In 2019, the United Nations General Assembly adopted a resolution declaring 2021 to 2030 the UN Decade of Ecosystem Restoration. The aim of this designation was to support and expand “efforts to prevent, halt and reverse the degradation of ecosystems worldwide and raise awareness of the importance of successful ecosystem restoration” (UN G.A. Res. 72/284). Ecological restoration comes in many forms and can be applied to a variety of terrestrial, marine, and aquatic contexts. From its early days, ecological restoration has included a focus on genetic diversity and protecting and restoring ecosystems as a means of preserving genetic richness within and across taxa. During the past three decades, as DNA testing and analyses have grown increasingly capable of distinguishing fine differences between organisms, ecological restoration has turned to the molecular scale to evaluate the merits of protecting or restoring biodiversity at a genetic level. The genetic details of organisms ranging from bison and wolves to trees, toads, and trout have been scrutinized in recent years to advance restoration efforts and discern what “belongs” and what does not (Merkle et al. 2007; Pröhl et al. 2021; Robinson et al. 2019; Rutherford et al. 2019; Stroupe et al. 2022).
Synthesizing literature from the natural and social sciences, this article reviews and builds upon the rise in genetic and genomic thinking, or what geographer Elizabeth Hennessy (2015) has described as the “molecular turn” in conservation and restoration. Biodiversity has long been conceptualized as three interconnected yet distinct levels: genetic diversity, species diversity, and ecosystem diversity. With the emergence of new technologies over the past several decades, ecological restoration and conservation have experienced a shift toward the molecular scale, with genealogical lineages, species’ genomes, and genes themselves becoming key objects of concern and intervention (Allendorf et al. 2004; Bernos et al. 2020; Berseth 2022; Hennessy 2015; Metcalf et al. 2007, 2012; Robbins et al. 2023). When defined narrowly, genetics represents analyses that use small numbers of molecular markers and focus on individual genes, while genomics refers to the more recent shift to the use of large sets of molecular markers that enable the sequencing and study of entire genomes. In this article we discuss both genetics and genomics, and often use “genetic” as a shorthand adjective to refer to both genetic and genomic data, recognizing that the line dividing these analyses is often fuzzy and that both types of data shape restoration in new ways.
This article takes stock of genetic and genomic technologies and their relevance for ecological restoration. More specifically, we articulate how genetics and genomics have altered how we understand, classify, protect, and restore nature, and how and why certain populations, taxa, and ecosystems become identified as targets for intervention. In this review, we heed Lisa Campbell and Matthew Godfrey (2010) in their call for social scientists to immerse themselves in genetic science in order to study its implications for environmental governance. We empirically ground this discussion using the restoration and management of cutthroat trout (Oncorhynchus clarkii) populations in the Western United States as one key example, since aquatic ecosystems and trout present specific challenges in terms of restoration and genetics (Allendorf 1988; Helfman 2007), and across the Western United States have been a particular focus of genetic-related restoration and conservation efforts since the late 1980s.
In the following section, we reflect on key techniques and developments in the field of restoration genetics, describing in brief their implications for how we think about and manage nature. We then review existing literature that critiques a reductionist view of genes, and we consider how advancements in biotechnology and the new science of epigenetics may complicate how we think about genes and genomes in restoration. Finally, we explore alternative frameworks for integrating genetics into restoration and conservation in a way that recognizes other ways of knowing.
Genetics for Restoration and Conservation
Over the past half century, applications of genetics in restoration and conservation have expanded along with the development of molecular tools and techniques. Today, molecular techniques help to identify distinct or native populations (Amavet et al. 2023), reconstruct evolutionary histories (Ghazi et al. 2021), monitor invasive or introgressed species (O'Donnell et al. 2023), improve seed provenance choices (Bischoff et al. 2010), and modify organisms to improve their fitness (Newhouse and Powell 2021).
In the 1970s, the study of allozymes using electrophoresis first enabled researchers to empirically test the body of population genetics theory that had been growing over the past several decades (Allendorf 2017). Using allozymes, the amount of genetic variation within and between populations could be quantified, allowing researchers to identify populations with limited genetic variation or recent population bottlenecks (Leberg 1992). This was a crucial development that had significant implications for biodiversity conservation, making potential genetic risks to species’ persistence visible and measurable. For example, allozyme research in the early 1980s showed a marked lack of genetic variation in cheetah populations (O'Brien et al. 1983). This was hypothesized to be the result of a population bottleneck more than 10,000 years ago and interpreted as placing cheetahs at greater risk of extinction. Extensive scientific debate followed, with researchers disagreeing about the extent of the risk posed by cheetahs’ lack of genetic variation (Caughley 1994; May 1995; Merola 1994). In both the popular media and academic literature, genetic data was used as evidence supporting more intensive research, captive breeding, and recovery and restoration efforts focused on augmenting or maintaining genetic variation. Conversely, some interpreted the lack of genetic variation as evidence that the species is doomed to extinction, and therefore not warranting resources for its protection (O'Brien 1998). Each of these competing narratives emphasized cheetah genetics, diverting attention and resources from other issues facing the species, such as habitat loss, poaching, and the illegal wildlife trade. This emphasis on the molecular also works to reinforce the focus of conservation and restoration efforts on single species—often charismatic species like the cheetah—that are privileged above others in the same ecosystem.
Alongside allozymes, researchers began to analyze mitochondrial DNA (mtDNA), which proved particularly useful in reconstructing historical genealogical lineages and spurred the creation of the new field of phylogeography (Allendorf 2017). Together, allozymes and mtDNA initiated a transition in restoration and conservation that began in earnest in the 1980s: populations were now knowable as genetic entities. Genes themselves, as well as related concepts such as genetic divergence, gene flow, and genealogical lineages, were becoming objects of concern and intervention (Hennessy 2015). The newfound ability to reconstruct phylogenetic relationships based on mtDNA data also had implications for the concept of species and the practices of distinguishing species, contributing to a shift toward evolutionary and lineage concepts of species and away from morphological or biological (i.e., interbreeding) definitions of species (de Queiroz 1998; Freudenstein et al. 2017). As science-society scholars have noted, reducing restoration and conservation directives to the molecular scale relies on a view of genes as discrete, transferable bits of information that produce controllable and predictable traits (Barnes and Delborne 2022; Büscher et al. 2012; McAfee 2003; Rossi 2014). This leads to often-lethal decisions about wildlife populations, even as information about which genetics are “pure” for a given species or subspecies may be in flux.
For cutthroat trout in the Western United States, these scientific developments reconceptualized trout as genetic bodies, with the conservation value of populations now determined in large part by their genetic composition—their purity or lack of hybridization (i.e., genetic introgression)—but also by genetic divergence. In other words, the more genetically distinct a population is from others in the species, the more worthy of protection it becomes. Prior to the development of allozymes and mtDNA, patterns of genetic diversity in cutthroat trout were poorly understood, and fisheries managers and scientists struggled to determine how best to classify, manage, and conserve populations that looked generally similar but resided in different watersheds. Not only is the cutthroat trout a polytypic species, containing multiple subspecies, but it also can hybridize in the wild with rainbow trout (Oncorhynchus mykiss), as well as among different cutthroat subspecies.
Together, allozymes and mtDNA brought forward new understandings of cutthroat trout diversity and distribution, suggesting that there were more lineages of cutthroat trout than had been previously thought. The burgeoning molecular toolkit also enabled researchers and managers to quantify the extent of hybridization using criteria other than morphological differences. Findings about hybridization and genetic divergence between westslope cutthroat trout (Oncorhynchus lewisi) and other cutthroat trout species raised new conservation questions. Should hybridized populations receive protection under the Endangered Species Act? How should vulnerability be assessed for species that are widespread but often hybridized (Allendorf et al. 2004)? As with the cheetah, genetic threats to trout became more visible as technologies developed, and as a result they sometimes overshadowed broader threats of habitat degradation, water management, introduced species, climate change, and other challenges that aquatic species face.
The turn toward the molecular scale was hastened further by the development of polymerase chain reaction (PCR) techniques in the 1990s. For PCR analysis, researchers amplify small segments of DNA into millions to billions of copies, which can then be examined in detail. Using this process, researchers could measure genetic variation at the DNA level using other new techniques such as amplified fragment length polymorphism, microsatellites, and single nucleotide polymorphisms (Allendorf 2017).
