense, invasion success can differ for introduced plant populations with different degrees of domestication. Around 2,500 plant species are believed to have been in some way domesticated globally (Meyer et al. 2012 ). In the Neotropics, more than 6,500 native plant species have been managed and used in different regions, and thousands have been cultivated, suggesting interactions that had resulted in populations at least incipient domesticated (Clement et al. 2021 ). Among these, there is a great diversity of species domesticated because of their fruits, such as palm trees and perennial fruit trees from the Amazon region [ e.g. açaí ( Euterpe precatoria ) and patauá ( Oecnocarpus bataua )] (Clement et al. 2021 ). The phenotypic changes selected in plant populations with edible fruits due to domestication, often described as domestication syndromes (Miller and Gross 2011 ), include larger fruit size (Miller and Gross 2011 ; Clement et al. 2017 ), variations in fruit color and taste (Purugganan 2019 ), and changes in seed structure and physiology, such as reduced toxicity, increased oil content, and reduced dormancy (Miller and Gross 2011 ). Some changes in reproductive strategies are also significant, such as vegetative propagation (Meiri and Bar-Oz 2024 ), development of parthenocarpic fruit development (without fertilization), and self-pollination (Miller and Gross 2011 ). Many of these changes may also increase the invasion potential. For example, fruits selected to be more palatable to humans or plants with prolific seed production are likely to become more attractive to wildlife dispersers in the environments where they have been introduced (Buckley et al. 2006 ), which can directly help to overcome the dispersal barrier of the invasion process (introduction - establishment - dispersal continuum) (Traveset and Richardson 2011 , 2014 ). Plants with fleshy fruits play a significant role in ecosystems by providing food for wildlife and humans and are crucial for food security, nutrition, and the global economy (Bvenura and Sivakumar 2017 ). In the Americas, there are crucial centers of plant domestication (Larson et al. 2014 ), with many fruit plant species known to be useful for human consumption (Clement et al. 2010 ; 2021 ; Casas et al. 2019 ). Notable domesticated fruit plants from this region, such as guava ( Psidium guajava ) (Landrum 2021 ) and Brazilian pepper tree ( Schinus terebinthifolia ) (Freitas et al. 2020 ), are considered invasive in several regions worldwide. Understanding their invasion potential can help protect agricultural resources and ensure sustainable production, helping to predict and manage ecological disruptions caused by invasive species. Therefore, it is imperative to investigate the relationship between invasion and domestication of these important plants native to the Americas. The main aim of this study was to assess the relationship between degree of domestication and invasion potential in domesticated native plants whose fruits have been used for human consumption in the Americas. We hypothesized that species with intermediate degrees of domestication are more likely to be recorded as invasives than species with lower or higher degrees of domestication due to phenotypic changes that enhance invasion potential without complete dependence on human care. 2 Methods 2.1 Data collection We used a list of 340 native plant species that have undergone the domestication process in the Americas, with their respective degrees of domestication qualitatively and quantitatively developed by Lemes ( 2021 ). The degrees of domestication range from 1 to 15 and are divided qualitatively into managed wild (0–5), incipiently domesticated (6–7), semi-domesticated (8–10), and domesticated (11–15). The calculation of this index was based on five traits representing domestication patterns, which are the result of seven management and use processes documented in the literature (Lemes 2021 ). Each of these patterns and processes was categorized for each species on a binary scale of presence (1) or absence (0), generating a quantitative value representing each species' domestication degree. To obtain a list of the native plants of the Americas with fruits used for human consumption, we used the database of useful neotropical plants, called Useflora ( https://useflora.ufsc.br/ ) (Ferrari 2020 ; Clement et al. 2021 ). The filters used were: part used = fruit; type of use = food use. In addition, we used the fruit species described in the book by Patiño ( 2002 ). Data processing resulted in 467 plant species with native plants of the Americas with fruits used for human consumption. For quantitative data on the occurrence of invasions, we used global data on the occurrence of invasions by plants through 197 checklists available on the Global Register of Introduced and Invasive Species (GRIIS) (Pagad et al. 2018 ). The filters used were: Plantae Kingdom and True Species. This resulted in a total of 13,249 introduced and/or invasive plant species worldwide. The three species lists had their scientific names corrected and standardized according to the WorldFlora Online package WorldFlora 2023.03 version (Kindt 2020 ). After correcting the nomenclature of the species, the lists were manually compared, resulting in a list of 125 species of plants with fruits useful for human consumption that have information on their degree of domestication (Table S1 , supplementary material). From these, we extracted only the species that had records of occurrence as introduced and/or invasive. For these species, we calculated an invasion potential index (IP) using the ratio between the number of checklists in which the species occurred as an invader and the total number of checklists in which it is present (introduced), using the formula below: $$\:IP=\frac{number\:as\:invasive}{total\:number\:of\:introductions}$$ 2.2 Data analysis To investigate the factors associated with the invasion potential (IP) of each species, we fitted a generalized linear model (GLM) using the stats package in the R software (R Core Team 2023 ). We used the Invasion Potential index (IP) as the dependent variable and degrees of domestication (degree) as the independent variable. Due to the nature of the data, as a numerical vector with values between 0 and 1, interpreted as the proportion of successful cases, we used the quasibinomial family (R Core Team 2023 ). We incorporated the total number of introductions as an offset, as an a priori known component in the linear predictor during fitting. To validate the model, we assessed the normality and homoscedasticity of the residuals. 3 Results Of the 125 species with fruits for human consumption that presented information on domestication, 74 were introduced outside their natural range (59.2%), and of these, 33 are invasive in at least one checklist (26.4%, Fig. 1 ). A total of 41 domesticated species and those introduced elsewhere did not show any occurrences as invaders (Figure S1 , supplementary material). The most introduced species were Psidium guajava (93 checklists), Jatropha curcas (93 checklists) and Physalis peruviana (74 checklists). The species with the highest occurrence as invaders were Psidium guajava (31 checklists), Eugenia uniflora (14 checklists) and Jatropha curcas (12 checklists) (Table 1). Passiflora alata (IP = 0.50), Eugenia uniflora (IP = 0.37) were the species with the greatest invasion potential, followed by Psidium guajava , Schinus terebinthifolia , Chrysobalanus icaco , Pouteria campechiana and Diospyros virginiana (IP = 0.33 for all of them). All categorical degrees of domestication showed occurrences of invasion (Fig. 1 ). The majority of species that have occurrences as invaders in at least one checklist are from the fully domesticated class (n = 15 species, Fig. 1 ), followed by semi-domesticated (n = 10 species, Fig. 1 ), incipient (n = 5 species, Fig. 1 ), and wild (n = 3 species, Fig. 1 ). We found a non-linear negative correlation between the degree of domestication and invasion potential (t=-4.362, p < 0.005), with an apparent decrease in invasion potential as the degree of domestication increases (Fig. 2 ). The reduction in the invasion potential is more pronounced for the degrees of wild and incipient domestication compared to the degrees of semi- and fully domesticated (Fig. 2 ). 