Feralization: Confronting the Complexity of Domestication and Evolution
Authors: Makenzie E. Mabry, Troy N. Rowan, J. Chris Pires, Jared E. Decker
Journal: Trends in Genetics (2021)

Feral populations, those which successfully persist outside of cultivation or husbandry, provide unique opportunities to study the genomic impacts of domestication and local adaptation. We argue that by leveraging genomic resources designed for domestic counterparts, powerful phylogenetic and population genomic data collection and analyses can be designed to disentangle complex demographic processes. Feral populations, those which successfully persist outside of cultivation or husbandry, provide unique opportunities to study the genomic impacts of domestication and local adaptation. We argue that by leveraging genomic resources designed for domestic counterparts, powerful phylogenetic and population genomic data collection and analyses can be designed to disentangle complex demographic processes. Surveys of feral populations in a wide range of organisms from animals to plants reflects growing interest in feralization (see Glossary) [1.Gering E. et al.Getting back to nature: feralization in animals and plants.Trends Ecol. Evol. 2019; 34: 1137-1151Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar, 2.Fang M. et al.Contrasting mode of evolution at a coat color locus in wild and domestic pigs.PLoS Genet. 2009; 5e1000341Crossref PubMed Scopus (167) Google Scholar, 3.Page A. et al.Eggplant domestication: pervasive gene flow, feralization, and transcriptomic divergence.Mol. Biol. Evol. 2019; 36: 1359-1372Crossref PubMed Scopus (20) Google Scholar]. Although feral populations have fascinated researchers since Darwin, the demographic and selective processes that accompany feralization are not well characterized. Further, defining feral populations is difficult due to each population's unique life history (see Table 2 in [1.Gering E. et al.Getting back to nature: feralization in animals and plants.Trends Ecol. Evol. 2019; 34: 1137-1151Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar]). However, feral populations can be used to improve domesticated populations (Box 1) and offer opportunities to understand important concepts applicable to many different fields of study. These opportunities come with many potential confounders; temporal, geographic, and demographic in nature. In this forum, we showcase opportunities using feral populations to understand the complex processes involved in domestication and evolution, emphasizing the need to design powerful analyses that span both phylogenetics and population genomics to better understand the causal mechanisms underlying these processes.Box 1A Feral FutureAs the climate changes, there is increased interest in integrating locally adaptive variation from wild populations into domesticated species. We argue that feral populations may, in some cases, be better suited than wild relatives for studying complex biological process such as local adaption.Similar Genetic BackgroundsWe expect that a genetic background more similar to the domesticate would increase the efficiency of adaptive introgression. Beneficial mutations selected for in domesticates will likely be present in feral populations, provided they are not deleterious. Therefore, adaptive alleles (i.e., disease resistance) could be introgressed without large initial drops in productivity (i.e., yield), reducing the number of necessary backcrosses to achieve a breeding goal (i.e., disease-resistant high yielding).Locally AdaptedMost feral populations experience gene flow with related wild populations, producing areas of the genome enriched for adaptive variation that make them more fit in a given environment. When introgressed into domestic species, this variation may aid in their adaptation to environmental and climatic stressors.Precision IntrogressionBeneficial introgressed alleles will stand out more on feral genetic backgrounds than in wild populations. In identifying adaptive alleles, we can generate candidate loci for precision introgression into domestic populations using CRISPR or other gene editing techniques.RedomesticationWhile domestication for new species has been explored in the context of performing modern domestications of domestic species, it is relatively unexplored for feral populations. However, at least one example of a feral plant (cherry tomatoes [12.Bauchet G. Causse M. Genetic diversity in tomato (Solanum lycopersicum) and its wild relatives.in: Caliskan M. Genetic Diversity in Plants. InTech, 2012Crossref Google Scholar]) becoming redomesticated exists. As the climate changes, there is increased interest in integrating locally adaptive variation from wild populations into domesticated species. We argue that feral populations may, in some cases, be better suited than wild relatives for studying complex biological process such as local adaption. Similar Genetic Backgrounds We expect that a genetic background more similar to the domesticate would increase the efficiency of adaptive introgression. Beneficial mutations selected for in domesticates will likely be present in feral populations, provided they are not deleterious. Therefore, adaptive alleles (i.e., disease resistance) could be introgressed without large initial drops in productivity (i.e., yield), reducing the number of necessary backcrosses to achieve a breeding goal (i.e., disease-resistant high yielding). Locally Adapted Most feral populations experience gene flow with related wild populations, producing areas of the genome enriched for adaptive variation that make them more fit in a given environment. When introgressed into domestic species, this variation may aid in their adaptation to environmental and climatic stressors. Precision