More recently, next-generation sequencing (NGS) technologies have further revolutionized genetic approaches to restoration, enabling vast amounts of DNA to be sequenced rapidly and relatively inexpensively (Williams et al. 2014). An example of this is environmental DNA (eDNA) barcoding, in which DNA in environmental samples (e.g., air or water samples) is extracted and sequenced, and DNA sequences are then linked to taxonomic groups (Deiner et al. 2017). Initially eDNA was used primarily for single-species detection, but through NGS a few water samples may now essentially replace a time- and resource-intensive biodiversity census of an entire body of water or watershed, with the added benefit of minimal habitat disturbance (Evans and Lamberti 2018). Still, there are shortcomings of eDNA; for example, it does not provide a clear picture of population structure, fitness, condition of organisms, or spatial distribution. Additionally, it is particularly challenging to distinguish closely related species or subspecies and hybridized populations using eDNA (Evans and Lamberti 2018). For species such as cutthroat trout with unresolved taxonomies, high rates of hybridization, and local polymorphisms within subspecies, the deployment of eDNA is particularly challenging (Wilcox et al. 2015). Still, eDNA is now part of a suite of technologies used in trout restoration projects, for example by detecting survivors of fish removal projects and monitoring watersheds post-restoration (Carim et al. 2020).
Hybridization and Gene Flow
Since the 1990s, when the establishment of molecular markers began to allow for estimations of current and historical gene flow, a major thrust of restoration genetics has been the quantification of gene flow between species and within populations of the same species (McKay et al. 2005). Quantifying gene flow and, relatedly, measuring genetic diversity, is important for identifying and selecting source populations for translocations, evaluating restoration outcomes, and determining the appropriate scale for management (Campbell and Godfrey 2010; Mijangos et al. 2015). In some restoration contexts, gene flow between a targeted population and surrounding populations is considered a positive outcome, increasing population persistence and enhancing genetic diversity. In other contexts, gene flow may threaten the local adaptation of a population, potentially undermining population persistence, as in the case of outbreeding depression, or may result in hybridization between different species (McKay et al. 2005). Management centering on genetics faces a tension between encouraging habitat connectivity, thereby decreasing risks of genetic bottlenecks or vulnerability to stochastic events wiping out isolated populations, and isolating populations in the interest of protecting genetic lineages and purity.
Hybridization between native species and non-native or introduced species is a particular concern, as in the case of native cutthroat trout hybridizing with introduced rainbow trout in the Western United States. This form of gene flow is often framed as inherently negative, and in scientific literature the use of terms such as “genetic contamination” and “genetic pollution” has increased since the 1980s (Hirashiki et al. 2021; see also O'Brien 2006). Critiques of the use of terms such as “genetic purity,” “genetic contamination,” “genetic pollution,” and “genetic integrity” highlight their value-laden nature and/or roots in racist thinking (Biermann and Havlick 2021; Hirashiki et al. 2021; Rohwer and Marris 2015). However, ideas of “genetic purity” and “genetic integrity” remain central to the scientific and management lexicon concerning cutthroat trout, even if these same concepts are framed more subtly by designating populations for conservation or recreation priorities based on thresholds of genetic purity.
Concerns about hybridization have significant implications for how we think about and manage nature. On one hand, the threat of hybridization has been invoked in arguments against assisted migration and translocation, interventions that involve introducing taxa into new areas. Concerns about gene flow are also used to caution against “willy nilly genetic interventionism” (Peña-Guzmán et al. 2015: 259). On the other hand, concerns about hybridization may be accompanied by a sense of its inevitability. For some restoration advocates, this has led to increased support for novel forms of restoration that focus less on nativity of species and more on ecological function (Davis et al. 2011; Hirashiki et al. 2021; Rohwer and Marris 2016).
The view of hybridization as a profound threat is countered by the idea that gene flow among species may actually enhance evolutionary potential, reduce extinction risk, and/or improve resilience to environmental change (Brauer et al. 2023; Vallejo-Marín and Hiscock 2016). Claire Hirashiki and colleagues (2021) call for hybridization to be examined on a case-by-case basis. Rather than starting from the position that hybridization threatens species survival, they contend that potential positive effects on species survival or resilience should also be considered. Even in cases where hybridization is generally considered to be a threat rather than an asset, there are markedly different views about the level of risk that hybridization poses. This is the case in scientific literature about westslope cutthroat trout (Muhlfeld et al. 2009, 2017; Young et al. 2017), as well in responses to apparent inbreeding effects for the Bear Creek/greenback cutthroat trout in Colorado (Fendt 2019).
In thinking about hybridization and gene flow, social scientists have analyzed how conservation and restoration science function through biopolitical technologies (including genetics) that work to differentiate between “who or what is worthy of living—what kinds of biological diversity are promoted in conservation projects and what kinds are not” (Biermann and Mansfield 2014: 258). For example, Aurora Fredriksen (2015) discusses introgressive hybridization among Scottish wildcats and domestic feral cats, exploring how taxonomy and genetic analyses work to draw a line between unhybridized wildcats—which are cast as belonging and in need of protection—and wild cats that are hybridized or domestic—which are presented as threats in need of eradication. This biopolitical framework also analyzes how species-based approaches to conservation and restoration often run up against both care for individual organisms and “life's immanent, disorganising tendencies to ‘become otherwise’” (Fredriksen 2015: 690). In Fredriksen's research on wildcats, these “disorganizing tendencies” are the agencies of the cats themselves. In the example of cutthroat trout restoration, these dynamics might include fish that breach ecological barriers on their own, fish that escape death by moving to an isolated eddy during a piscicide treatment, wildfires that destroy barriers to fish passage, and so on. This biopolitical perspective suggests that even as genetics aims to make nature knowable and governable on the molecular scale, management efforts are constantly subverted: nature is never fully controlled or controllable.
These decisions about what forms of nature to protect, restore, or eradicate have spatial implications, as genetic data are mobilized in debates about appropriate scales for managing nature and establishment of conservation territories. In the traditional model of “fortress conservation,” nature is managed in bounded spaces such as national parks or wilderness areas, within which visions of a pristine past are attempted to be re-created or maintained (Adams 2004). This vision rests upon an assumption that these places were not previously inhabited or utilized by people, which in turn requires writing an array of Indigenous land uses and histories out of view (Jacoby 2001; Spence 1996, 1999; Wilson 2020). Bringing this down to the organismic scale, Hennessy (2015: 88) suggests that genetics has enabled the geography of pristine nature to be reimagined “as something manageable not only in Cartesian spaces, but also in the purity of species lineages.” In such cases, a particular landscape is not sought to be protected or restored to a pristine state, but instead the central focus becomes the “purity” or “integrity” of a particular genealogical lineage.
At some point, prioritizing genetic purity in ecological restoration and wildlife management will necessarily lead wildlife officials to determine how pure is pure enough to count for conservation. In the case of cutthroat trout, some states in the Western United States address this question by setting specific thresholds of genetic purity to classify trout populations’ conservation value. These efforts seek to set restoration and conservation goals objectively, but there remains some variability across states or species, and even standardized thresholds for genetic purity reflect numerical convenience (e.g., less than 1 percent or less than 10 percent introgressed) rather than precise ecological significance.
Besides the slightly different genetic standards applied to native trout management, and the question of how these numbers are established, the genetic testing itself may be imperfect. Techniques have improved over time, as we have already noted, but an influential study from 2005 reported that only about 15 percent of genetic samples in trout could be classified with a high degree of confidence (Shepard et al. 2005). Lacking a stable and reliable means of analysis, fish may face multiple rounds of eradication and restoration in an ongoing quest to establish truly “pure” populations.
A restoration project in Yellowstone National Park highlights some of these issues. Aquatic life in the park's rivers and lakes has been heavily modified since the mid-nineteenth century, particularly with the introduction of non-native rainbow trout, brown trout (Salmo trutta), and brook trout (Salvelinus fontinalis). The Park Service aims to reverse this trend, identifying sites where non-native or hybridized trout could be removed and restocked with native, unhybridized fish populations (Perkins 2020).