4 Discussion The Invasion potential index (IP) of plants with fruit used for human consumption varied according to the degree of domestication. Our hypothesis was not corroborated given that species with intermediate degrees of domestication only showed higher invasion potential than species with higher degree of domestication. We observed a decline of the potential for invasion along the domestication gradient and although fully domesticated plant species have lower invasion potential, they comprehend the majority of species that have occurrences as invaders. This finding suggests that even fully domestication of plants with fruits used for human consumption does not eliminate the invasion risk for some species. Interesting results emerged about the relationship between these two processes that can support public policies and provide suggestions for future studies. No degree of domestication was entirely free from having at least one invasive population, contrary to what was expected based on the literature (see Clement 1999a ; Clement et al. 2017 ). This indicates that some plants with intermediated (incipient and semi) and others considered with high degrees of domestication do not lose their ecological adaptability and can persist without human care. This is evidenced by species such as Psidium guajava and 14 other fully domesticated species that are invasive somewhere (Fig. 1 ). Although it is expected that domesticated species have low genetic variation due to genetic bottlenecks (Miller and Gross 2011 ), Clement ( 1999a ) defines some fully domesticated species as " landraces ," which are populations selected in a cultivated landscape within a restricted geographical region with high phenotypic variability and relatively high genetic variability (Clement et al. 1999a). In particular, domesticated populations of perennial fruit crops maintain a large part of the total genetic variation of the species (Miller and Gross 2011 ). Genetic variation can reflect high phenotypic plasticity in some fully domesticated plants and can be key for invasion success. Phenotypic plasticity is crucial for colonization of new environments (Gering et al 2019 ), being an important factor when species are being selected for domestication (Mueller et al. 2023 ) as well as for the success of biological invasions (Daly et al. 2023 ). Phenotypic plasticity allows plants to reacquire adaptive wild characteristics and survive without human intervention. This process, known as de-domestication or feralization, is an evolutionary phenomenon where domesticated crops regain wild-like traits and form independent reproducing populations, escaping intensive human management (Wu et al. 2021 ). As emphasized by Sun et al. ( 2022 ), domestication is not a one-way road. Domestication can increase the invasion potential of plant species, as it combines resistance acquired along the process with the robustness of wild species. De-domestication could explain why some fully domesticated plants exhibit high invasion potential, emphasizing the need for continuous monitoring of these species. Thus, we highlight the importance of deepening these studies for de-domestication and invasion. The plant species with fleshy fruits more frequently recorded as introduced were also more frequently recorded as invasive, as for Psidium guajava (93 checklists) and Jatropha curcas (93 checklists). This can be considered a consequence of repeated introductions in different regions, which make it possible for the species to be present in several checklists. Repeated introductions in the same region result in high propagule pressure, which can increase the likelihood of survival of individuals and establishment of populations (Simberloff 2009 ; Duncan 2011 ). High propagule pressure also increases genetic diversity for populations and promotes gene admixture, thus increasing the adaptive potential of non-native populations, and ultimately the probability of successful introduction (Daly et al. 2023 ). This gene admixture forms intraspecific hybrids between lineages that have been isolated (Gaskin 2017 ). Globalization has provided opportunities for hybridization (Chornesky and Randall 2003 ). One example is the plant Brazilian peppertree (Schinus terebinthifolia ), one of the species with the greatest invasion potential in our study (IP = 0.33). Native to South America and invasive in the USA, this species formed hybrids from two different Brazilian lineages. These hybrids seem to be more resistant to certain biological control agents, exhibit greater vigor, with 45% more seedlings established compared to the original plants (Geiger et al. 2011 ) and have an increased ability of colonizing new areas (Gaskin 2016). Interspecific hybridization is another important process in the success of biological invasions (Daly et al. 2023 ) and seems to be an important mechanism for adaptive evolution in several crop-domesticated species (Purugganan 2019 ). Species transported by humans to new areas are subject to hybridization with wild species (exoferal ancestry, Ellstrand et al. 2010 ), which can facilitate the establishment and invasion by introduced species (Harrison and Larson 2014 ; Purugganan 2019 ). This suggests that if the introduced species contacts closely-related native species in the new area, the non-native species may be favored, while the native species could be threatened by direct competition or a loss of genetic diversity. Psidium guajava (guava) is the most frequently introduced species in our study, with the highest number of invasive records and showing a high invasion potential (IP = 0.33). Hybridization between P. guajava and other Psidium species is a real possibility (Gomes et al. 2017 ), as evidenced by reported cases of hybridization between P. guajava and P. guineense in Mexico, Honduras and Argentina (Landrum et al. 1995 ). In Ecuador, on the Galapagos islands, the distribution of P.guajava overlaps with the endemic Psidium galapageium , raising concerns about potential hybridization and competition (Urquía et al. 2019 ; Reatini et al. 2022 ). Similar situation occurred in Mexico with the hybridization of Psidium socorrense (López-Caamal et al. 2014 ). Although hybridization between P. guajava and P. galapageium has not yet been confirmed, the risk persists, making future studies crucial to understand its potential impact (Urquía et al. 2019 ). That said, we highlight that the presence of native species that are close relatives to introduced species must be considered in prevention tools for the intentional introduction of species such as risk analysis, in order to avoid negative impacts due to hybridization with the native flora. A possible key component to the invasion of plants with fruits domesticated for human consumption is that many of these plants may not have lost their seed dispersal capability. Many of the progenitors of modern domesticated crops relied on animals for seed dispersal and most are fleshy fruits, which represent evolutionary adaptations for seed dispersal with animals as vectors (Spengler 2020 ). Domesticated fruits are very attractive on the landscape, as increases in pericarp tissue and sugar concentrations are among the basic traits of domestication in fruit plants (Miller and Gross 2011 ). These fruits are available to both humans and animals, which can consume and disperse the seeds, facilitating their spread to areas far from the introduction site and outside of cultivation zones, thereby increasing the chances of germination and invasion (Petri et al. 2021 ). Additionally, the