Abstract

Humans have served their needs and interests by modifying plants, animals, and ecosystems for millennia. Technology has expanded, accelerated, and intensified the impact. Experimental efforts are now under way to rescue or re-create nature employing highly sophisticated technologies. These endeavors are not aimed at satisfying basic human needs or serving economic interests; their goal is the conservation of biodiversity and ecological restoration. At the same time, they fundamentally alter the fabric of life and guarantee unintended consequences. An examination of the ecological and cultural risks, benefits, and costs of employing synthetic biology to assist evolution and de-extinct species provides a valuable test case for environmentalists and conservationists grappling with the implications of ecological restoration technologies.

Human beings modify nature to serve their needs. In this respect, they are no different from ants making hills, beavers constructing dams, and elephants digging water holes. What distinguishes our species from all others are the scale, speed, and impact of our modifications. That is the product of technology.

Of course, many animals use tools. Chimpanzees throw stones at antagonists and extract termites from mounds with sticks. Otters employ stones to pry abalone from rocks, and woodpecker finches wield cactus spines to impale their prey. The list goes on. While many other species use tools, none craft complex implements and machines. Human technology is unparalleled in its sophistication, power, and ecological repercussions.

Over the millennia, humans have utilized implements and machines to deplete the planet’s species and severely degrade its biomes. Currently efforts to rescue and resuscitate the natural world employing highly sophisticated technologies are under way. Artificial intelligence, often coupled with drones, is used to monitor wildlife, identify poachers, exterminate invasive species, and power “precision agriculture” that grows more food without usurping natural habitats. Geoengineering technologies are proposed as crucial means to conserve ecosystems threatened by global warming, and synthetic biology is being deployed to assist evolution and de-extinct species.

These technologies aim to benefit nature. While they are anthropogenic (caused by humans), they are not anthropocentric (holding human needs and interests supreme). Advocates argue that ecological restoration technologies will provide a second life for the natural world in an age of environmental devastation. Critics believe they will precipitate the end of nature—extending, amplifying, and intensifying our species’ conquest of the biosphere. The controversy is fueled by the paradox of engineering nature to save it.

This essay grapples with the implications of ecological restoration technologies. Specifically, it focuses on the use of synthetic biology for assisted evolution and de-extinction. To date, nature conservation has mostly been backward looking, with the aim of reducing ecological loss or maintaining the status quo. Notwithstanding heroic efforts and many notable achievements, this approach has not conserved aggregate planetary biodiversity. And future prospects are dim given the impacts of climate change. Synthetic biology might reverse the trend. However, once the taboo of releasing genetically engineered species into the wild is thoroughly broken, albeit for the best of conservation reasons, there may be no stopping, or even slowing down, the undiscriminating proliferation of synthetic life-forms.

I focus on assisted evolution and de-extinction for several reasons. Unlike geoengineering, these ecological restoration technologies have left the drawing board to enter the biosphere. They are currently being deployed. Unlike artificial intelligence, they have received widespread attention from conservationists and have produced heated debate. In turn, assisted evolution and de-extinction are the ecological restoration technologies most consistently depicted and justified as non-anthropocentric in orientation.

Assisted evolution and de-extinction present a daunting challenge for environmentalists. They may become dominant forces for conservation in an age of global ecological crises, providing a crucial means of protecting and sustaining the natural world. Yet they stretch, if not tear apart, the very meaning of nature. In turn, they may serve as the Trojan horse that opens the gates to bioengineering for pleasure and profit.

As such, assisted evolution and de-extinction constitute powerful test cases for evaluating ecological restoration technologies. Will these wildly ambitious yet increasingly feasible technological endeavors signal a new beginning for nature or the last nail in its coffin? And should the answer to this question determine their fate? We are faced with critical choices—and time is short.

A Brief History of Nature

The word nature means different things to different people, and probably always has. The range of definitions is large and discordant. For some, nature signifies a realm of conflict, competition, and survival of the fittest. For others, it bespeaks symbiotic cooperation and organic harmony. Nature is understood to embody reason and order. It is also depicted as an irrational, brute force. The natural world is embraced as a source of nourishment, healing, and beauty. It is also experienced as an unforgiving, unmerciful, and, ultimately, fatal reality.