In 2005, the East Fork of Specimen Creek watershed was selected for Yellowstone's first westslope cutthroat trout restoration project with the goal of eliminating a population that was deemed “highly hybridized” (less than 80 percent pure) in order to restore unhybridized westslope cutthroat trout (Koel et al. 2006). The restoration required the construction of barriers to isolate the watershed; the elimination of all existing fish by applying rotenone, a piscicide that would be added in measured doses along the treatment areas of the watershed; and stocking the now-fishless waters with unhybridized westslope cutthroat trout from a combination of three wild sources and one brood raised in a nearby hatchery managed for precisely these kinds of restoration efforts.
In 2018 and 2019, approximately six years after the last translocation of “genetically pure” fish into East Fork Specimen Creek, the watershed was sampled to evaluate the success of restoration efforts. Unexpectedly, of 290 successfully genotyped fish, 11.5 percent were determined to be hybrids with a combination of westslope cutthroat trout alleles and Yellowstone cutthroat trout (Oncorhynchus clarkii bouvieri) and/or rainbow trout alleles (Puchany 2021). This seemed to indicate that hybridization and genetic introgression were occurring due to fish breaching a barrier and invading from downstream, or from incomplete eradication of hybrids during the rotenone phase. In considering next steps, Andriana Puchany (2021) concluded that complete re-treatment of the watershed using piscicides, followed by re-stocking of “genetically pure” fish, was likely required.
This situation raises uncomfortable questions about genetics-driven restoration decisions, both for what these lead to intentionally and for the impacts on other organisms that can be overlooked by managers. The lethal effects of rotenone on target fish are relatively well documented, but research less often accounts for the impacts of this piscicide on a variety of other organisms ranging from zooplankton and macroinvertebrates to amphibians and non-target fish species (Beaulieu et al. 2021; Billman et al. 2011; Dalu et al. 2015). A single-species focus in restoration projects risks disregarding the complexity and variety of organisms that may be impacted by rotenone.
Focusing more directly on the intended impacts of rotenone treatments, it seems important to ask, how many rounds of treatment and monitoring are required to successfully establish and maintain unhybridized, “pure” populations? Indeed, can we expect the need for monitoring and treatment to ever end? How many hybridized fish populations ought fisheries managers be willing to sacrifice to establish one that is unhybridized? And more broadly, how did we arrive at this juncture, where genes have become the target of restoration initiatives? What are the broader implications of this shift toward the molecular scale in restoration and environmental governance?
These and related questions rise to the fore as new genetic and genomic tools clarify the differences between trout lineages. This has moved the object of concern from specific rivers or habitats toward populations with the purest (i.e., least hybridized) genes. There are spatial implications to this shift, as unhybridized populations are often found in isolated streams that have been disconnected from downstream waters through human modifications of the landscape, such as roads, culverts or dams (Biermann and Havlick 2021). In many restoration projects, genetic isolation is required to protect a restored population from hybridization. This necessitates the establishment of barriers that prevent fish from moving into the waterway from either upstream or downstream, an intervention that again privileges a single species and de-emphasizes or even potentially harms other taxa, such as invertebrates and amphibians.
This downscaling of restoration spurred by concerns about hybridization is potentially at odds with longstanding ideas in conservation biology that promote landscape connectivity through conservation corridors, mega-reserves, and networks of protected areas. In other cases, genetic data are mobilized to support the scaling up of conservation beyond local or national management and toward international management (Campbell and Godfrey 2010). When genetic analyses indicated linkages among geographically disparate sea turtles in the Caribbean Sea (e.g., linking foraging populations to distant nesting populations), researchers and conservationists used this data to make the case for managing sea turtles as a common pool resource that required conservation at an international level. Such scaling up, however, served to write certain actors and communities out of the governance process (Campbell 2007), largely bypassing the communities that were “living with, using, and conserving sea turtles” (Campbell and Godfrey 2010: 905).
Genes as Discrete and Separable Units
One of the key questions surrounding the molecular turn in conservation and ecological restoration is the degree to which genes are treated as discrete, transferable bits of information (Hennessy 2015; McAfee 2003; Rossi 2014; Valve 2011). Geographer Kathleen McAfee examined how genes are often conceptualized as discrete entities: “functional units of information which can be characterized precisely, counted, added or subtracted, altered, switched on and off, or moved from one organism or one species to another” (McAfee 2003: 204). Despite scientific evidence that supports a more complex understanding of genes and genomes, this reductionist genetic discourse continues to circulate in various fields, from agriculture and biotechnology to conservation and restoration. For example, the powerful field of synthetic biology embraces genes as severable or distinct units, where genetic parts, or short sequences of DNA, can be moved, created, inserted, or modified to produce organisms with new characteristics, increased resilience to adverse environmental factors, or even to create entirely novel forms of life. However, despite claims that biotechnology “permits precise control of life processes” (McAfee 2003: 203), the process is far messier and more complex than its nano-precision would suggest.
McAfee's critique of operating at the molecular scale centers largely on agriculture and genetic engineering, but many of the same concerns can be translated to other contexts such as ecological restoration and biodiversity conservation. Genetic reductionism can abstract genes from nature with its “spatial and temporal specificity . . . and from the environmental and social contexts in which [it] co-evolves” (McAfee 2003: 204). A similar critique has been made about how genetic and genomic concepts of indigeneity reduce ancestry to genetic ancestry, thus abstracting genetics from “biological and cultural kinship constituted in dynamic, long-standing relations with each other and with living landscapes” (TallBear 2013: 509). In this way, reducing our understanding of organisms to a genetic level can be seen as a turn farther afield from Indigenous or relational perspectives of socioecological connectivity (Todd 2014; Trigger et al. 2008).
With respect to environmental governance, when organisms and species are classified by and managed primarily for their genetic composition, other aspects of their identities, such as life histories and ecological relationships, may be obscured or overlooked (Havlick and Biermann 2021). For some species, establishing standards of genetic purity can abstract these organisms from what are often rich eco-social histories of particular populations. In addition, life-and-death decisions about wildlife populations may then be predicated on an outdated and overly deterministic view of genes. With this, the conservation value of populations is determined by genetic composition.
According to McAfee, the reductionist view of genes-as-information also contributes to an economic reductionism that allows genetic information to be patented and commodified down to the molecular scale. For example, if organisms are modified through genetic engineering or created through synthetic biology, these entities may then be subject to proprietary claims for patenting, monetization, or the commodification of what previously were viewed as natural systems (and thus seemingly beyond the reach of complete human control). This raises concerns about neoliberal entrainment or market capture of nature and may facilitate unconstrained assertions of lethal control over these newly modified or hybrid ecosystems. Whether designed with this in mind or not, genetic-focused interventions can contribute both to neoliberal biodiversity conservation (Büscher et al. 2012; cf Barnes and Delborne 2022) and an expansion and deepening of human control over living organisms—what some consider a problematic extension of biopower reaching down to the building blocks of life (Lorimer 2015; Preston 2019). This sense of control, however, may indeed be false, as it not only relies on a reductionist view of genetics but also underestimates nonhuman agency and dynamism.
One example of how the commodification and marketization of genetic information is deployed comes from an initiative by the International Union for the Conservation of Nature and a technology start-up company, NatureMetrics. The eBioAtlas1 seeks to respond to the loss of biodiversity in aquatic systems and wetlands by developing comprehensive inventories of existing biota, utilizing tens of thousands of eDNA samples gathered across the world. Generating a global atlas of DNA found in freshwater ecosystems, the project will “target areas threatened by climate change and development, and rapidly fill in critical gaps in knowledge to support conservation efforts, unlock business investment to protect the natural world, and build a rich databank to inform global policy to reverse the rapid decline in biodiversity” (NatureMetrics 2021). NatureMetrics promotes itself as a “global leader in using eDNA to turn nature into data” (Cruickshanks and Czachur 2021). Businesses are expected to pay to access this data and fund areas that are important to their operations or supply chains. In this way, genetic data are actively monetized while also, at least prospectively, contributing to ecological restoration and conservation efforts.
Although eBioAtlas promoters position their effort as a win-win, good for business and good for biodiversity, critiques of this type of approach hinge not just on the commodification of nature, but also on its reliance on genes as authoritative bit of information. McAfee argues that while convenient, treating the gene as a unitary site conveying a genetic “code” is highly problematic (see also Kay 2000), as the gene's “ontological status as a discrete causal unit of heredity is increasingly in doubt” (McAfee 2003: 205). Other social analyses of genetics in restoration have suggested that not all restoration practices rely on this same reductionism. Geographer Jairus Rossi describes genes as “contextual and contingent entities” and suggests that certain kinds of restoration practices can push against a reductionist view of genetic information and instead lead to a view of genes as “embodied relational entities, rather than abstract information” (2014: 66). According to Rossi, this view can contribute to a decommodification of genetic knowledge and promote more relational or socioecological restoration practices.