establishment of these frugivory interactions can be facilitated if the non-native plant presents fleshy fruits with small seeds, high energy content and fruiting phenologies at different times compared to native species (Richardson et al. 2000; Gosper et al. 2005 ). Domesticated species are often adapted to anthropogenic environments (Clement et al. 2021 ), which may give them an advantage in disturbed or human-made ecosystems. Ecosystem degradation further facilitates the invasion of many non-native plants by altering species distributions and resource dynamics within ecosystems (Buckley et al. 2006 ; Feng et al. 2022 ). It is likely that the general attractiveness of these fruits to local fauna, combined with the decreasing availability of native fruits in highly fragmented landscapes, promotes generalist frugivorous to feed on what is available and most accessible (Gosper et al. 2005 ; Siegel et al. 2024 ). We detail some of the species that stood out for their invasion potential along with information regarding its use, seed dispersal, type of fruit, and natural history (Box 1). Our study has some limitations that should be considered and may guide future studies. First, the scope of the study was restricted to the Americas and to plants with fruit used for human consumption, which may limit the generalizability of the results to other regions and types of plant use. However, we consider that the geographical extension and relevance of the Americas regarding species domestication and biological invasions enables us to extrapolate our results and conclusions to other regions. Second, domestication and invasion may be different for perennial and annual plants because these plants differ in terms of genetic variation and rates of evolution (Miller and Groos 2011), and we did not make this distinction in this study. Third, we used the available information on occurrences of invasion, but this does not imply that all species are absent in other areas that are data deficient. There are significant gaps in information regarding occurrences, assessments of whether species are invasive, the dates of their first records, and the pathways involved (IPBES 2023 ). Finally, the available databases did not allow us to distinguish degrees of domestication between different plant populations. This intrinsic variation could provide additional insights into the relationship between domestication and invasion. Future studies can address these limitations as well as include functional traits in order to assess the altered characteristics that can facilitate or hinder biological invasions. Conclusions This study highlights the complexity and multifaceted nature of two important processes mediated by humans, occurring at the plant population level: plant domestication and biological invasions. We provide a general overview of the global situation of biological invasions caused by plants with a history of domestication in the Americas. We showed that domestication degree can have an influence on invasion potential. Full domestication seems to reduce the invasion potential but does not eliminate completely the invasion risk, given the continued persistence and adaptability to human-dominated landscapes of species such as Psidium guajava . New studies are necessary to investigate the determination of the invasion potential of these species based on the interplay between domestication, genetic diversity, phenotypic plasticity, and seed dispersal mechanisms. Declarations Conflict of Interest The authors declare that the research was conducted in the absence of any conflict of interest. Author Contributions All authors contributed to the study conception and design. Brisa Marciniak, Nivaldo Peroni, and Michele de Sa Dechoum originally formulated the idea. Material preparation, data collection and analysis were performed by Brisa Marciniak. The first draft of the manuscript was written by Brisa Marciniak and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript. Funding This study was funded in part by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brasil (CAPES)—Finance Code 001. Competing Interests The authors have no relevant financial or non-financial interests to disclose. Data Availability Not applicable. References Achten WM, Nielsen LR, Aerts R et al (2010) Towards domestication of Jatropha curcas. Biofuels 1(1):91-107. https://doi.org/10.4155/bfs.09.4 Arévalo-Marín E, Casas A, Alvarado-Sizzo H et al (2024) Genetic analyses and dispersal patterns unveil the Amazonian origin of guava domestication. 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Am J Bot 98(9):1389–1414. https://doi.org/10.3732/ajb.1000522 Mueller NG, Horton ET, Belcher ME, Kistler L (2023) The taming of the weed: Developmental plasticity facilitated plant domestication. PLoS One 18(4):e0284136. https://doi.org/10.1371/journal.pone.0284136 Pagad S, Genovesi P, Carnevali L, Schigel D, McGeoch MA (2018) Introducing the global register of introduced and invasive species. Sci Data 5(1):1–12. https://doi.org/10.1038/sdata.2017.202 Patiño VM (2002) Historia y dispersión de los frutales nativos del Neotrópico. Centro Internacional de Agricultura Tropical, Cali Petri T, Canavan S, Gordon DR, Lieurance D, Flory SL (2021) Potential effects of domestication on non-native plant invasion risk. Plant Ecol 222(5):549–559. https://doi.org/10.1007/s11258-021-01130-8 Purugganan MD (2019) Evolutionary insights into the nature of plant domestication. Curr Biol 29(14):R705-R714. https://doi.org/10.1016/j.cub.2019.05.053 Pyšek P, Křivánek M, Jarošík V (2009) Planting intensity, residence time, and species traits determine invasion success of alien woody species. Ecology 90(10):2734–2744. https://doi.org/10.1890/08-0857.1 R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at https://www.R-project.org/. Reatini B, Lourdes Torres M, Vision TJ (2022) Local exclusion and regional decline of an endemic Galápagos tree species (Psidium galapageium) by an invasive relative (P. guajava). bioRxiv https://doi.org/10.1101/2022.10.11.511772 Richardson DM, Pyšek P (2006) Plant invasions: merging the concepts of species invasiveness and community invasibility. Prog Phys Geogr 30(3):409–431. https://doi.org/10.1191/0309133306pp490pr Roy HE, Pauchard A, Stoett PJ, Renard Truong T, Meyerson LA, Bacher S et al (2024) Curbing the major and growing threats from invasive alien species is urgent and achievable. Nat Ecol Evol:1–8. https://doi.org/10.1038/s41559-024-02412-w Siegel TD, Cooper WJ, Forkner RE, Laurance WF, Luís Camargo J, Luther D (2024) Forest fragmentation effects on mutualistic interactions: frugivorous birds and fruiting trees. Oikos 2024(10): e10383. https://doi.org/10.1111/oik.10383 Simberloff D (2009) The role of propagule pressure in biological invasions. Annu Rev Ecol Evol Syst 40(1):81–102. https://doi.org/10.1146/annurev.ecolsys.110308.120304 Spengler RN (2020) Anthropogenic seed dispersal: rethinking the origins of plant domestication. Trends Plant Sci 25(4):340–348. https://doi.org/10.1016/j.tplants.2020.01.005 Sun Y, Guo L, Zhu QH, Fan L (2022) When domestication bottleneck meets weed. Mol Plant 15(9):1405–1408. https://doi.org/10.1016/j.molp.2022.08.002 Thomas R, Sah NK, Sharma P (2008) Therapeutic biology of Jatropha curcas: a mini review. Curr Pharm Biotechnol 9(4):315–324. https://doi.org/10.2174/138920108785161505 Traveset A, Richardson DM (2011) Mutualisms: key drivers of invasions… key casualties of invasions. In: Richardson DM (ed) Fifty Years of Invasion Ecology. The Legacy of Charles Elton. Wiley-Blackwell, Oxford, pp 143–160 Traveset A, Richardson DM (2014) Mutualistic interactions and biological invasions. Annu Rev Ecol Evol Syst 45(1):89–113. https://doi.org/10.1146/annurev-ecolsys-120213-091857 Urquía D, Gutierrez B, Pozo G, Pozo MJ, Espín A, Torres MDL (2019) Psidium guajava in the Galapagos Islands: population genetics and history of an invasive species. PLoS One 