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Getting Back to Nature: Feralization in Animals and Plants

2019; Elsevier BV; Volume: 34; Issue: 12 Linguagem: Inglês

10.1016/j.tree.2019.07.018

1872-8383

Eben Gering, Darren C. Incorvaia, Rie Henriksen, Jeffrey K. Conner, Thomas Getty, Dominic Wright,

Plant Reproductive Biology

Feral animals and plants have become ubiquitous worldwide, but their evolution has not been well studied.The process of feralization offers unique and important opportunities to study adaptive evolution, often in model systems inhabiting diverse, novel, and/or changing environments.Recent work shows that feral taxa undergo rapid evolutionary changes at loci controlling an array of fitness-related traits, including morphology, behavior, and development.Gene flow between domesticated and wild populations has important, diverse, and context-dependent effects on fitness in recipient populations.Legacies of domestication are seen in many feral plants and animals. These features can have important and unexpected roles in subsequent adaptation to changing (e.g., feral) environments. Formerly domesticated organisms and artificially selected genes often escape controlled cultivation, but their subsequent evolution is not well studied. In this review, we examine plant and animal feralization through an evolutionary lens, including how natural selection, artificial selection, and gene flow shape feral genomes, traits, and fitness. Available evidence shows that feralization is not a mere reversal of domestication. Instead, it is shaped by the varied and complex histories of feral populations, and by novel selection pressures. To stimulate further insight we outline several future directions. These include testing how 'domestication genes' act in wild settings, studying the brains and behaviors of feral animals, and comparative analyses of feral populations and taxa. This work offers feasible and exciting research opportunities with both theoretical and practical applications. Formerly domesticated organisms and artificially selected genes often escape controlled cultivation, but their subsequent evolution is not well studied. In this review, we examine plant and animal feralization through an evolutionary lens, including how natural selection, artificial selection, and gene flow shape feral genomes, traits, and fitness. Available evidence shows that feralization is not a mere reversal of domestication. Instead, it is shaped by the varied and complex histories of feral populations, and by novel selection pressures. To stimulate further insight we outline several future directions. These include testing how 'domestication genes' act in wild settings, studying the brains and behaviors of feral animals, and comparative analyses of feral populations and taxa. This work offers feasible and exciting research opportunities with both theoretical and practical applications. Domesticated animals and plants comprise a rapidly growing proportion of life on our planet [1Bar-On Y.M. et al.The biomass distribution on Earth.Proc. Natl. Acad. Sci. U. S. A. 2018; 115: 6506-6511Crossref PubMed Scopus (14) Google Scholar]. The vast ranges and abundance of these organisms show that domestication (see Glossary) can have remarkable evolutionary payoffs. At the same time, it can induce both plastic and genetic modifications that limit the capacity of an organism to thrive in nature (e.g., [2Araki H. et al.Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild.Biol. Lett. 2009; 5: 621-624Crossref PubMed Scopus (131) Google Scholar, 3Milla R. et al.Plant domestication through an ecological lens.Trends Ecol. Evol. 2015; 30: 463-469Abstract Full Text Full Text PDF PubMed Google Scholar, 4Gering E. et al.Maladaptation in feral and domesticated animals.Evol. Appl. 2019; 12: 1274-1286Crossref PubMed Scopus (2) Google Scholar]). Despite this maladaptation, feralization of animals and plants has proven, sometimes to humans' great frustration, that domestication is not always a one-way process. The flow of domesticated organisms and their genes into noncaptive settings has important conservation implications; it also presents unique opportunities to characterize general and novel evolutionary processes of Anthropocene environments [5Sarrazin F. Lecomte J. Evolution in the Anthropocene.Science. 