Epigenetics and Conservation
Another challenge of working through a strict genetic lens for restoration and conservation is the growing understanding of epigenetics. Epigenetics is the study of heritable changes in the ways genes work that are not associated with changes in the underlying structure or pattern of DNA in the genetic code. In other words, epigenetics shows how environment and behavior can affect an organism's expression of genes in ways that can be passed down to future generations. This has contributed to what some consider a post-genomic science or a rejection of genetic determinism (Lehrner and Yehuda 2018; Mansfield and Guthman 2014). In one sense, epigenetics counters the abstraction at work in reductionist understanding of genetics, re-embedding genes within their biological and social environments. However, as critical analyses of epigenetic science have shown, a non-deterministic view of genes may still reinforce eugenic logics about biological differences in human populations (Mansfield and Guthman 2014).
Much of the epigenetic research has focused on human effects, but studies in lab animals have contributed substantially to understanding epigenetic effects, leading to calls to incorporate conservation epigenetics in biodiversity protection (Rey et al. 2020). In recent years, a relative flurry of articles has brought epigenetics into conversation with biodiversity conservation (Amaral et al. 2020; Angers et al. 2020; Pazzaglia et al. 2021; Segelbacher et al. 2022; Theissinger et al. 2023). With epigenetic impacts such as DNA methylation likely showing greater responsiveness to short-term environmental changes, intraspecific epigenetic diversity may be underappreciated and a new front for restoration and conservation of biodiversity (Rey et al. 2020). Fish raised in hatcheries for restoration, for example, have been shown to experience rapid epigenetic modifications that lead to reduced fitness once released in the wild (Le Luyer et al. 2017). As such, epigenetics may complicate existing genetics-focused restoration strategies that rely on raising “genetically pure” local broodstock in hatcheries.
Attending to epigenetics does not necessarily expand the focus of ecological restoration to broader or more integrative approaches, but may facilitate more diverse ontological framings, including blurred socio-natural constructions that lead to different pathways to restoring biodiversity (Meloni et al. 2022). With interest in epigenetics seemingly on the rise, it remains to be seen how ready or able restoration ecologists and wildlife managers are to transfer these more nuanced, potentially reversible features of ecosystems into practice.
Biotechnology, Genetic Engineering, and Synthetic Biology
With advances in biotechnology and synthetic biology, geneflow between organisms is now possible not only through happenstance or painstaking programs of intentional breeding but also through techniques such as genetic engineering and, more recently, gene editing. Gene editing via CRISPR and similar techniques increasingly allows scientists to micromanage genetic composition and diversity within and between organisms, snipping and replacing original genetic material with influential bits from disparate other organisms or, in some cases, from entirely synthesized sources (Piaggio et al. 2017; Preston 2019; Redford and Adams 2021; Redford et al. 2014).
The use of biotechnology to alter genetic material within organisms and populations continues to stir controversy; some view it as a potent new resource in restoration ecologists’ toolbox (e.g., Barnhill-Dilling and Delborne 2019), while others raise concerns that meddling with genetic foundations risks unforeseen consequences and destabilizes long-standing notions of what is natural versus human-generated artifacts (Calvert 2010; Kolisis 2021). Even as debates persist surrounding the merits of modifying and synthesizing life forms to better withstand changing climates, degraded habitats, or other factors that imperil biodiversity, a growing array of organisms produced through biotechnology (from older techniques such as gene transfers through bacteria or virus vectors to newer gene editing techniques such as CRISPR) suggest that advances in biotechnology are outpacing ethical or ecological concerns (Preston 2019).
Fully synthetic organisms have yet to be deployed in wild ecosystems, but it may only be a matter of time before these lab creations are released, whether intentionally or not, into what have been considered “natural” settings (Popkin 2018). US scientists created the world's first organism with a synthetic genome in 2010, and less than a decade later British researchers announced the creation of the world's first organism made from DNA that was entirely synthetic (Sample 2019). Applications of synthetic biology currently underway range from the de-extinction of species such as the passenger pigeon and woolly mammoth to managing (or eradicating) malarial mosquitoes and introduced Norway rat populations in island ecosystems (e.g., Piaggio et al. 2017).
Although synthetic biology has yet to be deployed for native trout restoration, genetic engineering via bacteria or virus vectors or gene editing tools could potentially be used either to remove undesirable material, such as rainbow trout DNA in cutthroat species, or to add new diversity to the genes of native species in order to boost resiliency or help these organisms adapt to changing habitat conditions, such as warmer water temperatures. The genetic makeup of trout is already altered through less invasive, established methods as well. Since the early 1980s, fisheries scientists have heat-shocked trout to create triploid fish that develop an extra, third set of chromosomes, rendering them sterile (Rohrer and Thorgaard 1986). In this way, fisheries managers have relied on genetic manipulation to stock triploid hatchery fish and reduce risks of introgression with native trout, or to gradually eradicate non-native trout without resorting to piscicides.
Alternative Frameworks for Using Genetics in Restoration
As we have shown, genetic science has changed not only how nature is understood but also how it is governed, by whom, and at what scale. Genetic analyses are used to decide the value of organisms and populations and to justify life-and-death decisions, sometimes despite incomplete knowledge or at the expense of other species or other forms of knowledge or values. This is not to say that genetic techniques should be jettisoned, or that genetic knowledge is always used in a singular fashion. Rather, a lesson we take from this review is that the science of genetics—including the advancing fields of epigenetics and synthetic biology—provides a partial perspective on the world (Haraway 1988). In this final section we explore visions of ecological restoration and conservation that are epistemologically diverse, and that do not necessarily prioritize genetic science over other values or ways of knowing. As Campbell and Godfrey (2010: 905) argue, “Any decision that this way of knowing is the best, only, or natural way, in essence replacing or at least out-weighing other ways, is ultimately a human and political decision.” Genetics may help us understand evolutionary patterns, interrelationships between populations or organisms, reproductive fitness, and fine distinctions between different types of organisms, but it alone cannot tell us “whether or not particular outcomes are acceptable nor whether or not they are sustainable” (Campbell and Godfrey 2010: 905). What does a culture of ecological restoration look like when we recognize that genetics alone cannot provide an answer key for the difficult, value-laden decisions that comprise restoration and environmental governance? When genetic science is treated as the central arbiter of truth about a population or ecosystem, what other opportunities, forms of knowledge, or actors are disregarded or obscured?
To begin to address these questions, it is helpful to understand the broader context of social research on restoration and conservation. Chris Sandbrook and colleagues (2013) distinguished between social research for conservation and social research on conservation. Research for conservation is driven by the mission to conserve biological diversity and seeks to improve existing conservation policy and practice. Research on conservation may come from various other starting points and generally works to “understand how conservation as a social, political practice works” and “to situate conservation with respect to broader social and political economic issues” (Sandbrook et al. 2013: 1488). A similar heuristic could be applied to research on and for ecological restoration. Conservation and restoration professionals often look explicitly to research for conservation/restoration to guide management actions, and research on conservation and restoration may be viewed as unnecessarily critical, opaque, unhelpful, or even antagonistic to the broader mission.
A more holistic and robust approach to ecological restoration dissolves this dichotomy, insisting that research for restoration should also reflect on the context in which it is produced and the broader social, political, ecological, and economic networks in which it is embedded. Yet conversations about the science of restoration genetics and critical reflections on genetics in restoration and conservation have by and large proceeded separately. Natural and social scientists are often siloed in conducting research, reporting findings, and intersecting with agency officials and practitioners. Rather than thinking of research on and for restoration as separate, we envision integrating these domains to bring the insights of critical social science into the practices of natural science and ecological restoration.