14(3): e0203737. https://doi.org/10.1371/journal.pone.0203737 Van Kleunen M, Essl F, Pergl J et al (2018) The changing role of ornamental horticulture in alien plant invasions. Biol Rev 93(3):1421–1437 https://doi.org/10.1111/brv.12402 Wu D, Lao S, Fan L (2021) De-domestication: an extension of crop evolution. Trends Plant Sci 26(6):560–574. https://doi.org/10.1016/j.tplants.2021.02.003 Box 1 Box 1 is available in the Supplementary Files section. Additional Declarations No competing interests reported. Supplementary Files Box1.docx Suplementarymaterial.docx Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-5362570","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":376642129,"identity":"0091a6d2-4e7e-42f1-9f4a-79f9ea236ebe","order_by":0,"name":"Brisa Marciniak","email":"data:image/png;base64,iVBORw0KGgoAAAANSUhEUgAAAZAAAAAyAQMAAABI0h/eAAAABlBMVEX///8AAABVwtN+AAAACXBIWXMAAA7EAAAOxAGVKw4bAAAA+UlEQVRIiWNgGAWjYBACAwbGBgiLmYHhAMMBGyCLsfEAKVrSQFoaCGhBAQcOQyh8WsylDzd/+Jljl8/fznvwwI8z5+3Wth8G2lJjE41Li2VfYptk77ZkyxmH+RIO9ty4nbztTCJQy7G03AZcDjvD2MbAu43ZwICZx+AAz4fbyWYHgFoYGw7j09L88e+2erCWg38+nEs2O/+QoJYGad5th8FaDvPcOGBndoOALZY9jG3SstuOG0gcBmqROZOcYHYDaEsCHr+Y87A//vh2W7UBf/8Z449vjtnZm51Pf/jgQ40NTi0YIBGsMoFY5SBgT4riUTAKRsEoGBkAAAGcZxRVigNGAAAAAElFTkSuQmCC","orcid":"","institution":"Universidade Federal de Santa Catarina","correspondingAuthor":true,"submittingAuthor":false,"prefix":"","firstName":"Brisa","middleName":"","lastName":"Marciniak","suffix":""},{"id":376642132,"identity":"99fac238-2a1f-411c-8936-ac596296b52e","order_by":1,"name":"Michele S. Dechoum","email":"","orcid":"","institution":"Universidade Federal de Santa Catarina","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Michele","middleName":"S.","lastName":"Dechoum","suffix":""},{"id":376642136,"identity":"c8c2e963-6bf6-48df-b9e5-0a4a4dcad03b","order_by":2,"name":"Carolina Levis","email":"","orcid":"","institution":"Universidade Federal de Santa Catarina","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Carolina","middleName":"","lastName":"Levis","suffix":""},{"id":376642138,"identity":"2cf96469-f621-4f09-a449-4e3910bc3b28","order_by":3,"name":"Gustavo Lemes","email":"","orcid":"","institution":"Universidade Federal de Santa Catarina","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Gustavo","middleName":"","lastName":"Lemes","suffix":""},{"id":376642141,"identity":"dba1ffd3-e6eb-4710-8289-5362ee291ca7","order_by":4,"name":"Nivaldo Peroni","email":"","orcid":"","institution":"Universidade Federal de Santa Catarina","correspondingAuthor":false,"submittingAuthor":false,"prefix":"","firstName":"Nivaldo","middleName":"","lastName":"Peroni","suffix":""}],"badges":[],"createdAt":"2024-10-30 16:53:13","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-5362570/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-5362570/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":68941953,"identity":"a2d34345-e704-47b7-b905-a2c1801e34a9","added_by":"auto","created_at":"2024-11-13 18:13:23","extension":"png","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":11192286,"visible":true,"origin":"","legend":"\u003cp\u003ePlants with occurrences of invasive populations (orange) and their total number of presences in checklists (blue). The domestication degree is shown accordingly: W (wild), I (incipient), SD (semi-domesticated), and F (fully). Species are organized by decreasing invasion potential (IP), with the calculated IP index indicated in orange above the bars.\u003c/p\u003e","description":"","filename":"1.png","url":"https://assets-eu.researchsquare.com/files/rs-5362570/v1/dd1f48ca692f9b1e106ca9ad.png"},{"id":68941950,"identity":"f3f55b87-b06b-4e72-a599-4ac84d7d21da","added_by":"auto","created_at":"2024-11-13 18:13:23","extension":"png","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":35824,"visible":true,"origin":"","legend":"\u003cp\u003eInvasion potential according to the domestication gradient. The degrees of domestication range from 1 to 15 and are divided qualitatively into managed wild (0-5), incipiently domesticated (6-7), semi-domesticated (8-10), and domesticated (11-15) by Lemes (2021).\u003c/p\u003e","description":"","filename":"2.png","url":"https://assets-eu.researchsquare.com/files/rs-5362570/v1/d17c9521c1fb8b14295daf2c.png"},{"id":70515438,"identity":"df54c4a1-9dbb-4b33-bba0-82a0f338e8d1","added_by":"auto","created_at":"2024-12-04 02:17:06","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":11902594,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-5362570/v1/0e734ea3-e6b2-43cd-8d5b-84ce47b00361.pdf"},{"id":68941952,"identity":"730dab19-8251-4c01-b637-a04ebf9fcacc","added_by":"auto","created_at":"2024-11-13 18:13:23","extension":"docx","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":145072,"visible":true,"origin":"","legend":"","description":"","filename":"Box1.docx","url":"https://assets-eu.researchsquare.com/files/rs-5362570/v1/671314aa4af66aaf19875c9e.docx"},{"id":68941951,"identity":"8e927424-55f3-447a-9f0f-28633506c060","added_by":"auto","created_at":"2024-11-13 18:13:23","extension":"docx","order_by":5,"title":"","display":"","copyAsset":false,"role":"supplement","size":87394,"visible":true,"origin":"","legend":"","description":"","filename":"Suplementarymaterial.docx","url":"https://assets-eu.researchsquare.com/files/rs-5362570/v1/31bcd0c22713725a6c77f7a1.docx"}],"financialInterests":"No competing interests reported.","formattedTitle":"Low degree of domestication can be an indicator of high potential of biological invasion","fulltext":[{"header":"1 Introduction","content":"\u003cp\u003eThe domestication of plants is a complex mutualistic and co-evolutionary process that has selected and transformed populations of wild species into populations highly adapted to human habitats (Purugganan \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Clement et al. \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Over time, humans have utilized and transported these valuable plants, intensifying the selection of desirable phenotypic traits (Van Kleunen et al. \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Fuller et al. \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). With globalization, the scale of this movement has exponentially increased, leading to the introduction of numerous non-native species into new environments (Meyerson and Mooney \u003cspan citationid=\"CR42\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). This marks a critical point in the history of biodiversity and biological invasions, especially considering that biological invasions constitute one of the greatest threats to global biodiversity and human well-being (Roy et al. \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). However, the interrelationship between domestication and plant invasion remains underexplored, particularly considering the correlation between invasion potential and different degrees of domestication.