For the purposes of this inquiry, nature refers to the Earth’s biological and ecological entities, relationships, and processes, and specifically those that preceded our species or have coexisted with it largely unimpacted. I am not claiming to define what nature most essentially is, simply how the word is most commonly understood. As a gesture toward this nonessentialism, I utilize the term Nature 1.0.

Nature 1.0 is what C. S. Lewis called the “uninterfered with.” For we humans, Lewis observes, “nature is all that is not man-made; the natural state of anything is its state when not modified by man.” This definition is defensibly species-centric. As Lewis (1960, 45–46) notes, “if ants had a language they would, no doubt, call their anthill an artifact and describe the brick wall in its neighborhood as a natural object. Nature in fact would be for them all that was not ‘ant-made.’” To call nature the uninterfered with does belie the fact that nature is a network of interdependent relationships, a web of life. In the “real world,” as Lewis acknowledges, “everything is continuously ‘interfered with’ by everything else; total mutual interference … is of the essence of nature.”

Notwithstanding these caveats, nature is not an “idle term,” because people “know pretty well what they mean by it and sometimes use it to communicate what would not easily be communicable in other ways” (Lewis 1960, 74). That is my justification for employing the term Nature 1.0. It is not nature, full stop (whatever that might mean). Nature 1.0 does not include cornfields, house pets, the atomic physics that occurs in neutron stars, and countless other (natural) phenomena. Nature 1.0 simply refers to biological and ecological entities, relationships, and processes here on Earth that have not been interfered with by human beings. It is nature commonly understood.

For millennia, humans have modified Nature 1.0 to serve their needs and interests in agriculture and horticulture, hunting and security, health and medicine, aesthetics and entertainment. I call this human-impacted biological and ecological realm Nature 2.0. Nature 2.0 began with primitive hunting and gathering, broadening in scale and deepening in scope with the domestication and selective breeding of plants and animals, the use of fire to create grasslands for improved predation, swidden (slash and burn) agriculture, and large-scale water diversion for irrigation. Nature 2.0 is the natural world as anthropogenically and anthropocentrically altered. Technology is always involved.

The span between Nature 1.0 and Nature 2.0 is graduated. The hands that transform the former into the latter may have a light or heavy touch, and effects range from the negligible to the transformative. The impact of hunting and gathering, for instance, would have been difficult to discern in many if not most of the planet’s biomes in the Pleistocene. Still, Stone Age hominins caused the continental extinction of many species of megafauna. Unquestionably the human handprint has grown more forceful and expansive over the last dozen millennia. That increasing impact is the product of technological development and the growth in human populations that advancing technology facilitated.

Although some argue otherwise (Coates 1998, 177), anthropogenic modifications did not put an end to Nature 1.0. A field of maize in the ancient Aztec empire at the bottom of a steep, forested, and seldom-if-ever climbed mountain represented, respectively, Nature 2.0 butting up against Nature 1.0. Today, however, the greatest share of planetary life has taken the form of Nature 2.0 or is being crowded out by it. Nature 1.0 is in full retreat.

The last seven decades, known as the “great acceleration” (Steffen et al. 2007), saliently demonstrate the crowding out of Nature 1.0 by Nature 2.0. It reached a watershed sometime last century, prompting geologists to announce the Anthropocene. Unlike all earlier epochs, the Anthropocene is not characterized by climatic or tectonic events that stamped the planet with geologic markers; rather, it signifies the massive and enduring technological impact of a single species, anthropos (the Greek word for humanity). Evidence for the Anthropocene abounds.

Humankind now moves more rock and earth across the planet’s surface than all of its rivers and glaciers combined. It converts more nitrogen from the atmosphere into reactive forms, such as fertilizer, than all other terrestrial processes. Humans already farm almost half the planet’s viable terrain—a fivefold increase over the last three centuries—and are bringing ever more into production, while causing tens of thousands of square miles of arable land each year to become degraded beyond use. Currently the biomass of domesticated birds and mammals far exceeds that of all wild birds and mammals. In turn, humans are the single major cause of extinction of the Earth’s myriad forms of life. This decline in biodiversity is the product of rapidly advancing agriculture, the cutting and burning of forests, other forms of habitat loss, the overexploitation of wildlife, the introduction of invasive exotic species, pollution, and the generation of vast amounts of greenhouse gases, which are altering weather and climate, melting glaciers and polar ice, and acidifying ever-rising oceans.