While there is a growing literature of examples of this type of boundary-crossing work (Keeve et al. 2021; Sinner et al. 2022), critical physical geography provides one possible framework through which to integrate genetic knowledge and restoration science with diverse approaches such as feminist science studies, Indigenous knowledge, and queer and trans theory (Lave et al. 2018; Wölfle Hazard 2022). The three tenets of critical physical geography provide a useful starting point for this integration. First, we must recognize that genetics are deeply shaped by human activities and social power relations. The genetic composition of populations, the genomic structure of species, and the distribution of genes across space, have been fundamentally shaped by people. We therefore can interpret genetic data in connection with human values, actions, and social dynamics—including, but not limited to, Indigenous land uses, settler colonialism, Western science, and conflict and warfare (e.g., Darimont and Pelletier 2021). Second, the same social dynamics and power relations that have shaped the distribution of genes across space also shape who studies genetics and how they are studied. The methods and techniques previously discussed—from allozymes to epigenetics—have not emerged out of a vacuum but are themselves shaped by social power relations in ways that affect the types of questions that are asked, the scales at which questions are analyzed and answered, and the forms of knowledge that are accepted in governance and decision making. Finally, this approach recognizes that genetic knowledge has deep impacts on the organisms it purports to know as well as the other species with whom they interact in an ecosystem.
Starting from these assumptions, it is possible to build a more expansive form of restoration that is both more collaborative, interdisciplinary, community-grounded and epistemically diverse. The “underflows” approach of Cleo Wölfle Hazard is illustrative: with Western scientists, native communities and scientists, and community activists, Wölfle Hazard (2022) practices a collaborative river restoration science rooted in ethics of reciprocity, community benefit, and respect for multiple forms of knowledge. Thinking about genetics, this could mean that research starts from a place where the authority of genetic science is not “universal or unquestioned, but neither is science dismissed out of hand” (Wölfle Hazard 2022: 26). It may also lead researchers to follow principles of Indigenous data sovereignty in conservation and restoration genetics (Robbins et al. 2023), and to develop opportunities for idea generation and communication across difference (such as the ecocultural restoration field school cocreated by Wölfle Hazard and research partners). These possibilities are not the focus of this article, but we mention them here as potential pathways for incorporating both genetic data and critiques of genetics into restoration, in ways that “see, recognize, and reach out for different streams—dissident streams, decolonizing upwellings that rework science and governance from within but also from below—into a lively, muddy, organic machine” (Wölfle Hazard 2022: 31). Restoration ecology has long positioned itself as an integrative field that accommodates the contributions of natural and physical scientists, social scientists, environmental philosophers, and contributors from the humanities. In light of the molecular turn and conservation genetics, restoration scholars and practitioners should continue to embrace this tradition, engaging across disciplines and social differences, opening to new ways of knowing, and recognizing that genetics is one of many modes of valuing and relating to other species.
Acknowledgments
We appreciate the reviewers’ and editor's helpful and constructive feedback. This material is based upon work supported by the National Science Foundation under Grant No. SES-1922157.
References
Adams, William. 2004. Against Extinction: The Story of Conservation. London: Earthscan.
Allendorf, Fred W. 1988. “Conservation Biology of Fishes.” Conservation Biology 2 (2): 145–148. https://doi.org/10.1111/j.1523-1739.1988.tb00165.x
Allendorf, Fred W. 2017. “Genetics and the Conservation of Natural Populations: Allozymes to Genomes.” Molecular Ecology 26 (2): 420–430. https://doi.org/10.1111/mec.13948
Allendorf, Fred W., Robb Leary, Nathaniel Hitt, Nathaniel, Kathy Knudsen, Laura Lundquist, and Paul Spruell. 2004. “Intercrosses and the US Endangered Species Act: Should Hybridized Populations be Included as Westslope Cutthroat Trout?” Conservation Biology 18 (5): 1203–1213. https://doi.org/10.1111/j.1523-1739.2004.00305.x
Amaral, Joana, Zoé Ribeyre, Julien Vigneaud, Mamadou D. Sow, Régis Fichot, Christian Messier, Gloria Pinto, Philippe Nolet, and Stéphane Maury. 2020. “Advances and Promises of Epigenetics for Forest Trees.” Forests 11 (9): 976–997. https://doi.org/10.3390/f11090976
Amavet, Patricia, Gisela Poletta, Lucía Odetti, María Virginia Parachú Marcó, and Pablo Siroski. 2023. “Detection of the Maned Wolf, a Cryptic and Vulnerable Species, Through Environmental DNA Studies.” Journal for Nature Conservation: 126439. https://doi.org/10.1016/j.jnc.2023.126439.
Angers, Bernard, Maëva Perez, Tatiana Menicucci, and Christelle Leung. 2020. “Sources of Epigenetic Variation and Their Applications in Natural Populations.” Evolutionary Applications 13 (6): 1262–1278. https://doi.org/10.1111/eva.12946
Barnes, Jessica C., and Jason A. Delborne. 2022. “The Politics of Genetic Technoscience for Conservation: The Case of Blight-Resistant American Chestnut.” Environment and Planning E: Nature and Space 5 (3): 1518–1540. https://doi.org/10.1177/25148486211024910
Barnhill-Dilling, S. Kathleen, and Jason A. Delborne. 2019. “The Genetically Engineered American Chestnut Tree as Opportunity for Reciprocal Restoration in Haudenosaunee Communities.” Biological Conservation 232: 1–7. https://doi.org/10.1016/j.biocon.2019.01.018.
Beaulieu, J., D. Trépanier-Leroux, J. M. Fischer, M. H. Olson, S. Thibodeau, S. Humphries, D. J. Fraser, and A. M. Derry. 2021. “Rotenone for Exotic Trout Eradication: Nontarget Impacts on Aquatic Communities in a Mountain Lake.” Lake and Reservoir Management 37 (3): 323–338. https://doi.org/10.1080/10402381.2021.1912864
Bernos, Thaïs A., Ken M. Jeffries, and Nicholas E. Mandra. 2020. “Linking Genomics and Fish Conservation Decision Making: A Review.” Reviews in Fish Biology and Fisheries 30 (4): 587–604. https://doi.org/10.1007/s11160-020-09618-8
Berseth, Valerie. 2022. “In Pursuit of Wildness: Genomic Science, Risk, and the Production of Wild Salmon.” PhD diss., University of British Columbia.
Biermann, Christine, and Becky Mansfield. 2014. “Biodiversity, Purity, and Death: Conservation Biology as Biopolitics.” Environment and Planning D: Society and Space 32 (2): 257–273. https://doi.org/10.1068/d13047p
Biermann, Christine, and David G. Havlick. 2021. “Genetics and the Question of Purity in Cutthroat Trout Restoration.” Restoration Ecology 29 (8): e13516. https://doi.org/10.1111/rec.13516.
Billman, Hilary G., Sophie St-Hilaire, Carter G. Kruse, Teri S. Peterson, and Charles R. Peterson. 2011. “Toxicity of the Piscicide Rotenone to Columbia Spotted Frog and Boreal Toad Tadpoles.” Transactions of the American Fisheries Society 140 (4): 919–927. https://doi.org/10.1080/00028487.2011.599260
Bischoff, Armin, Thomas Steinger, and Heinz Müller-Schärer. 2010. “The Importance of Plant Provenance and Genotypic Diversity of Seed Material Used for Ecological Restoration.” Restoration Ecology 18 (3): 338–348. https://doi.org/10.1111/j.1526-100X.2008.00454.x
Brauer, Chris J., Jonathan Sandoval-Castillo, Katie Gates, Michael P. Hammer, Peter J. Unmack, Louis Bernatchez, and Luciano B. Beheregaray. 2023. “Natural Hybridization Reduces Vulnerability to Climate Change.” Nature Climate Change 13 (3): 282–289. https://doi.org/10.1038/s41558-022-01585-1
Büscher, Bram, Sian Sullivan, Katja Neves, Jim Igoe, and Dan Brockington. 2012. “Towards a Synthesized Critique of Neoliberal Biodiversity Conservation.” Capitalism, Nature, Socialism 23 (2): 4–30. https://doi.org/10.1080/10455752.2012.674149
Calvert, Jane. 2010. “Synthetic Biology: Constructing Nature?” The Sociological Review 58 (1): 95–112. https://doi.org/10.1111/j.1467-954X.2010.01913.x
Campbell, Lisa M. 2007. “Local Conservation Practice and Global Discourse: A Political Ecology of Sea Turtle Conservation.” Annals of the Association of American Geographers 97 (2): 313–334. https://doi.org/10.1111/j.1467-8306.2007.00538.x
Campbell, Lisa M., and Matthew H. Godfrey. 2010. “Geo-Political Genetics: Claiming the Commons through Species Mapping.” Geoforum 41 (6): 897–907. https://doi.org/10.1016/j.geoforum.2010.06.003
Carim, K. J., N. J. Bean, J. M. Connor, W. P. Baker, M. Jaeger, M. P. Ruggles, K. S. McKelvey, T. W. Franklin, M. K. Young, and M. K. Schwartz. 2020. “Environmental DNA Sampling Informs Fish Eradication Efforts: Case Studies and Lessons Learned.” North American Journal of Fisheries Management 40 (2): 488–508. https://doi.org/10.1002/nafm.10428
Caughley, Graeme. 1994. “Directions in Conservation Biology.” Journal of Animal Ecology: 215–244. https://doi.org/10.2307/5542.