2016; 351: 922923Crossref Scopus (27) Google Scholar]. With these applications in mind, our review summarizes current knowledge regarding the process of feralization and provides a roadmap for further investigation into this tractable, exciting, and understudied research area. Feralization merits special consideration because its subjects are uniquely distinguished from other animals and plants. Biologists have long appreciated how domestication shapes wild organisms via both deliberate artificial selection by humans and unintended effects of anthropogenic propagation [6Darwin C. The Variation of Animals and Plants under Domestication. John Murray, 1868Google Scholar]. In recent decades, these effects have been elucidated by intensive studies bridging disparate fields (e.g., anthropology, plant and animal science, and organismal, behavioral, and developmental biology) [7Martin A. Orgogozo V. The loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation.Evolution. 2013; 67: 1235-1250PubMed Google Scholar, 8Larson G. et al.Current perspectives and the future of domestication studies.Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 6139-6146Crossref PubMed Scopus (188) Google Scholar, 9Brandenburg J.T. et al.Independent introductions and admixtures have contributed to adaptation of European maize and its American counterparts.PLoS Genet. 2017; 13e1006666Crossref PubMed Scopus (5) Google Scholar]. By contrast, there has been relatively little research into the process of feralization. Here, progress is also hindered by long-held speculations and misconceptions. These include: (i) the idea that formerly domesticated populations are incapable of rapid adaptation, due to their genetic homogeneity or recent establishment [10Allaby R.G. et al.A re-evaluation of the domestication bottleneck from archaeogenomic evidence.Evol. Appl. 2019; 12: 29-37Crossref PubMed Scopus (4) Google Scholar]; (ii) the idea that captive propagation invariably reduces fitness outside of domesticated settings due to evolutionary tradeoffs and relaxed natural selection (e.g., [2Araki H. et al.Carry-over effect of captive breeding reduces reproductive fitness of wild-born descendants in the wild.Biol. Lett. 2009; 5: 621-624Crossref PubMed Scopus (131) Google Scholar, 11Meyer R.S. Purugganan M.D. Evolution of crop species: genetics of domestication and diversification.Nat. Rev. Genet. 2013; 14: 840Crossref PubMed Scopus (314) Google Scholar]); and (iii) a belief that feralization predictably results in atavism (e.g., [12Price E.O. Behavioral aspects of animal domestication.Q. Rev. Biol. 1984; 59: 1-32Crossref Google Scholar]). These ideas have received only mixed support from a small but growing body of relevant research. Here, we draw on case studies to: (i) show that routes to feralization are diverse and can facilitate rapid evolution; (ii) synthesize current knowledge concerning feral genotypes and phenotypes; and (iii) outline avenues for future studies. There are many extended discussions of problems surrounding the definition of domestication (e.g., [13Russell N. The wild side of animal domestication.Soc. Anim. 2002; 10: 285-302Crossref Scopus (54) Google Scholar, 14Bökönyi S. Definitions of animal domestication.in: Clutton-Brock J. The Walking Larder. Patterns of Domestication, Pastoralism, and Predation. Routledge, 1989: 24-27Google Scholar, 15Gamborg C. et al.De-domestication: ethics at the intersection of landscape restoration and animal welfare.Environ. Values. 2010; 19: 57-78Crossref Scopus (27) Google Scholar]). The broadest definitions encompass nonhuman species, such as leaf-cutter ants, that also cultivate mutualists (e.g., [16Zeder M.A. Core questions in domestication research.Proc. Natl. Acad. Sci. U. S. A. 2015; 112: 3191-3198Crossref PubMed Scopus (0) Google Scholar]). Yet, while these cultivars can feralize [17Mueller U.G. et al.The evolution of agriculture in insects.Annu. Rev. Ecol. Evol. Syst. 2005; 36: 563-595Crossref Scopus (304) Google Scholar], such non-anthropogenic processes lie beyond the scope of this review. Others [13Russell N. The wild side of animal domestication.Soc. Anim. 2002; 10: 285-302Crossref Scopus (54) Google Scholar, 18Ballard J.W.O. Wilson L.A.B. The Australian dingo: untamed or feral?.Front. Zool. 2019; 16: 2Crossref PubMed Scopus (0) Google Scholar] describe domestication as movement along continua of human–animal interactions or, alternatively, as solely the onset of human-facilitated propagation (e.g., [11Meyer R.S. Purugganan M.D. Evolution of crop species: genetics of domestication and diversification.Nat. Rev. Genet. 