Over the last thirty years, the human impact on plants, animals, and ecosystems has become not only more extensive than ever before but also more intensive. New technologies have penetrated the most fundamental life forces. Employing nanotechnology to manipulate the smallest building blocks of nature, humans have constructed atomic and molecular structures hitherto unknown to the planet. In turn, new species have been fashioned from scratch with synthetic biology. Thousands more have been genetically modified.

Nature 3.0 is the term I employ for this intensification and expansion of the adaptation of the biosphere to serve human needs and interests. It is chiefly characterized by the capacity for the accelerated, nonincremental, and precisely controlled modification or creation of life-forms and their environments. The primary Nature 3.0 technologies are nanotechnology, geoengineering, and biotechnology. The environmental repercussions of nanotechnology are limited to date but could scale quickly. The impact of geoengineering, if it is ever deployed, will be planetary. Biotechnology is well advanced and generates an ever-growing ecological footprint.

The terms biotechnology and synthetic biology are often used interchangeably, though the latter is generally understood to refer to an advanced stage of the former that allows for the (re)design and construction of artificial biological parts, processes, organisms, devices, or systems. Synthetic biology effectively reduces genetics into DNA “parts” that can be identified, edited, assembled, and synthesized. Genome-editing technologies, such as CRISPR/Cas9, generate breaks in DNA to allow modification at targeted loci. Genes that control for unwanted characteristics can be eliminated, and new genes or suites of genes, potentially drawn from different kinds of organisms, can be inserted to create new metabolic pathways and the behaviors to which they give rise.

Examples of environmentally impactful synthetic biology include the creation of gene drives designed to wipe out vector-borne diseases (such as malaria); carbon capture and storage mechanisms employing synthesized microbes; engineered algae to replace fossil fuels, polymers, and plastics; bioremediation that deploys synthesized bacteria to clean up contaminated industrial sites; GM crops with increased capacity for photosynthesis, tolerance of herbicides and pesticides, and resistance to drought or disease; GM animals with quicker maturation rates, higher food value, or other desired characteristics; and milk, egg, meat, leather, and seafood products cultured from engineered animal, yeast, and algae cells.

There are also growing numbers of retail Nature 3.0 products that may have environmental impacts, including designer pets and bioluminescent microbes and plants for home decor or landscaping. Heralding the arrival of “domesticated biotechnology” in the hands of laypeople and even children, Dyson (2007) predicts “an explosion of diversity of new living creatures. … Designing genomes will be a personal thing, a new art form as creative as painting or sculpture.” In keeping with Dyson’s prediction, biohacking sites now hawk their wares, coaxing visitors to join the SynBio fight against cancer or, more prosaically, to impress friends with their glowing ecoli farms.1 Inexpensive kits employing CRISPR technology are widely available. A few hundred dollars allows DIYers to produce fluorescent yeast or to genetically modify frogs.

For conservationists, an explosion of new life-forms produced by do-it-yourself (DIY) dabblers and teenagers in their parents’ garages is a horrifying thought. To be sure, the prospect of innumerable (fun-loving or misanthropic) biohackers is at least as disturbing as weakly regulated biotech corporations stimulating consumer demand for designer organisms. Nature 3.0 appears to be opening up a Pandora’s box, and conservationists are rightly worried. This brings us to Nature 4.0.

Nature 4.0

Nature 4.0 is newly born—but purpose rather than chronology is its distinguishing feature. Like Nature 3.0, it is generated by technologies that accelerate and precisely control the modification and creation of life-forms. But Nature 4.0 serves a particular objective: the restoring or reviving of natural organisms and ecosystems. The most prominent examples are the use of biotechnology to facilitate the assisted evolution of species in the face of the stresses associated with climate change and de-extinction efforts to resuscitate species employing remnant DNA. Nature 4.0 is anthropogenic. But unlike Nature 2.0 and Nature 3.0, it is not anthropocentric in the strict sense; rather, the purpose of Nature 4.0 is to rescue and resuscitate the natural world.