Cruickshanks, Katie, and Molly Czachur. 2021. “Turning Nature Into Data With NatureMetrics,” news release, April 7, https://www.naturemetrics.com/2021/04/07/turning-nature-into-data-with-naturemetrics/ (accessed 1 June 2023).
Dalu, Tatenda, Ryan J. Wasserman, Martine Jordaan, William P. Froneman, and Olaf Weyl. 2015. “An Assessment of the Effect of Rotenone on Selected Non-Target Aquatic Fauna.” PLoS One 10 (11): e0142140. https://doi.org/10.1371/journal.pone.0142140.
Darimont, Chris T., and Fanie Pelletier. 2021. “Of War, Tusks, and Genes.” Science 374 (6566): 394–395. https://doi.org/10.1126/science.abm2980
Davis, Mark A., Matthew K. Chew, Richard Hobbs, Ariel E. Lugo, John Ewel, Geerat Vermeij, James Brown, Mark R. Gardener, Scott Carroll, Ken Thompson, Steward Pickett, Juliet Stromberg, Peter Del Tredici, Katharine Suding, Joan Ehrenfeld, J. Philip Grime, Joseph Mascaro, and John Briggs. 2011. “Don't Judge Species on their Origins.” Nature 474 (7350): 153–154. https://doi.org/10.1038/474153a
Deiner, Kristy, Holly Bik, Elvira Mächler, Mathew Seymour, Anaïs Lacoursière-Roussel, Floria Altermatt, Simon Creer, Iliana Bista, David Lodge, Natasha De Vere, Michael Pfrender, and Louis Bernatchez. 2017. “Environmental DNA Metabarcoding: Transforming How We Survey Animal and Plant Communities.” Molecular Ecology 26 (21): 5872–5895. https://doi.org/10.1111/mec.14350
de Queiroz, Kevin. 1998. “The General Lineage Concept of Species, Species Criteria, and the Process of Speciation.” In Endless Forms: Species and Speciation, ed. Howard Daniel and Berlocher Steward, 57–75. Oxford: Oxford University Press.
Evans, Nathan, and Gary Lamberti. 2018. “Freshwater Fisheries Assessment Using Environmental DNA: A Primer on the Method, Its Potential, and Shortcomings as a Conservation Tool.” Fisheries Research 197: 60–66. https://doi.org/10.1016/j.fishres.2017.09.013.
Fendt, Lindsay. 2019. “Resurrecting the Greenback, Take Two.” Biographic, 7 February. https://www.biographic.com/resurrecting-the-greenback-take-two/.
Fredriksen, Aurora. 2015. “Of Wildcats and Wild Cats: Troubling Species-Based Conservation in the Anthropocene.” Environment and Planning D: Society and Space 34 (4): 689–705. https://doi.org/10.1177/0263775815623539
Freudenstein, John, Michael Broe, Ryan Folk, and Brandon Sinn. 2017. “Biodiversity and the Species Concept: Lineages Are Not Enough.” Systematic Biology 66 (4): 644–656. https://doi.org/10.1093/sysbio/syw098
Ghazi, Mirza Ghazanfarullah, Surya Prasad Sharma, Chongpi Tuboi, Sangeeta Angom, Tennison Gurumayum, Parag Nigam, and Syed Ainul Hussain. 2021. “Population Genetics and Evolutionary History of the Endangered Eld's Deer with Implications for Planning Species Recovery.” Scientific Reports 11 (1): 2564. https://doi.org/10.1038/s41598-021-82183-7.
Haraway, Donna. 1988. “Situated Knowledges: The Science Question in Feminism and the Privilege of Partial Perspective.” Feminist Studies 14 (3): 575–599. https://doi.org/10.2307/3178066
Havlick, David, and Christine Biermann. 2021. “Wild, Native, or Pure: Trout as Genetic Bodies.” Science, Technology, and Human Values 46 (6): 1201–1229. https://doi.org/10.1177/0162243920978307
Helfman, Gene. 2007. Fish Conservation: A Guide to Understanding and Restoring Global Aquatic Biodiversity and Fishery Resources. Washington, DC: Island Press.
Hennessy, Elizabeth. 2015. “The Molecular Turn in Conservation: Genetics, Pristine Nature, and the Rediscovery of an Extinct Species of Galápagos Giant Tortoise.” Annals of the Association of American Geographers 105 (1): 87–104. https://doi.org/10.1080/00045608.2014.960042
Hirashiki, Claire, Peter Kareiva, and Michelle Marvier. 2021. “Concern Over Hybridization Risks Should Not Preclude Conservation Interventions.” Conservation Science and Practice 3 (4): e424. https://doi.org/10.1111/csp2.424.
Jacoby, Karl. 2001. Crimes Against Nature: Squatters, Poachers, Thieves, and the Hidden History of American Conservation. Berkeley: University of California Press.
Kay, Lily E. 2000. Who Wrote the Book of Life?: A History of the Genetic Code. Stanford: Stanford University Press.
Keeve, Christian, Erin Clancy, Karen Kinslow, and Kallista Bley. 2021. “Meandering through Critical Restoration Geographies: A Reading Group Collective.” Antipode Online. https://antipodeonline.org/2021/10/15/critical-restoration-geographies/.
Koel, Todd, Jeffrey Arnold, Patricia Bigelow, Philip Doepke, Brian Ertel, Daniel Mahony, and Michael Ruhl. 2006. Yellowstone Fisheries & Aquatic Sciences: Annual Report, 2005. National Park Service, Yellowstone Center for Resources, Yellowstone National Park, Wyoming, YCR-2006-09.
Kolisis, Nikolaos, and Fragiskos Kolisis. 2021. “Synthetic Biology: Old and New Dilemmas—The Case of Artificial Life.” BioTech 10 (3): 16. https://doi.org/10.3390/biotech10030016.
Lave, Rebecca, Christine Biermann, and Stuart N. Lane. 2018. The Palgrave Handbook of Critical Physical Geography. Palgrave: London.
Le Luyer, Jeremy, Martin Laporte, Terry D. Beacham, Karia H. Kaukinen, Ruth E. Withler, Jong S. Leong, Eric B. Rondeau, Ben F. Koop, and Louis Bernatchez, 2017. “Parallel Epigenetic Modifications Induced by Hatchery Rearing in a Pacific Salmon.” Proceedings of the National Academy of Sciences 114 (49): 12964–12969. https://doi.org/10.1073/pnas.1711229114
Leberg, Paul L. 1992. “Effects of Population Bottlenecks on Genetic Diversity as Measured by Allozyme Electrophoresis.” Evolution 46 (2): 477–494. https://doi.org/10.1111/j.1558-5646.1992.tb02053.x
Lehrner, Amy, and Rachel Yehuda. 2018. “Cultural Trauma and Epigenetic Inheritance.” Development and Psychopathology 30: 1763–1777. https://doi.org/10.1017/S0954579418001153.
Lorimer, Jamie. 2015. Wildlife in the Anthropocene: Conservation After Nature. Minneapolis: University of Minnesota Press.
Mansfield, Becky, and Julie Guthman. 2014. “Epigenetic Life: Biological Plasticity, Abnormality, and New Configurations of Race and Reproduction.” Cultural Geographies 22 (1): 3–20. https://doi.org/10.1177/1474474014555659
May, Robert M. 1995. “The Cheetah Controversy.” Nature 374: 309–310. https://doi.org/10.1038/374309a0.