2013; 14: 840Crossref PubMed Scopus (314) Google Scholar]). In this review, we expand an operational definition developed for animals [19Price E.O. Animal Domestication and Behavior. CABI, 2002Crossref Google Scholar] to include agricultural and ornamental plants. Except where noted otherwise, we also adopt the inclusion by this definition of both the establishment and subsequent improvement stages of anthropogenic propagation. Our review also examines how the allele frequencies, traits, and fitness of wild populations can be altered by the introgression of feral alleles from artificially selected sources; thus, it encompasses many wild gene pools that are chiefly derived from undomesticated ancestors [20Randi E. Detecting hybridization between wild species and their domesticated relatives.Mol. Ecol. 2008; 17: 285-293Crossref PubMed Scopus (190) Google Scholar, 21Canestrelli D. et al.The tangled evolutionary legacies of range expansion and hybridization.Trends Ecol. Evol. 2016; 31: 677-688Abstract Full Text Full Text PDF PubMed Scopus (27) Google Scholar]. Here, we show that even limited introgression from artificially selected sources can have important evolutionary consequences. For clarity, however (except where noted), we use 'feral' to describe free-living organisms or populations that are primarily descended from domesticated ancestors. Our discussion of feralization requires a few caveats. First, some feral populations still receive limited, intentional support from humans. For example, feral cats and horses are sometimes provisioned with food, yet remain highly self-reliant compared with their domestic counterparts and do not fulfill an artificially selected utility. Additionally, some taxa have oscillated between feral and domestic states, blurring lines between the two processes (e.g., longhorn cattle that were redomesticated from feral ancestors) [22McTavish E.J. et al.New World cattle show ancestry from multiple independent domestication events.Proc. Natl. Acad. Sci. U. S. A. 2013; 110: E1398-E1406Crossref PubMed Scopus (68) Google Scholar]. Finally, we acknowledge that feralization need not involve a return to truly 'wild' habitats. Instead, it often unfolds within cultivated or disturbed settings (e.g., agricultural fields and cities). Still, its subjects are distinguished from domesticated ancestors by the withdrawal of intentional efforts to support their reproduction. This alters selection regimes in ways that can, both in principle and practice, produce rapid evolutionary changes (Figure 1). To understand how populations evolve, it is usually helpful to examine their sources and genetic structures. Given that feral populations compound demographic and selective effects of domestication with a subsequent 're-invasion', they present unique challenges for DNA-based ancestry reconstructions, as well as for sequence-based tests of adaptation [4Gering E. et al.Maladaptation in feral and domesticated animals.Evol. Appl. 2019; 12: 1274-1286Crossref PubMed Scopus (2) Google Scholar, 23McFarlane S.E. Pemberton J.M. Detecting the true extent of introgression during anthropogenic hybridization.Trends Ecol. Evol. 2019; 34: 315-326Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar]. Despite these obstacles, many investigators have succeeded in elucidating pathways to ferality. Gressel [24Gressel J. Crop Ferality and Volunteerism. CRC Press, 2005Crossref Scopus (9) Google Scholar] delineated two alternative categories, which we illustrate with diverse examples in Table 1. 