\u003c/p\u003e \u003cp\u003eThere are several barriers that introduced species need to overcome before they become invasive, including the capacity to survive in new environmental conditions and to disperse and establish new self-sustainable populations (Blackburn et al. \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). The changes caused by the domestication process can facilitate or hinder different steps of the invasion process (Petri et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The introduction of domesticated species is usually intentional, with the species being pre-adapted to human-made environments due to human selection. The faster transport of a greater number of propagules facilitates biological invasions (Petri et al., \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Furthermore, traits such as high dispersal ability, adaptation to a wide range of environmental conditions (phenotypic plasticity), and resistance to pests and pathogens can enhance invasion risk (Petri et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). On the other hand, some studies have assumed that domestication reduces the risk of invasion (Gordon et al. \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Petri et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). This is based on several domesticated plants that lose their reproduction ability without interaction with humans and become highly dependent on human management in human-made environments (Clement et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). This dependency can reduce invasion potential by limiting dispersal and establishment in new environments (Petri et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2021\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eAlthough there has been an inconclusive discussion about the relationship between domestication and invasion, the degrees of domestication have not been considered so far. Compared to wild populations, artificially selected populations may vary in a domestication gradient from wild to fully domesticated plant populations, with some intermediate degrees of domestication (Clement \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e1999a\u003c/span\u003e). Degrees of domestication can also be assessed as a domestication gradient in a quantitative way (Lemes \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). These degrees significantly influence the ability of plant populations to establish in areas outside cultivation (Clement et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). While fully domesticated plants are highly dependent on human care, which makes it difficult to establish individuals/populations outside cultivation, plants with lower degrees of domestication (wild, incipient, and semi-domesticated) can establish new plants outside cultivated areas. This ability to establish new individuals/populations may be due to the retention of the capacity of ecological adaptation (Clement \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e1999a\u003c/span\u003e) but also due to hybridization with local wild plants (Miller and Gross \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). In this sense, invasion success can differ for introduced plant populations with different degrees of domestication.\u003c/p\u003e \u003cp\u003eAround 2,500 plant species are believed to have been in some way domesticated globally (Meyer et al. \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2012\u003c/span\u003e). In the Neotropics, more than 6,500 native plant species have been managed and used in different regions, and thousands have been cultivated, suggesting interactions that had resulted in populations at least incipient domesticated (Clement et al. \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Among these, there is a great diversity of species domesticated because of their fruits, such as palm trees and perennial fruit trees from the Amazon region [\u003cem\u003ee.g.\u003c/em\u003e a\u0026ccedil;a\u0026iacute; (\u003cem\u003eEuterpe precatoria\u003c/em\u003e) and patau\u0026aacute; (\u003cem\u003eOecnocarpus bataua\u003c/em\u003e)] (Clement et al. \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The phenotypic changes selected in plant populations with edible fruits due to domestication, often described as domestication syndromes (Miller and Gross \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), include larger fruit size (Miller and Gross \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Clement et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), variations in fruit color and taste (Purugganan \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), and changes in seed structure and physiology, such as reduced toxicity, increased oil content, and reduced dormancy (Miller and Gross \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Some changes in reproductive strategies are also significant, such as vegetative propagation (Meiri and Bar-Oz \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2024\u003c/span\u003e), development of parthenocarpic fruit development (without fertilization), and self-pollination (Miller and Gross \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Many of these changes may also increase the invasion potential. For example, fruits selected to be more palatable to humans or plants with prolific seed production are likely to become more attractive to wildlife dispersers in the environments where they have been introduced (Buckley et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2006\u003c/span\u003e), which can directly help to overcome the dispersal barrier of the invasion process (introduction - establishment - dispersal continuum) (Traveset and Richardson \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2011\u003c/span\u003e, \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e2014\u003c/span\u003e).\u003c/p\u003e \u003cp\u003ePlants with fleshy fruits play a significant role in ecosystems by providing food for wildlife and humans and are crucial for food security, nutrition, and the global economy (Bvenura and Sivakumar \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). In the Americas, there are crucial centers of plant domestication (Larson et al. \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2014\u003c/span\u003e), with many fruit plant species known to be useful for human consumption (Clement et al. \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2021\u003c/span\u003e; Casas et al. \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Notable domesticated fruit plants from this region, such as guava (\u003cem\u003ePsidium guajava\u003c/em\u003e) (Landrum \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e2021\u003c/span\u003e) and Brazilian pepper tree (\u003cem\u003eSchinus terebinthifolia\u003c/em\u003e) (Freitas et al. \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2020\u003c/span\u003e), are considered invasive in several regions worldwide. Understanding their invasion potential can help protect agricultural resources and ensure sustainable production, helping to predict and manage ecological disruptions caused by invasive species. Therefore, it is imperative to investigate the relationship between invasion and domestication of these important plants native to the Americas.\u003c/p\u003e \u003cp\u003eThe main aim of this study was to assess the relationship between degree of domestication and invasion potential in domesticated native plants whose fruits have been used for human consumption in the Americas. We hypothesized that species with intermediate degrees of domestication are more likely to be recorded as invasives than species with lower or higher degrees of domestication due to phenotypic changes that enhance invasion potential without complete dependence on human care.\u003c/p\u003e"},{"header":"2 Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003e2.1 Data collection\u003c/h2\u003e \u003cp\u003eWe used a list of 340 native plant species that have undergone the domestication process in the Americas, with their respective degrees of domestication qualitatively and quantitatively developed by Lemes (\u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The degrees of domestication range from 1 to 15 and are divided qualitatively into managed wild (0\u0026ndash;5), incipiently domesticated (6\u0026ndash;7), semi-domesticated (8\u0026ndash;10), and domesticated (11\u0026ndash;15). The calculation of this index was based on five traits representing domestication patterns, which are the result of seven management and use processes documented in the literature (Lemes \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Each of these patterns and processes was categorized for each species on a binary scale of presence (1) or absence (0), generating a quantitative value representing each species' domestication degree.