Introgression Beneficial introgressed alleles will stand out more on feral genetic backgrounds than in wild populations. In identifying adaptive alleles, we can generate candidate loci for precision introgression into domestic populations using CRISPR or other gene editing techniques. Redomestication While domestication for new species has been explored in the context of performing modern domestications of domestic species, it is relatively unexplored for feral populations. However, at least one example of a feral plant (cherry tomatoes [12.Bauchet G. Causse M. Genetic diversity in tomato (Solanum lycopersicum) and its wild relatives.in: Caliskan M. Genetic Diversity in Plants. InTech, 2012Crossref Google Scholar]) becoming redomesticated exists. Feralization, like domestication, is a process not an event [4.Larson G. Burger J. A population genetics view of animal domestication.Trends Genet. 2013; 29: 197-205Abstract Full Text Full Text PDF PubMed Scopus (154) Google Scholar], accompanied by incomplete transitions, admixture, and introgression [5.Allaby R.G. et al.The genetic expectations of a protracted model for the origins of domesticated crops.Proc. Natl. Acad. Sci. U. S. A. 2008; 105: 13982-13986Crossref PubMed Scopus (184) Google Scholar]. On the surface, feralization appears linear: a transition from cultivation to wild existence. In reality, it is a convoluted demographic process (Figure 1A ) involving extensive admixture and multiple reversions into and out of cultivation/husbandry [1.Gering E. et al.Getting back to nature: feralization in animals and plants.Trends Ecol. Evol. 2019; 34: 1137-1151Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar,4.Larson G. Burger J. A population genetics view of animal domestication.Trends Genet. 2013; 29: 197-205Abstract Full Text Full Text PDF PubMed Scopus (154) Google Scholar]. Feralized populations, most frequently, are not simply escaped, isolated domesticates existing in the wild. Rather, they are constantly admixing with natural, domestic, and other feral populations. This complex combination of processes makes disentangling the effects of domestication, local adaptation, and natural selection challenging. However, we argue that feral populations, combined with existing genomic resources from domesticated counterparts, are powerful models for understanding complex population changes not fully resolved by studying domesticated, wild, or ancient genomes alone. The transition of a population from domestic to feral is accompanied by a range of genetic, phenotypic, and demographic changes. The natural selection pressures placed on newly feral populations are twofold; a general shift in fitness optimum from domesticated to wild and local adaptation to a new environment outside of cultivation and husbandry. It is important to note that selective pressures on feral populations are not exclusively aimed at undoing the effects of domestication. Early evidence suggests that the specific genomic changes occurring during 'de-domestication' appear to be different from those targeted by domestication [3.Page A. et al.Eggplant domestication: pervasive gene flow, feralization, and transcriptomic divergence.Mol. Biol. Evol. 2019; 36: 1359-1372Crossref PubMed Scopus (20) Google Scholar]. That said, the phenotypic changes accompanying feralization typically make individuals appear more phenotypically similar to their wild ancestors (Figure 1A) [1.Gering E. et al.Getting back to nature: feralization in animals and plants.Trends Ecol. Evol. 2019; 34: 1137-1151Abstract Full Text Full Text PDF PubMed Scopus (24) Google Scholar]. The selection outcomes of domestication also determine how reversible the process is. If selective change was via sweeps, genotype reversal will be nearly impossible, but if domestication resulted from polygenic selection on complex traits, allele frequency changes will be easier to reverse. Regardless of the footprint of selection, the selection reversing phenotypes of feral populations may be acting on similar pathways and networks as domestication (Figure 1B). In the absence of local adaptation, we would expect that the major selective pressures on feral populations would be related to reversing low-fitness domestic phenotypes [6.Gering E. et al.Maladaptation in feral and domesticated animals.Evol. Appl. 2019; 12: 1274-1286Crossref PubMed Scopus (17) Google Scholar]. In a controlled setting, feralization would be sufficient to understand selection that occurs during domestication. However, as feral populations begin experiencing natural selection, we expect that local environmental stressors such as climate, geography, pathogens, parasites, and novel predators typically managed in agricultural contexts will exert different selective pressures on feral populations across landscapes. To discover both feral species-wide selection and local adaptation, future studies should perform broad geographic sampling of multiple feral subpopulations as well as wild and domesticated relatives. Without broad sampling across environments, it is impossible to distinguish novel 'de-domestication' signatures from those modulating local adaptation. Signatures of selection consistently identified across regional subpopulations are likely major drivers of feralization (Figure 1A). Additionally, using phylogenetics to determine the relationships between wild, cultivated, and feral populations will indicate the role of admixture. Traits under selection during domestication, and presumably feralization, are overwhelmingly complex in nature. Selection for tameness in animals is one crucial step towards domestication and has been repeatedly shown to be a highly complex trait, controlled by hundreds or thousands of genomic loci, only a few of which have moderate-to-large effects [7.Carneiro M. et al.Rabbit genome analysis reveals a polygenic basis for phenotypic change during domestication.Science. 