'Endoferal' populations stem from a single domesticated lineage (e.g., a breed or crop), whereas 'exoferal' populations are derived via admixture, either among domesticated lineages (e.g., crop varieties) or between domestic taxa and their wild relatives. Current data suggest that both endo- and exoferality are common. Among 23 plants that have feralized into weedy or invasive forms, approximately equal numbers were found to involve endo- versus exoferal origins [25Ellstrand N.C. et al.Crops gone wild: evolution of weeds and invasives from domesticated ancestors.Evol. Appl. 2010; 3: 494-504Crossref PubMed Scopus (0) Google Scholar]. Both mechanisms have also produced feral animal populations (Table 2), although their relative roles have not been systematically reviewed.Table 1Animal and Plant Domestications That Have Resulted in Feralization, and Their Primary (Artificially Selected) UtilitiesOrderDomesticated taxonAntiquity (years before present)FoodCompanionshipAidSecurityOrnamentSport-racingWarfareSport-fightingTransport or draftTextilesPest controlPollinationMammalsCarnivoraDog, dingoCanis lupus15 000aFrom [100].House catFelis catus9500aFrom [100].American minkNeovison vison80bFrom [101].LagomorphaRabbitOryctolagus cuniculus1300–17 000cFrom [102].PerissodactylaPigSus scrofa10 300aFrom [100].HorseEquus ferus5500aFrom [100].AssEquus africanus5500aFrom [100].ArtiodactylaGoatCapra aegagrus hircus10 000aFrom [100].SheepOvis aries10 000aFrom [100].CowBos taurus10 300aFrom [100].Dromedary camelCamelus dromedarius3000aFrom [100].BirdsGalliformesChickenGallus gallus4000aFrom [100].TurkeyMeleagris gallopavo2000dFrom [103].ColumbiformesStreet pigeonColumbus livia>5000bFrom [101].AnseriformesMallardAnas platyrhynchos1000aFrom [100].Muscovy duckCairina moschataPre-ColumbianInsectsHymenopteraHoneybeeApis mellifera9000eFrom [104].LepidopteraSilkwormBombyx mori7500eFrom [104].FishSalmoniformes, Cyprinodontiformes, Cypriformes, Cichliformes, AnabantiformesAquacultural and pet speciese.g., salmon, cichlids, guppies, betasVariablePlantsAsteralesJerusalem artichokeHelianthus tuberosusPoalesBread wheatTriticum aestivum10 000fFrom [105].Finger milletEleusine coracana5000fFrom [105].Grain sorghumSorghum bicolor5000fFrom [105].RiceOryza sativa7000fFrom [105].RyeSecale cereale5000fFrom [105].BrassicalesRadishRaphanus raphanistrum8000gFrom [106].CaryohyllalesSugarbeetBeta vulgaris300fFrom [105].a From 100MacHugh et al.Taming the past: ancient DNA and the study of animal domestication.Annu. Rev. Anim. Biosci. 2017; 5: 329-351Crossref PubMed Scopus (13) Google Scholar.b From 101Hansen S.W. Selection for behavioural traits in farm mink.Appl. Anim. Behav. Sci. 1996; 49: 137-148Crossref Scopus (0) Google Scholar.c From 102Domyan E.T. Shapiro M.D. Pigeonetics takes flight: evolution, development, and genetics of intraspecific variation.Dev. Biol. 2017; 427: 241-250Crossref PubMed Scopus (12) Google Scholar.d From 103Thornton E.K. et al.Earliest Mexican Turkeys (Meleagris gallopavo) in the Maya region: implications for pre-Hispanic animal trade and the timing of Turkey domestication.PLoS One. 2012; 7e42630Crossref PubMed Scopus (36) Google Scholar.e From 104Lecocq T. Insects: the disregarded domestication histories.in: Teletchea F. Animal Domestication. IntechOpen, 2018: 35-68Google Scholar.f From 105Cordain L. Cereal grains: humanity's double-edged sword.World Rev. Nutr. Diet. 1999; 84: 19-19Google Scholar.g From 106Charbonneau A. et al.Weed evolution: genetic differentiation among wild, weedy, and crop radish.Evol. Appl. 2018; 11: 1964-1974Crossref PubMed Scopus (0) Google Scholar. Open table in a new tab Table 2Sources of Feral Animals and PlantsDomestic population crossed withDefinitionaAfter [24,25].ExamplesSelfEndoferalCrop rice (Oryza sativa) appears to be particularly prone to feralization, because there is evidence for multiple de-domestication events with varying origins in Asia and North America. Weed rice populations of endoferal origin are present on both continents 98Vigueira C.C. et al.Call of the wild rice: Oryza rufipogon shapes weedy rice evolution in Southeast Asia.Evol. Appl. 2019; 12: 93-104Crossref PubMed Scopus (5) Google Scholar. Endoferality is common in animals, including serial introductions of rabbits to Australia that have generated genetically distinct endoferal subpopulations 47Iannella A. et al.Genetic perspectives on the historical introduction of the European rabbit (Oryctolagus cuniculus) to Australia.Biol. Invasions. 