The same technology may be employed for Nature 3.0 and Nature 4.0 purposes. Solar radiation management, a form of geoengineering, might be deployed to protect agricultural yields in the face of global warming. Alternatively, its objective might be the preservation of heat-stressed species that cannot migrate to higher altitudes or latitudes. Likewise, synthetic biology may be employed to engineer novel cosmetics and designer pets. Alternatively, it may be used to assist the evolution of threatened species.

The purpose that these technologies serve is important because it typically justifies their development and deployment. As such, Nature 4.0 presents a conceptual and normative watershed for environmentalists and conservationists—people who cherish the experience of Nature 1.0, seek to preserve it, and, to the extent they remain anthropocentric, align the long-term, collective interests of humanity with the ecological health of a biodiverse planet. For such individuals and their organizations, Nature 4.0 is a double-edged sword.

The conservation impacts of Nature 4.0 are promising. The development of gene drives might improve the heat tolerance of species threatened by climate change and win the fight against invasive species that threaten native flora and fauna (Ortiz 2008). Engineered substitutes for products of overharvested and endangered wild species are in development. In turn, biotech crops that use less water, need fewer nutrients, are more disease resistant, and produce better yields would allow the “sustainable intensification” of agriculture, obviating the need to bring more land under cultivation to feed growing human populations. Such “land sparing” would allow the conservation of existing wilderness and wildlife (Redford et al. 2013b, 2). But the environmental risks associated with synthetic biology are as manifold as its promised benefits. We face the development and release of a proliferating array of—mostly unregulated and, given its DIY variations, possibly unregulatable—engineered organisms. Unintended consequences are guaranteed.

The stakes are too high for knee-jerk reactions, either pro or contra. Rightfully, conservationists are urging their colleagues to engage in “a clear-eyed examination of the norms, oversight, and public education necessary to make decisions about the enormous power of altering life on Earth” (Redford et al. 2013b, 4). Due diligence is required. As a preliminary exercise in meeting this obligation, I examine the risks, benefits, costs, and conundrums that Nature 4.0 presents in the arenas of assisted evolution and de-extinction.

Assisted Evolution

Assisted evolution entails genetically tweaking endangered species so they are better able to adapt to changing environmental conditions and reclaim their native habitats (van Oppen et al. 2015). For wild plants and animals severely impacted by anthropogenic disturbances—including novel disease vectors, overharvesting, habitat loss, invasive exotics, and thermal stress—the original stock of the native species may be ill suited for restoration. The genetic alteration of these populations might greatly enhance their resilience.

Before the Asian fungus introduced by humans took its toll, for example, the North American landscape was populated with four billion chestnut trees. By the early 1900s, few remained. In 2006, the first American chestnuts genetically engineered to be resistant to the fungus were planted. There are more than 1,000 such transgenic chestnut trees growing in New York State today. Similar efforts for other species are under way.

One of the most prominent projects of assisted evolution is coral restoration. Coral reefs have suffered massive declines in health and abundance over the last decades as a result of pollution, destructive fishing and recreational practices, thermal stresses associated with climate change, and the acidification of oceans. Some areas, such as Australia’s Great Barrier Reef, have lost almost half of their coverage, with greater degradation predicted for the coming decade. Globally, these losses jeopardize a million species of sea life for which coral reefs serve as a crucial habitat (Anthony et al. 2017, 1421).

The Coral Restoration Foundation maintains the world’s largest “genetic ark” and database of coral genotypes. It breeds promising species in nurseries and outplants them to existing reefs. Such artificial selection allows the development of coral stocks with enhanced resilience to climate change and other anthropogenic disruptions. These efforts do not employ biotechnology; rather, standard forms of breeding and hybridization in laboratories or in situ are used (Jones 2015; Linden and Rinkevich 2011; van Oppen et al. 2015). The slow and steady progress of selective breeding programs, however, is vastly outpaced by the scope and speed of global coral degradation. Consequently, it is no surprise that biotechnology is playing an ever-larger role in coral restoration efforts (Jones and Monaco 2009, 541–543).

Though still at a preliminary stage, genome editing employing CRISPR has been successful in targeting and enhancing specific coral genes (Cleves et al. 2018). This technique, accompanied with gene drives, could facilitate the rapid spread of climate-adapted coral genotypes and the preservation of crucial ecosystem functions. As long as such technologies are “developed and deployed under a stringent and adaptive framework that includes extensive societal consultation,” many conservationists believe the ecological benefits outweigh associated risks given the severity of the crisis (Anthony et al. 2017, 1421).