\u003c/p\u003e \u003cp\u003eTo obtain a list of the native plants of the Americas with fruits used for human consumption, we used the database of useful neotropical plants, called Useflora (\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://useflora.ufsc.br/\u003c/span\u003e\u003cspan address=\"https://useflora.ufsc.br/\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e) (Ferrari \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Clement et al. \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). The filters used were: part used\u0026thinsp;=\u0026thinsp;fruit; type of use\u0026thinsp;=\u0026thinsp;food use. In addition, we used the fruit species described in the book by Pati\u0026ntilde;o (\u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2002\u003c/span\u003e). Data processing resulted in 467 plant species with native plants of the Americas with fruits used for human consumption.\u003c/p\u003e \u003cp\u003eFor quantitative data on the occurrence of invasions, we used global data on the occurrence of invasions by plants through 197 checklists available on the Global Register of Introduced and Invasive Species (GRIIS) (Pagad et al. \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). The filters used were: Plantae Kingdom and True Species. This resulted in a total of 13,249 introduced and/or invasive plant species worldwide.\u003c/p\u003e \u003cp\u003eThe three species lists had their scientific names corrected and standardized according to the WorldFlora Online package WorldFlora 2023.03 version (Kindt \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). After correcting the nomenclature of the species, the lists were manually compared, resulting in a list of 125 species of plants with fruits useful for human consumption that have information on their degree of domestication (Table \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e, supplementary material). From these, we extracted only the species that had records of occurrence as introduced and/or invasive. For these species, we calculated an invasion potential index (IP) using the ratio between the number of checklists in which the species occurred as an invader and the total number of checklists in which it is present (introduced), using the formula below:\u003cdiv id=\"Equa\" class=\"Equation\"\u003e\u003cdiv format=\"TEX\" class=\"mathdisplay\" id=\"FileID_Equa\" name=\"EquationSource\"\u003e\n$$\\:IP=\\frac{number\\:as\\:invasive}{total\\:number\\:of\\:introductions}$$\u003c/div\u003e\u003c/div\u003e\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003e2.2 Data analysis\u003c/h2\u003e \u003cp\u003eTo investigate the factors associated with the invasion potential (IP) of each species, we fitted a generalized linear model (GLM) using the stats package in the R software (R Core Team \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). We used the Invasion Potential index (IP) as the dependent variable and degrees of domestication (degree) as the independent variable. Due to the nature of the data, as a numerical vector with values between 0 and 1, interpreted as the proportion of successful cases, we used the quasibinomial family (R Core Team \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). We incorporated the total number of introductions as an offset, as an a priori known component in the linear predictor during fitting. To validate the model, we assessed the normality and homoscedasticity of the residuals.\u003c/p\u003e \u003c/div\u003e"},{"header":"3 Results","content":"\u003cp\u003eOf the 125 species with fruits for human consumption that presented information on domestication, 74 were introduced outside their natural range (59.2%), and of these, 33 are invasive in at least one checklist (26.4%, Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). A total of 41 domesticated species and those introduced elsewhere did not show any occurrences as invaders (Figure \u003cspan refid=\"MOESM1\" class=\"InternalRef\"\u003eS1\u003c/span\u003e, supplementary material).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e \u003cp\u003eThe most introduced species were \u003cem\u003ePsidium guajava\u003c/em\u003e (93 checklists), \u003cem\u003eJatropha curcas\u003c/em\u003e (93 checklists) and \u003cem\u003ePhysalis peruviana\u003c/em\u003e (74 checklists). The species with the highest occurrence as invaders were \u003cem\u003ePsidium guajava\u003c/em\u003e (31 checklists), \u003cem\u003eEugenia uniflora\u003c/em\u003e (14 checklists) and \u003cem\u003eJatropha curcas\u003c/em\u003e (12 checklists) (Table\u0026nbsp;1). \u003cem\u003ePassiflora alata\u003c/em\u003e (IP\u0026thinsp;=\u0026thinsp;0.50), \u003cem\u003eEugenia uniflora\u003c/em\u003e (IP\u0026thinsp;=\u0026thinsp;0.37) were the species with the greatest invasion potential, followed by \u003cem\u003ePsidium guajava\u003c/em\u003e, \u003cem\u003eSchinus terebinthifolia\u003c/em\u003e, \u003cem\u003eChrysobalanus icaco\u003c/em\u003e, \u003cem\u003ePouteria campechiana\u003c/em\u003e and \u003cem\u003eDiospyros virginiana\u003c/em\u003e (IP\u0026thinsp;=\u0026thinsp;0.33 for all of them).\u003c/p\u003e \u003cp\u003eAll categorical degrees of domestication showed occurrences of invasion (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The majority of species that have occurrences as invaders in at least one checklist are from the fully domesticated class (n\u0026thinsp;=\u0026thinsp;15 species, Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e), followed by semi-domesticated (n\u0026thinsp;=\u0026thinsp;10 species, Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e), incipient (n\u0026thinsp;=\u0026thinsp;5 species, Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e), and wild (n\u0026thinsp;=\u0026thinsp;3 species, Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eWe found a non-linear negative correlation between the degree of domestication and invasion potential (t=-4.362, p\u0026thinsp;\u0026lt;\u0026thinsp;0.005), with an apparent decrease in invasion potential as the degree of domestication increases (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e). The reduction in the invasion potential is more pronounced for the degrees of wild and incipient domestication compared to the degrees of semi- and fully domesticated (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e2\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e \u003c/p\u003e"},{"header":"4 Discussion","content":"\u003cp\u003e The Invasion potential index (IP) of plants with fruit used for human consumption varied according to the degree of domestication. Our hypothesis was not corroborated given that species with intermediate degrees of domestication only showed higher invasion potential than species with higher degree of domestication. We observed a decline of the potential for invasion along the domestication gradient and although fully domesticated plant species have lower invasion potential, they comprehend the majority of species that have occurrences as invaders. This finding suggests that even fully domestication of plants with fruits used for human consumption does not eliminate the invasion risk for some species. Interesting results emerged about the relationship between these two processes that can support public policies and provide suggestions for future studies.