2019; 21: 603-614Crossref Scopus (1) Google ScholarDivergent population (e.g., breed or crop)Exo–endoferal (intercrop)In Bhutan, weedy rice is a hybrid of two crop varieties (O.s. japonica × O.s. Indica) 98Vigueira C.C. et al.Call of the wild rice: Oryza rufipogon shapes weedy rice evolution in Southeast Asia.Evol. Appl. 2019; 12: 93-104Crossref PubMed Scopus (5) Google Scholar. Feral cattle in the New World that were subsequently re-domesticated stemmed from admixture between independently domesticated taurine and indicine aurochs (Bos primigenius), and this admixture may have facilitated adaptation to novel environments outside the native range 22McTavish E.J. et al.New World cattle show ancestry from multiple independent domestication events.Proc. Natl. Acad. Sci. U. S. A. 2013; 110: E1398-E1406Crossref PubMed Scopus (68) Google ScholarWild conspecificExoferal (crop–wild)SNP diversity of weedy rice is higher in southwest Asia than in the range of wild rice, due to introgression from wild rice and also perhaps from local crop rice landraces 98Vigueira C.C. et al.Call of the wild rice: Oryza rufipogon shapes weedy rice evolution in Southeast Asia.Evol. Appl. 2019; 12: 93-104Crossref PubMed Scopus (5) Google Scholar. Exoferal (domestic–wild) animals include chickens that hybridize with red junglefowl (Gallus gallus) within the native and introduced ranges of the species 30Gering E. et al.Mixed ancestry and admixture in Kauai's feral chickens: invasion of domestic genes into ancient Red Junglefowl reservoirs.Mol. Ecol. 2015; 2421122124Crossref Scopus (17) Google Scholar, 107Thakur M. et al.Understanding the cryptic introgression and mixed ancestry of Red Junglefowl in India.PLoS One. 2018; 13e0204351Crossref PubMed Scopus (0) Google ScholarOther domesticated speciesExoferal (domestic hybrid)Feral Jerusalem artichoke (Helianthus tuberosus) and domesticated sunflower (Helianthus annuus) may hybridize in Europe 25Ellstrand N.C. et al.Crops gone wild: evolution of weeds and invasives from domesticated ancestors.Evol. Appl. 2010; 3: 494-504Crossref PubMed Scopus (0) Google ScholarOther wild speciesExoferal (crop–wild hybrid)California wild radish is an interspecific hybrid between the crop radish (Raphanus sativus) and the agricultural weed ecotype of native wild radish (Raphanus raphanistrum; 64Hegde S.G. et al.The evolution of California's wild radish has resulted in the extinction of its progenitors.Evolution. 2006; 60: 1187-1197Crossref PubMed Google Scholar). Available evidence suggests that the agricultural weed radish is derived from the native wild radish 106Charbonneau A. et al.Weed evolution: genetic differentiation among wild, weedy, and crop radish.Evol. Appl. 2018; 11: 1964-1974Crossref PubMed Scopus (0) Google Scholar. Animal examples are rare, but include coyote–dog (Canis latrans × C. lupus) hybrids 58Monzón J. et al.Assessment of coyote–wolf–dog admixture using ancestry-informative diagnostic SNPs.Mol. Ecol. 2014; 23: 182-197Crossref PubMed Scopus (48) Google ScholarGenetically modified organismExoferal (transgene hybrid)Transgenes have been found in several wild plant populations 37Ellstrand N. 'Born to run'? Not necessarily: species and trait bias in persistent free-living transgenic plants.Front. Bioeng. Biotechnol. 2018; 6: 88Crossref PubMed Google Scholar, 38Wegier A. et al.Recent long-distance transgene flow into wild populations conforms to historical patterns of gene flow in cotton (Gossypium hirsutum) at its centre of origin.Mol. Ecol. 2011; 20: 4182-4194Crossref PubMed Scopus (33) Google Scholar, 39Reichman J.R. et al.Establishment of transgenic herbicide-resistant creeping bentgrass (Agrostis stolonifera L.) in nonagronomic habitats.Mol. Ecol. 2006; 15: 4243-4255Crossref PubMed Scopus (0) Google Scholar, 40Mallory-Smith C. Zapiola M. Gene flow from glyphosate-resistant crops.Pest Manag. Sci. 2008; 64: 428-440Crossref PubMed Scopus (71) Google Scholar. Animal cases are not yet known, partly due to legal, logistical, and technological barriers to the cultivation of transgenic animalsa After 24Gressel J. Crop Ferality and Volunteerism. CRC Press, 2005Crossref Scopus (9) Google Scholar, 25Ellstrand N.C. et al.Crops gone wild: evolution of weeds and invasives from domesticated ancestors.Evol. Appl. 2010; 3: 494-504Crossref PubMed Scopus (0) Google Scholar. Open table in a new tab Endoferality can occur when individuals from a domestic population escape into local environments in which they can survive and reproduce. This is what most people envision when contemplating feralization. Endoferality can also result from intentional releases of organisms to establish feral descendants. We call this process 'de-domestication' (sensu [15Gamborg C. et al.De-domestication: ethics at the intersection of landscape restoration and animal welfare.Environ. Values. 