McAfee, Kathleen. 2003. “Neoliberalism on the Molecular Scale: Economic and Genetic Reductionism in Biotechnology Battles.” Geoforum 34 (2): 203–219. https://doi.org/10.1016/S0016-7185(0200089-1).
McKay, John K., Caroline E. Christian, Susan Harrison, and Kevin J. Rice. 2005. “How Local Is Local? A Review of Practical and Conceptual Issues in the Genetics of Restoration.” Restoration Ecology 13 (3): 432–440. https://doi.org/10.1111/j.1526-100X.2005.00058.x
Meloni, Maurizio, Rachael Wakefield-Rann, and Becky Mansfield. 2022. “Bodies of the Anthropocene: On the Interactive Plasticity of Earth Systems and Biological Organisms.” The Anthropocene Review 9 (3): 473–493. https://doi.org/10.1177/20530196211001517
Merkle, Scott A., G. Andrade, C. Nairn, William Powell, and Charles Maynard. 2007. “Restoration of Threatened Species: A Noble Cause for Transgenic Trees.” Tree Genetics & Genomes 3: 111–118. https://doi.org/10.1007/s11295-006-0050-4.
Merola, Michele. 1994. “A Reassessment of Homozygosity and the Case for Inbreeding Depression in the Cheetah, Acinonyx jubatus: Implications for Conservation.” Conservation Biology 8 (4): 961–971. https://doi.org/10.1046/j.1523-1739.1994.08040961.x
Metcalf, Jessica L., Victoria Pritchard, Sarah Silvestri, Jazzmin Jenkins, John Wood, David Cowley, R. Paul Evans, Dennis Shiozawa, and Andrew Martin. 2007. “Across the Great Divide: Genetic Forensics Reveals Misidentification of Endangered Cutthroat Trout Populations.” Molecular Ecology 16 (21): 4445–4454. https://doi.org/10.1111/j.1365-294X.2007.03472.x
Metcalf, Jessica L., S. Love Stowell, C. Kennedy, K. Rogers, D. McDonald, J. Epp, K. Keepers, A. Cooper, J. Austin, and A. P. Martin. 2012. “Historical Stocking Data and 19th Century DNA Reveal Human-Induced Changes to Native Diversity and Distribution of Cutthroat Trout.” Molecular Ecology 21 (21): 5194–5207. https://doi.org/10.1111/mec.12028
Mijangos, Jose Luis, Carlo Pacioni, Peter Spencer, and Michael Craig. 2015. “Contribution of Genetics to Ecological Restoration.” Molecular Ecology 24 (1): 22–37. https://doi.org/10.1111/mec.12995
Muhlfeld, Clint C., Steven T. Kalinowski, Thomas E. McMahon, Mark L. Taper, Sally Painter, Robb F. Leary, and Fred W. Allendorf. 2009. “Hybridization Rapidly Reduces Fitness of a Native Trout in the Wild.” Biology Letters 5 (3): 328–331. https://doi.org/10.1098/rsbl.2009.0033
Muhlfeld, Clint C., Ryan P. Kovach, Robert Al-Chokhachy, Stephen J. Amish, Jeffrey L. Kershner, Robb F. Leary, Winsor H. Lowe, Gordon Luikart, Phil Matson, David A. Schmetterling, Bradley B. Shepard, Peter Westley, Diane Whited, Andrew Whiteley, and Fred W. Allendorf. 2017. “Legacy Introductions and Climatic Variation Explain Spatiotemporal Patterns of Invasive Hybridization in a Native Trout.” Global Change Biology 23 (11): 4663–4674. https://doi.org/10.1111/gcb.13681
NatureMetrics. 2021. “Global Atlas of Freshwater Life Will Use DNA to Tackle the Extinction Crisis.” https://www.naturemetrics.com/wp-content/uploads/2021/06/eBioAtlas-Release-Final.pdf (accessed 10 May 2023).
Newhouse, Andrew E., and William A. Powell. 2021. “Intentional Introgression of a Blight Tolerance Transgene to Rescue the Remnant Population of American Chestnut.” Conservation Science and Practice 3 (4): e348. https://doi.org/10.1111/csp2.348.
O'Brien, Stephen J. 1998. “Intersection of Population Genetics and Species Conservation.” In Evolutionary Biology, ed. Max K. Hecht, Ross J. MacIntyre, and Michael T. Clegg Evolutionary Biology. Boston: Springer. https://doi.org/10.1007/978-1-4899-1751-5_3.
O'Brien, Stephen J., David E. Wildt, David Goldman, Carl Merril, and Mitchell Bush. 1983. “The Cheetah is Depauperate in Genetic Variation.” Science 221 (4609): 459–462. https://doi.org/10.1126/science.221.4609.459.
O'Brien, William. 2006. “Exotic Invasions, Nativism, and Ecological Restoration: On the Persistence of a Contentious Debate.” Ethics, Place and Environment 9 (1): 63–77. https://doi.org/10.1080/13668790500512530
O'Donnell, Ryan P., Jennifer Fox, and Michael Ingraldi. 2023. “Environmental DNA in the Management of Invasive and Native Amphibians: American Bullfrogs and Barred Tiger Salamanders on the Grand Canyon-Parashant National Monument.” Sonoran Herpetologist 36 (2): 28–30.
Pazzaglia, Jessica, Hung Manh Nguyen, Alex Santillán-Sarmiento, Miriam Ruocco, Emanuela Dattolo, Lázaro Marín-Guirao, and Gabriele Procaccini. 2021. “The Genetic Component of Seagrass Restoration: What We Know and the Way Forwards.” Water 13 (6): 829. https://doi.org/10.3390/w13060829.
Peña-Guzmán, David M., G. K. Peña-Guzmán, and Albrecht Schulte-Hostedde. 2015. “Genetic Integrity, Conservation Biology and the Ethics of Non-Intervention.” Ethics, Policy & Environment 18 (3): 259–261. https://doi.org/10.1080/21550085.2015.1111622
Perkins, Harold A. 2020. “Killing One Trout to Save Another: A Hegemonic Political Ecology with its Biopolitical Basis in Yellowstone's Native Fish Conservation Plan.” Annals of the American Association of Geographers 110 (5): 1559–1576. https://doi.org/10.1080/24694452.2020.1723395
Piaggio, Antoinette J., Gernot Segelbacher, Philip J. Seddon, Luke Alphey, Elizabeth L. Bennett, Robert H. Carlson, Robert Friedman, Dona Kanavy, Ryan Phelan, Kent Redford, Marina Rosales, Lydia Slobodian, and Keith Wheeler, 2017. “Is it Time for Synthetic Biodiversity Conservation?” Trends in Ecology & Evolution 32 (2): 97–107. https://doi.org/10.1016/j.tree.2016.10.016
Popkin, Gabriel. 2018. “To Save Iconic American Chestnut, Researchers Plan Introduction of Genetically Engineered Tree into the Wild,” Science (29 August). https://www.science.org/content/article/save-iconic-american-chestnut-researchers-plan-introduction-genetically-engineered-tree (accessed 30 June 2023).
Preston, Christopher J. 2019. The Synthetic Age: Outdesigning Evolution, Resurrecting Species, and Reengineering Our World. Cambridge, MA: MIT Press.
Pröhl, Heike, Jana Auffarth, Tjard Bergmann, Holger Buschmann, and Niko Balkenhol. 2021. “Conservation Genetics of the Yellow-Bellied Toad (Bombina variegata): Population Structure, Genetic Diversity and Landscape Effects in an Endangered Amphibian.” Conservation Genetics 22: 513–529. https://doi.org/10.1007/s10592-021-01350-5.
Puchany, Andriana R. 2021. “Success of Westslope Cutthroat Trout and Arctic Grayling Conservation Translocations in Yellowstone National Park, Montana and Wyoming, USA.” PhD diss., Montana State University.
Redford, Kent H., and William M. Adams. 2021. Strange Natures: Conservation in the Era of Synthetic Biology. New Haven, CT: Yale University Press.