Initiatives focused on other species and ecosystems are under way. Revive and Restore, a prominent nonprofit founded by Stewart Brand, is pursuing the assisted evolution of the black-footed ferret. Synthetic biology is deployed to endow the animal, whose survival is most hindered by sylvanic plague and inbreeding, with resistance to the disease and greater genetic diversity. The mission of Revive and Restore is the “genetic rescue” of threatened species. Here assisted evolution goes by the name de-endangerment. As the number of threatened species across the planet is large and growing, the scope of de-endangerment is quickly expanding.

De-extinction

Also known as resurrection biology, species revivalism, and reanimation, de-extinction is the project of producing organisms, and eventually breeding populations of organisms, that closely resemble extinct species. Various techniques for de-extinction are being pursued, and not all involve genetic engineering.

Back-breeding, for example, is a form of artificial selection that attempts to resurrect ancestral characteristics persisting within an extant population. Rather than creating or enhancing new traits, which is the goal of most efforts in artificial selection, back-breeding aims to revive or concentrate phenotypic characteristics that have been lost or diluted over time. Genetic sequencing of the extinct species allows its genome to be compared to that of the back-bred organism, facilitating its selective breeding to ever more closely approximate its predecessor. The best example of back-breeding is the European effort to reintroduce the auroch, the extinct forebear of contemporary cattle.

De-extinction efforts that involve genetic engineering necessitate cloning, also known as somatic cell nuclear transfer (SCNT). Cloning is an effort to produce genetically identical copies of a species from preserved somatic cells. Dolly the sheep, in 1996, was the first successfully cloned mammal. Since then, at least twenty mammalian species have been cloned. In de-extinction efforts, the nucleus of a preserved somatic cell of an extinct species is injected into an enucleated egg cell of its nearest extant relative. As this renucleated egg starts to divide, the embryo is inserted into a host organism, where it is brought to term. The resulting offspring will have the genotype of the extinct species, though its fetal and postnatal environments will be of the contemporary host. As such, its phenotype, the observable characteristics of the organism, will closely resemble but not be identical to those of the extinct species.

From the perspective of conservation biology, a species is defined by its gene pool and flow, its ecological niche, and its evolutionary history. A de-extincted species would partially satisfy the first criterion, potentially the second, but not the third. As such, the goal of de-extinction from the perspective of conservation biology is not the status quo ante; rather, the aim is to create “proxy” organisms that fill the ecological niches of the extinct species (Shapiro 2017, 1001).

Cloning techniques have been successfully carried out with endangered animals, such as the banteng, a species of wild cattle from Southeast Asia. A cloned banteng calf was born at the San Diego Zoo in 2003 and lived until 2010. Efforts with extinct species have been less successful. An SCNT embryo of an extinct frog was produced, but it did not mature. The 2003 live birth of a bucardo, an extinct subspecies of Pyrenean ibex, was heralded as the first true de-extinction. Produced from frozen cells collected from the last living specimen, the kid lived fewer than eight minutes before expiring from a defective lung.

Advances in genome editing and assembly, such as CRISPR, might allow the revival of extinct species whose genetic material can be sequenced and reassembled from degraded tissues that contain fragmented DNA. Notwithstanding the popularity of the Jurassic Park film series, however, dinosaurs are not an option. Indeed, it is unlikely that species predating the Pleistocene would provide sufficiently intact DNA. Even then, to be viable, an organism would have had to become frozen immediately after death, and remained so. A prime candidate is a 42,000-year-old foal found in Siberian permafrost in 2018. A team of Russian and South Korean scientists have been able to extract blood cells and are working on cloning this extinct “Lenskaya” horse (Dvorsky 2019).

The most prominent example of de-extinction is the effort to revive the woolly mammoth (most likely employing Asian elephant hosts). Even the most intact mammoth tissue has such fragmented DNA, however, that the sequencing and synthesis required to faithfully reproduce the entire genome is some years away. A team of Japanese scientists from Kindai University recently coaxed cell nuclei from a 28,000-year-old mammoth found in Siberian permafrost to exhibit biological activity after being implanted into the egg cell of a mouse (AFP News 2019). Many significant technical hurdles remain.