2010; 19: 57-78Crossref Scopus (27) Google Scholar]), although the term is used in the plant literature synonymously with atavism (e.g., [26Wang H. et al.Asian wild rice is a hybrid swarm with extensive gene flow and feralization from domesticated rice.Genome Res. 2017; 27: 1029-1038Crossref PubMed Scopus (17) Google Scholar]). Motives for releases of domestic taxa range from ecosystem engineering [27Rubenstein D.R. et al.Pleistocene park: does re-wilding North America represent sound conservation for the 21st century?.Biol. Conserv. 2006; 132: 232-238Crossref Scopus (0) Google Scholar] to providing recreational, nutritional, and/or economic benefits (e.g., hunting and fishing) [28McCann B.E. et al.Molecular population structure for feral swine in the United States.J. Wildl. Manag. 2018; 82: 821-832Crossref Scopus (1) Google Scholar]. Exoferality, by definition, involves admixture. Sometimes, this gene flow precedes translocation into new environments, as shown by a subset of North American weedy rice that originated from admixture outside of their introduced range [29Londo J.P. Schaal B.A. Origins and population genetics of weedy red rice in the USA.Mol. Ecol. 2007; 16: 4523-4535Crossref PubMed Scopus (112) Google Scholar]. Admixture can also occur at multiple timepoints during and after establishment. For example, archeological, morphological, and genetic evidence suggest that, centuries after Polynesians dispersed red junglefowl (Gallus gallus) into Pacific Oceania, the descendants of these birds hybridized with chickens introduced by Europeans (e.g., [30Gering E. et al.Mixed ancestry and admixture in Kauai's feral chickens: invasion of domestic genes into ancient Red Junglefowl reservoirs.Mol. Ecol. 2015; 2421122124Crossref Scopus (17) Google Scholar, 31Thomson V.A. et al.Using ancient DNA to study the origins and dispersal of ancestral Polynesian chickens across the Pacific.Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 4826-4831Crossref PubMed Scopus (0) Google Scholar, 32Cornwallis C. The status and degree of hybridisation of Red junglefowl on three islands – a comment.Tragopan. 2002; 16: 26-29Google Scholar, 33Peterson A.T. Brisbin I.L. Phenotypic status of Red Junglefowl Gallus gallus populations introduced on Pacific islands.Bull. Br. Orn. Club. 2005; 125: 59-61Google Scholar]). These and other exoferal populations (e.g., Table 2) provide tractable systems for studying how gene flow impacts the establishment, fitness, and local adaptation of non-native organisms, a central goal of invasion biology (e.g., [4Gering E. et al.Maladaptation in feral and domesticated animals.Evol. Appl. 2019; 12: 1274-1286Crossref PubMed Scopus (2) Google Scholar, 23McFarlane S.E. Pemberton J.M. Detecting the true extent of introgression during anthropogenic hybridization.Trends Ecol. Evol. 2019; 34: 315-326Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar, 34Whitney K.D. Gering E. Five decades of invasion genetics.New Phytol. 2015; 205: 472-475Crossref PubMed Scopus (4) Google Scholar, 35Welles S.R. Dlugosch K.M. Population genomics of colonization and invasion.in: Rajora O. Population Genomics. Springer, 2018: 655-683Crossref Google Scholar, 36Bock D.G. et al.What we still don't know about invasion genetics.Mol. Ecol. 2015; 24: 2277-2297Crossref PubMed Scopus (89) Google Scholar]). In addition, a subset of exoferal gene pools harbor feralized transgenes, an increasingly common phenomenon that raises unique ethical issues and research questions [37Ellstrand N. 'Born to run'? Not necessarily: species and trait bias in persistent free-living transgenic plants.Front. Bioeng. Biotechnol. 