\u003c/p\u003e \u003cp\u003eNo degree of domestication was entirely free from having at least one invasive population, contrary to what was expected based on the literature (see Clement \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e1999a\u003c/span\u003e; Clement et al. \u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). This indicates that some plants with intermediated (incipient and semi) and others considered with high degrees of domestication do not lose their ecological adaptability and can persist without human care. This is evidenced by species such as \u003cem\u003ePsidium guajava\u003c/em\u003e and 14 other fully domesticated species that are invasive somewhere (Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Although it is expected that domesticated species have low genetic variation due to genetic bottlenecks (Miller and Gross \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), Clement (\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e1999a\u003c/span\u003e) defines some fully domesticated species as \"\u003cem\u003elandraces\u003c/em\u003e,\" which are populations selected in a cultivated landscape within a restricted geographical region with high phenotypic variability and relatively high genetic variability (Clement et al. 1999a). In particular, domesticated populations of perennial fruit crops maintain a large part of the total genetic variation of the species (Miller and Gross \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Genetic variation can reflect high phenotypic plasticity in some fully domesticated plants and can be key for invasion success.\u003c/p\u003e \u003cp\u003ePhenotypic plasticity is crucial for colonization of new environments (Gering et al \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), being an important factor when species are being selected for domestication (Mueller et al. \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2023\u003c/span\u003e) as well as for the success of biological invasions (Daly et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Phenotypic plasticity allows plants to reacquire adaptive wild characteristics and survive without human intervention. This process, known as de-domestication or feralization, is an evolutionary phenomenon where domesticated crops regain wild-like traits and form independent reproducing populations, escaping intensive human management (Wu et al. \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). As emphasized by Sun et al. (\u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e2022\u003c/span\u003e), domestication is not a one-way road. Domestication can increase the invasion potential of plant species, as it combines resistance acquired along the process with the robustness of wild species. De-domestication could explain why some fully domesticated plants exhibit high invasion potential, emphasizing the need for continuous monitoring of these species. Thus, we highlight the importance of deepening these studies for de-domestication and invasion.\u003c/p\u003e \u003cp\u003eThe plant species with fleshy fruits more frequently recorded as introduced were also more frequently recorded as invasive, as for \u003cem\u003ePsidium guajava\u003c/em\u003e (93 checklists) and \u003cem\u003eJatropha curcas\u003c/em\u003e (93 checklists). This can be considered a consequence of repeated introductions in different regions, which make it possible for the species to be present in several checklists. Repeated introductions in the same region result in high propagule pressure, which can increase the likelihood of survival of individuals and establishment of populations (Simberloff \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Duncan \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). High propagule pressure also increases genetic diversity for populations and promotes gene admixture, thus increasing the adaptive potential of non-native populations, and ultimately the probability of successful introduction (Daly et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). This gene admixture forms intraspecific hybrids between lineages that have been isolated (Gaskin \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e2017\u003c/span\u003e). Globalization has provided opportunities for hybridization (Chornesky and Randall \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2003\u003c/span\u003e). One example is the plant Brazilian peppertree \u003cem\u003e(Schinus terebinthifolia\u003c/em\u003e), one of the species with the greatest invasion potential in our study (IP = 0.33). Native to South America and invasive in the USA, this species formed hybrids from two different Brazilian lineages. These hybrids seem to be more resistant to certain biological control agents, exhibit greater vigor, with 45% more seedlings established compared to the original plants (Geiger et al. \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2011\u003c/span\u003e) and have an increased ability of colonizing new areas (Gaskin 2016).\u003c/p\u003e \u003cp\u003eInterspecific hybridization is another important process in the success of biological invasions (Daly et al. \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2023\u003c/span\u003e) and seems to be an important mechanism for adaptive evolution in several crop-domesticated species (Purugganan \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). Species transported by humans to new areas are subject to hybridization with wild species (exoferal ancestry, Ellstrand et al. \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e2010\u003c/span\u003e), which can facilitate the establishment and invasion by introduced species (Harrison and Larson \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Purugganan \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). This suggests that if the introduced species contacts closely-related native species in the new area, the non-native species may be favored, while the native species could be threatened by direct competition or a loss of genetic diversity. \u003cem\u003ePsidium guajava\u003c/em\u003e (guava) is the most frequently introduced species in our study, with the highest number of invasive records and showing a high invasion potential (IP = 0.33). Hybridization between \u003cem\u003eP. guajava\u003c/em\u003e and other \u003cem\u003ePsidium\u003c/em\u003e species is a real possibility (Gomes et al. \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), as evidenced by reported cases of hybridization between \u003cem\u003eP. guajava\u003c/em\u003e and \u003cem\u003eP. guineense\u003c/em\u003e in Mexico, Honduras and Argentina (Landrum et al. \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e1995\u003c/span\u003e). In Ecuador, on the Galapagos islands, the distribution of \u003cem\u003eP.guajava\u003c/em\u003e overlaps with the endemic \u003cem\u003ePsidium galapageium\u003c/em\u003e, raising concerns about potential hybridization and competition (Urquía et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Reatini et al. \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Similar situation occurred in Mexico with the hybridization of \u003cem\u003ePsidium socorrense\u003c/em\u003e (López-Caamal et al. \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). Although hybridization between \u003cem\u003eP. guajava\u003c/em\u003e and \u003cem\u003eP. galapageium\u003c/em\u003e has not yet been confirmed, the risk persists, making future studies crucial to understand its potential impact (Urquía et al. \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e2019\u003c/span\u003e). That said, we highlight that the presence of native species that are close relatives to introduced species must be considered in prevention tools for the intentional introduction of species such as risk analysis, in order to avoid negative impacts due to hybridization with the native flora.\u003c/p\u003e \u003cp\u003eA possible key component to the invasion of plants with fruits domesticated for human consumption is that many of these plants may not have lost their seed dispersal capability. Many of the progenitors of modern domesticated crops relied on animals for seed dispersal and most are fleshy fruits, which represent evolutionary adaptations for seed dispersal with animals as vectors (Spengler \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2020\u003c/span\u003e). Domesticated fruits are very attractive on the landscape, as increases in pericarp tissue and sugar concentrations are among the basic traits of domestication in fruit plants (Miller and Gross \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). These fruits are available to both humans and animals, which can consume and disperse the seeds, facilitating their spread to areas far from the introduction site and outside of cultivation zones, thereby increasing the chances of germination and invasion (Petri et al. \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Additionally, the establishment of these frugivory interactions can be facilitated if the non-native plant presents fleshy fruits with small seeds, high energy content and fruiting phenologies at different times compared to native species (Richardson et al. 2000; Gosper et al. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2005\u003c/span\u003e). Domesticated species are often adapted to anthropogenic environments (Clement et al. \u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e2021\u003c/span\u003e), which may give them an advantage in disturbed or human-made ecosystems. Ecosystem degradation further facilitates the invasion of many non-native plants by altering species distributions and resource dynamics within ecosystems (Buckley et al. \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2006\u003c/span\u003e; Feng et al. \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). It is likely that the general attractiveness of these fruits to local fauna, combined with the decreasing availability of native fruits in highly fragmented landscapes, promotes generalist frugivorous to feed on what is available and most accessible (Gosper et al. \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Siegel et al. \u003cspan citationid=\"CR54\" class=\"CitationRef\"\u003e2024\u003c/span\u003e). We detail some of the species that stood out for their invasion potential along with information regarding its use, seed dispersal, type of fruit, and natural history (Box 1).\u003c/p\u003e \u003cp\u003eOur study has some limitations that should be considered and may guide future studies. First, the scope of the study was restricted to the Americas and to plants with fruit used for human consumption, which may limit the generalizability of the results to other regions and types of plant use. However, we consider that the geographical extension and relevance of the Americas regarding species domestication and biological invasions enables us to extrapolate our results and conclusions to other regions. Second, domestication and invasion may be different for perennial and annual plants because these plants differ in terms of genetic variation and rates of evolution (Miller and Groos 2011), and we did not make this distinction in this study. Third, we used the available information on occurrences of invasion, but this does not imply that all species are absent in other areas that are data deficient. There are significant gaps in information regarding occurrences, assessments of whether species are invasive, the dates of their first records, and the pathways involved (IPBES \u003cspan citationid=\"CR30\" class=\"CitationRef\"\u003e2023\u003c/span\u003e). Finally, the available databases did not allow us to distinguish degrees of domestication between different plant populations. This intrinsic variation could provide additional insights into the relationship between domestication and invasion. Future studies can address these limitations as well as include functional traits in order to assess the altered characteristics that can facilitate or hinder biological invasions.\u003c/p\u003e "},{"header":"Conclusions","content":"\u003cp\u003eThis study highlights the complexity and multifaceted nature of two important processes mediated by humans, occurring at the plant population level: plant domestication and biological invasions. We provide a general overview of the global situation of biological invasions caused by plants with a history of domestication in the Americas. We showed that domestication degree can have an influence on invasion potential. Full domestication seems to reduce the invasion potential but does not eliminate completely the invasion risk, given the continued persistence and adaptability to human-dominated landscapes of species such as \u003cem\u003ePsidium guajava\u003c/em\u003e. New studies are necessary to investigate the determination of the invasion potential of these species based on the interplay between domestication, genetic diversity, phenotypic plasticity, and seed dispersal mechanisms.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003eConflict of Interest\u003c/p\u003e\n\u003cp\u003eThe authors declare that the research was conducted in the absence of any conflict of interest.\u003c/p\u003e\n\u003cp\u003eAuthor Contributions\u003c/p\u003e\n\u003cp\u003eAll authors contributed to the study conception and design. Brisa Marciniak, Nivaldo Peroni, and Michele de Sa Dechoum originally formulated the idea. Material preparation, data collection and analysis were performed by Brisa Marciniak. The first draft of the manuscript was written by Brisa Marciniak and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThis study was funded in part by the Coordena\u0026ccedil;\u0026atilde;o de Aperfei\u0026ccedil;oamento de Pessoal de N\u0026iacute;vel Superior\u0026mdash;Brasil (CAPES)\u0026mdash;Finance Code 001.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eCompeting Interests\u003c/strong\u003e\u003c/p\u003e\n\u003cp\u003eThe authors have no relevant financial or non-financial interests to disclose.\u003c/p\u003e\n\u003cp\u003eData Availability\u003c/p\u003e\n\u003cp\u003eNot applicable.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\n\u003cli\u003eAchten WM, Nielsen LR, Aerts R et al (2010) Towards domestication of Jatropha curcas. 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Species with higher degrees of domestication are highly dependent on humans for survival and reproduction. On the other hand, lower degrees may result in lower survival rates and reproduction output. However, the interrelationship between degrees of domestication and plant invasion remains underexplored. We focused our study on plant species native to the Americas with distinct degrees of domestication, with fruits used for human consumption, to test the hypothesis that plants with intermediate degrees of domestication show higher invasion potential than plants with lower or higher degrees of domestication. We calculated an invasion potential index as the ratio between the number of checklists where an introduced species was recorded as invasive and the total number of checklists where it was registered as introduced. Our results show a negative non-linear relationship between the degree of domestication and invasion potential. While species with intermediate degrees of domestication show higher invasion potential than those fully domesticated, species with the lowest degrees of domestication showed the highest invasion potential. These findings suggest that full domestication does not eliminate invasion risk, highlighting the complexity of the relationship between domestication and invasion. Our results provide valuable insights to support public policies, inform future studies on plant invasions, and the need for management strategies that consider different degrees of domestication.\u003c/p\u003e","manuscriptTitle":"Low degree of domestication can be an indicator of high potential of biological invasion","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-11-13 18:13:18","doi":"10.21203/rs.3.rs-5362570/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"962d6c10-68ee-415e-928b-68e082257047","owner":[],"postedDate":"November 13th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2024-12-04T02:08:50+00:00","versionOfRecord":[],"versionCreatedAt":"2024-11-13 18:13:18","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-5362570","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-5362570","identity":"rs-5362570","version":["v1"]},"buildId":"FbvkV6FR0MCFSLy54lSbu","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}