2014; 345: 1074-1079Crossref PubMed Scopus (232) Google Scholar]. Therefore, we expect that the majority of resulting selection is polygenic in nature, where small shifts of allele frequency at hundreds or thousands of sites in the genome can drive large phenotypic changes [8.Höllinger I. et al.Polygenic adaptation: from sweeps to subtle frequency shifts.PLoS Genet. 2019; 15e1008035Crossref PubMed Scopus (44) Google Scholar]. This means that the sites targeted by domestication do not have to change during feralization to observe a wild-like phenotype. Further, most existing studies of both domestication and feralization have focused on a handful of large-effect selective sweeps. This shifts our focus away from polygenic selection, which likely plays an outsized role in the feralization process. Leveraging genomic resources designed for studying their agriculturally important domestic counterparts, we can begin to understand the genomic architectures involved not only in feralization, but also in domestication, natural selection, and local adaptation. Despite these signatures, the polygenic nature of many traits may not create these easily detectable sweeps. Low genotyping costs for species with single nucleotide polymorphism (SNP) arrays and imputation panels allow for high-powered datasets, capable of detecting small shifts in allele frequency [9.Rowan T.N. et al.Powerful detection of polygenic selection and environmental adaptation in US beef cattle populations.bioRxiv. 2020; (Published online May 8, 2020. https://doi.org/10.1101/2020.03.11.988121)PubMed Google Scholar]. Many of these species have developed detailed annotations, allowing for exploration of the functional genomic basis of these processes. Studies of feral populations have largely focused either on purely genomic or transcriptomic data, searching for selective sweeps or differential gene expression. To fully understand the biology underlying feralization, integrative approaches using combinations of phenotypic, genomic, transcriptomic, and epigenomic data will be essential. These approaches will allow us to begin exploring the networks that control traits essential to survival in the wild and under environment-specific stressors. When interpreting the changes that a population undergoes during feralization, it is important to consider the multitude of factors that can create confounding genetic or phylogenetic signals. We know that feralization events are characterized by repeated admixture between domesticated populations and introgression with wild relatives if in proximity to these populations. These complex phylogenetic signals, while common in natural systems, are difficult to tease apart as they will have differing amounts of shared haplotypes depending on timing since feralization and amount of introgression. However, feral populations afford unique opportunities to further dissect these complex evolutionary patterns due to the availability of well-developed genomic resources from their cultivated relatives. Identifying these introgression events can also shed light on initial domestication events by helping to tease apart true progenitor species from ferals [3.Page A. et al.Eggplant domestication: pervasive gene flow, feralization, and transcriptomic divergence.Mol. Biol. Evol. 2019; 36: 1359-1372Crossref PubMed Scopus (20) Google Scholar]. In some cases of introgression, the introgressed variant or variants may increase agricultural production or fitness, referred to as adaptive introgression [10.Burgarella C. et al.Adaptive introgression: an untapped evolutionary mechanism for crop adaptation.Front. Plant Sci. 2019; 10: 4Crossref PubMed Scopus (43) Google Scholar]. Adaptive introgression is well-documented in natural populations and is being further exploited as a method for increasing the adaptability of agricultural species [10.Burgarella C. et al.Adaptive introgression: an untapped evolutionary mechanism for crop adaptation.Front. Plant Sci. 2019; 10: 4Crossref PubMed Scopus (43) Google Scholar,11.Dempewolf H. et al.Past and future use of wild relatives in crop breeding.Crop Sci. 2017; 57: 1070-1082Crossref Scopus (224) Google Scholar]. While there are examples of crop species that have utilized wild variation to introgress adaptive variants into domesticated varieties, we suggest that feral populations may provide a better source for adaptive introgression (Box 1). Feral animal and plant populations offer exciting new avenues for research as well as potential sources to make cultivated plants and animals more locally adapted. The wealth of associated genomic data due to the relationships to domesticated populations, combined with thorough sampling, should prove feral populations to be powerful datasets to understand complex biological systems. No interests are declared. genetic mixture between two populations, which can create a new population. characteristics of organisms influenced by many environmental and genetic factors, including interactions between them. Complex traits are typically polygenic, meaning they are influenced by hundreds or thousands of genes. when a feral population forms from a domesticated population. when a feral population forms due to admixture between domesticated and wild populations. the process of a domesticated population transitioning to life outside of cultivation or husbandry. statistical inference of unobserved genotypes. selection resulting in changes at hundreds or thousands of loci. returning to an ancestral state. a single base pair difference between two chromosomes. The genotyping of these DNA variants can be automated using SNP arrays.