2018; 6: 88Crossref PubMed Google Scholar]. Transgenes have introgressed into nonagronomic plant populations (e.g., wild cotton and bentgrass [38Wegier A. et al.Recent long-distance transgene flow into wild populations conforms to historical patterns of gene flow in cotton (Gossypium hirsutum) at its centre of origin.Mol. Ecol. 2011; 20: 4182-4194Crossref PubMed Scopus (33) Google Scholar, 39Reichman J.R. et al.Establishment of transgenic herbicide-resistant creeping bentgrass (Agrostis stolonifera L.) in nonagronomic habitats.Mol. Ecol. 2006; 15: 4243-4255Crossref PubMed Scopus (0) Google Scholar]), into cultivated crops (e.g., canola, soybean, and maize [40Mallory-Smith C. Zapiola M. Gene flow from glyphosate-resistant crops.Pest Manag. Sci. 2008; 64: 428-440Crossref PubMed Scopus (71) Google Scholar]), and into feral plants (e.g., weedy rice and beets [41Chen L.J. et al.Gene flow from cultivated rice (Oryza sativa) to its weedy and wild relatives.Ann. Bot. 2004; 93: 67-73Crossref PubMed Scopus (0) Google Scholar, 42Darmency H. et al.Transgene escape in sugar beet production fields: data from six years farm scale monitoring.Environ. Biosaf. Res. 2007; 6: 197-206Crossref PubMed Scopus (34) Google Scholar]). Thus, gene flow among domestic, feral, and wild plants comprises an important potential mechanism for transgene establishment and spread. In the near future, broadening of sampling and analytical tools will likely increase the number of feral populations with known exoferal origins [23McFarlane S.E. Pemberton J.M. Detecting the true extent of introgression during anthropogenic hybridization.Trends Ecol. Evol. 2019; 34: 315-326Abstract Full Text Full Text PDF PubMed Scopus (3) Google Scholar]. Ancient DNA can also be used to clarify population ancestries (e.g., [43Almathen F. et al.Ancient and modern DNA reveal dynamics of domestication and cross continental dispersal of the dromedary.Proc. Natl. Acad. Sci. U. S. A. 2016; 11367076712Crossref Scopus (32) Google Scholar, 44Ottoni C. et al.The palaeogenetics of cat dispersal in the ancient world.Nature Ecol. Evol. 2017; 1: 0139Crossref Google Scholar]). Recently, for instance, this approach revealed that modern Przewalski's horses are in fact feral descendants of horses domesticated by the Botai culture, rather than truly wild [45Gaunitz C. et al.Ancient genomes revisit the ancestry of domestic and Przewalski's horses.Science. 2018; 360: 111-114Crossref PubMed Scopus (13) Google Scholar]. Furthermore, recent introgression from domestic horses has introduced deleterious gene variants to this exoferal gene pool. The diversity of pathways to feralization (Table 2) raises an interesting issue regarding the modeling of the process. Although endoferal populations provide the clearest insights into how feral selection regimes affect formerly domestic gene pools and traits (i.e., evolution in absentia of admixture), they may also represent a minority of feralization episodes in nature. A parallel conundrum has catalyzed recent revisions of domestication models, since the process involves admixture more often than previously thought, and it can also be difficult to detect [8Larson G. et al.Current perspectives and the future of domestication studies.Proc. Natl. Acad. Sci. U. S. A. 2014; 111: 6139-6146Crossref PubMed Scopus (188) Google Scholar]. Viewing feralization 'in light of admixture' helps to clarify how future gene flow can impact outcomes and consequences of the process. For example, many feral taxa (e.g., weedy rice, dogs, and chickens) appear to exhibit both exo- and endoferal origins across their current ranges. These interpopulation differences result in both genetic and phenotypic variation (e.g., [25Ellstrand N.C. et al.Crops gone wild: evolution of weeds and invasives from domesticated ancestors.Evol. Appl. 2010; 3: 494-504Crossref PubMed Scopus (0) Google Scholar, 30Gering E. et al.Mixed ancestry and admixture in Kauai's feral chickens: invasion of domestic genes into ancient Red Junglefowl reservoirs.Mol. Ecol. 2015; 2421122124Crossref Scopus (17) Google Scholar, 46Randi E. et al.Multilocus detection of wolf × dog hybridization in Italy, and guidelines for marker selection.PLoS One. 2014; 9e86409Crossref PubMed Scopus (0) Google Scholar, 47Iannella A. et al.Genetic perspectives on the historical introduction of the European rabbit (Oryctolagus cuniculus) to Australia.Biol. Invasions. 2019; 21: 603-614Crossref Scopus (1) Google Scholar]), which would likely be affected by further introgression (e.g., admixture be