Redford, Kent H., William Adams, Rob Carlson, Georgina M. Mace, and Bertina Ceccarelli. 2014. “Synthetic Biology and the Conservation of Biodiversity.” Oryx 48 (3): 330–336. https://doi.org/10.1017/S0030605314000040
Rey, Olivier, Christophe Eizaguirre, Bernard Angers, Miguel Baltazar-Soares, Kostas Sagonas, Jérôme G. Prunier, and Simon Blanchet. 2020. “Linking Epigenetics and Biological Conservation: Towards a Conservation Epigenetics Perspective.” Functional Ecology 34 (2): 414–427. https://doi.org/10.1111/1365-2435.13429
Robbins, Paul, Hilary Habeck Hunt, Francisco Pelegri, and Jonathan Gilbert. 2023. “Sovereign Genes: Wildlife Conservation, Genetic Preservation, and Indigenous Data Sovereignty.” Frontiers in Conservation Science 4: 1099562. https://doi.org/10.3389/fcosc.2023.1099562.
Robinson, Jacqueline A., Jannikke Räikkönen, Leah M. Vucetich, John A. Vucetich, Rolf O. Peterson, Kirk E. Lohmueller, and Robert K. Wayne. 2019. “Genomic Signatures of Extensive Inbreeding in Isle Royale Wolves, a Population on the Threshold of Extinction.” Science Advances 5 (5). https://doi.org/10.1126/sciadv.aau0757.
Rohrer, Robert L., and Gary H. Thorgaard. 1986. “Evaluation of Two Hybrid Trout Strains in Henry's Lake, Idaho, and Comments on the Potential Use of Sterile Triploid Hybrids.” North American Journal of Fisheries Management 6 (3): 367–371. https://doi.org/10.1577/1548-8659(1986)6 percent3C367:EOTHTS percent3E2.0.CO;2.
Rohwer, Yasha, and Emma Marris. 2015. “Is There a Prima Facie Duty to Preserve Genetic Integrity in Conservation Biology?” Ethics, Policy & Environment 18 (3): 233–247. https://doi.org/10.1080/21550085.2015.1111629
Rossi, Jairus. 2014. “Genes are Not Information: Rendering Plant Genetic Resources Untradeable Through Genetic Restoration Practices.” Geoforum 55: 66–75. http://dx.doi.org/10.1016/j.geoforum.2014.05.001.
Rutherford, Susan, Marlien van der Merwe, Peter G. Wilson, Robert M. Kooyman, and Maurizio Rossetto. 2019. “Managing the Risk of Genetic Swamping of a Rare and Restricted Tree.” Conservation Genetics 20: 1113–1131. https://doi.org/10.1007/s10592-019-01201-4.
Sample, Ian. 2019. “World's First Living Organism with Fully Redesigned DNA Created.” The Guardian (15 May), https://www.theguardian.com/science/2019/may/15/cambridge-scientists-create-worlds-first-living-organism-with-fully-redesigned-dna.
Sandbrook, Chris, William M. Adams, Bram Büscher, and Bhaskar Vira. 2013. “Social Research and Bio-diversity Conservation.” Conservation Biology 27 (6): 1487–1490. https://doi.org/10.1111/cobi.12141
Segelbacher, Gernot, Mirte Bosse, Pamela Burger, Peter Galbusera, José A. Godoy, Philippe Helsen, Christina Hvilsom, Laura Iacolina, Adla Kahric, Chiara Manfrin, Marina Nonic, Delphine Thizy, Ivaylo Tsvetkov, Nevena Veličković, Carles Vilà, Samantha M. Wisely, and Elena Buzan. 2022. “New Developments in the Field of Genomic Technologies and their Relevance to Conservation Management.” Conservation Genetics 23 (2): 217–242. https://doi.org/10.1007/s10592-021-01415-5
Shepard, Bradley B., Bruce E. May, and Wendi Urie. 2005. “Status and Conservation of Westslope Cutthroat Trout Within the United States.” North American Journal of Fisheries Management 25 (4): 1426–1440. https://doi.org/10.1577/M05-004.1
Sinner, Jim, Marc Tadaki, Edward Challies, Margaret Kilvington, Paratene Tane, and Christina A. Robb. 2022. “Crafting Collective Management Institutions in Messy Real-World Settings: A Call for Action Research.” International Journal of the Commons 16 (1). https://doi.org/10.5334/ijc.1145.
Spence, Mark David. 1996. “Crown of the Continent, Backbone of the World: The American Wilderness Ideal and Blackfeet Exclusion from Glacier National Park.” Environmental History 1 (36): 29–49. https://doi.org/10.2307/3985155
Spence, Mark David. 1999. Dispossessing the Wilderness: Indian Removal and the Making of the National Parks. Oxford: Oxford University Press.
Stroupe, Sam, David Forgacs, Andrew Harris, James N. Derr, and Brian W. Davis. 2022. “Genomic Evaluation of Hybridization in Historic and Modern North American Bison (Bison bison).” Scientific Reports 12 (1): 6397. https://doi.org/10.1038/s41598-022-09828-z.
TallBear, Kim. 2013. “Genomic Articulations of Indigeneity.” Social Studies of Science 43 (4): 509–533. https://doi.org/10.1177/0306312713483893
Theissinger, Kathrin, Carlos Fernandes, Giulio Formenti, Iliana Bista, Paul R. Berg, Christoph Bleidorn, Aureliano Bombarely, Angelica Crottino, Guido R. Gallo, José A. Godoy, Sissel Jentoft, Joanna Malukiewicz, Alice Mouton, Rebekah A. Oomen, Sadye Paez, Per J. Palsbøll, Christophe Pampoulie, María J. Ruiz-López, Simona Secomandi, Hannes Svardal, Constantina Theofanopoulou, Jan de Vries, Ann-Marie Waldvogel, Guojie Zhang, Erich D. Jarvis, Miklós Bálint, Claudio Ciofi, Robert M. Waterhouse, Camila J. Mazzoni, and Jacob Höglund. 2023. “How Genomics Can Help Biodiversity Conservation.” Trends in Genetics 39 (7): 545–559. https://doi.org/10.1016/j.tig.2023.01.00
Todd, Zoe. 2014. “Fish Pluralities: Human-animal Relations and Sites of Engagement in Paulatuuq, Arctic Canada.” Études/Inuit/Studies 38 (1–2): 217–238. http://doi.org/10.7202/1028861ar.
Trigger, David, Jane Mulcock, Andrea Gaynor, and Yann Toussaint. 2008. “Ecological Restoration, Cultural Preferences and the Negotiation of ‘Nativeness’ in Australia.” Geoforum 39 (3): 1273–1283. https://doi.org/10.1016/j.geoforum.2007.05.010
United Nations (General Assembly). 2019. “United Nations Decade on Ecosystem Restoration (2021–2030): Resolution / Adopted by the General Assembly.” UN. General Assembly (73rd sess.: 2018–2019). March 6.
Vallejo-Marín, Mario, and Simon J. Hiscock. 2016. “Hybridization and Hybrid Speciation Under Global Change.” New Phytologist 211 (4): 1170–1187. https://doi.org/10.1111/nph.14004
Valve, Helena. 2011. “GM Trees on Trial in a Field: Reductionism, Risks and Intractable Biological Objects.” Geoforum 42 (2): 222–230. https://doi.org/10.1016/j.geoforum.2010.11.001
Wilcox, Taylor, Kellie Carim, Kevin McKelvey, Michael K. Young, and Michael K. Schwartz. 2015. “The Dual Challenges of Generality and Specificity When Developing Environmental DNA Markers for Species and Subspecies of Oncorhynchus.” PLoS One 10 (11): e0142008. https://doi.org/10.1371/journal.pone.0142008.
Williams, Anna V., Paul G. Nevill, and Siegfried Krauss. 2014. “Next Generation Restoration Genetics: Applications and Opportunities.” Trends in Plant Science 19 (8): 529–537. https://doi.org/10.1016/j.tplants.2014.03.011
Wilson, Randall K. 2020. America's Public Lands: From Yellowstone to Smokey Bear and Beyond. London: Rowman & Littlefield Publishers.
Wölfle Hazard, Cleo. 2022. Underflows: Queer Trans Ecologies and River Justice. Seattle: University of Washington Press.
Young, Michael K., Daniel J. Isaak, Kevin McKelvey, Taylor Wilcox, Matthew Campbell, Matthew Corsi, Dona Horan, and Michael K. Schwartz. 2017. “Ecological Segregation Moderates a Climactic Conclusion to Trout Hybridization.” Global Change Biology 23 (12): 5021–5023. https://doi.org/10.1111/gcb.13828