While faithfully reproducing the mammoth genome will be difficult, the migration of selected genes from the mammoth into the genome of the Asian elephant, or alternatively the genetic editing of the Asian elephant genome to incorporate selected mammoth genes, is quite feasible. The goal would be an Asian elephant with cold-resistant blood; longer, thicker hair; and an extra layer of fat that would allow it live in the tundra and taiga (boreal forests) of higher latitudes, where it could contribute to the transformation of these ecosystems into the more biodiverse and carbon-absorbing grassy steppes that existed in the Pleistocene. The Harvard Woolly Mammoth Revival team, headed by George Church, is identifying the alleles of the mammoth genome that might allow this form of de-extinction.

Church’s work, like most other de-extinction initiatives, aims to resuscitate traits of a species’ ancestral phenotypes (i.e., physiological, morphological, behavioral, and ecological) to create proxy organisms with greater adaptive capacities and positive ecological impacts. It is justified as a form of ecological enrichment (Church and Regis 2012, 140). Church (2013) observes that “the goal of reanimation research is not to make perfect living copies of extinct organisms, nor is it meant to be a one-off stunt in a laboratory or zoo. Reanimation is about leveraging the best of ancient and synthetic DNA. The goal is to adapt existing ecosystems to radical modern environmental changes, such as global warming, and possibly reverse those changes.” This is in keeping with the recommended protocol for de-extinction developed by the International Union for Conservation of Nature. De-extinction projects are only to be undertaken when there is “expectation of a positive conservation benefit,” such as increasing ecosystem resilience or reducing further loss of biodiversity (IUCN 2016, 1, 10).

For such ecological benefits to accrue, a sufficiently large, genetically diverse population of the de-extincted species that could successfully reproduce and adapt to a new, still changing environment would be needed (Steeves et al. 2017, 1032). Otherwise, the newly reanimated species would face the ignominy of a second extinction. The more redundant the proxy’s ecological function with extant species, and the longer the time span between its extinction and resurrection, the lower is its survivability, the fewer are the ecological benefits, and the higher are the ecological risks (McCauley et al. 2017; Robert et al. 2017).

Church’s effort to revive the woolly mammoth is supported by Revive and Restore, which, in addition to de-endangering the black-footed ferret, hopes to resuscitate the passenger pigeon. Massive flocks of these birds played a significant role in maintaining the woodland biodiversity of the eastern United States until their sudden extinction in the early twentieth century. By introducing passenger pigeon genes into the genome of extant band-tailed pigeons, a version of the former would be created for the purposes of ecosystem restoration. Passenger pigeon de-extinction is proposed as an umbrella program that would garner broad support for the protection of affected ecosystems and related projects. The extinction of the passenger pigeon mere decades after its wild population numbered in the billions, Revive and Restore states, symbolized the bane of “unchecked human consumption” and helped initiate “a new age of conservation regulation and game management.” As such, this iconic bird provides a “model de-extinction project” that could galvanize the next environmental revolution.2

As Seddon (2017, 994) observes, seeking such benefits is not the same thing as achieving them. For the foreseeable future, this distinguishes the feasibility of genetic de-endangerment from the technological hurdles and ecological uncertainties belaboring de-extinction. Still, the same risk–cost–benefit analysis arguably ought to be applied to all conservation efforts involving synthetic biology, as well as to those employing traditional methods (Iacona et al. 2017, 1046). We now turn to this empirical and normative analysis and the conundrums it presents.

Governing Nature 4.0

If the next environmental revolution is in the making, it still lacks a clear manifesto. The assisted evolution and de-extinction trains have left their respective stations, but destinations remain unknown—and no one is manning the brakes. The same may soon be true of other ecological restoration technologies.

The Cartagena Protocol on Biosafety, adopted in 2000 by the United Nations’ Conference of the Parties to the Convention on Biological Diversity (CBD) and now in force in virtually all nations, addresses the impacts and risks to human health and biodiversity of the transfer, handling, and use of technologically modified organisms. A recent report by the Secretariat of the Convention of Biological Diversity (2015, 10, 38) expressed confidence that the Cartagena Protocol was up to the task of addressing synthetic biology, including its uses for de-extinction. At the same time, it noted the perceived need for heightened attention to risks given growing technological power and the “unknown unknowns” that synthetic biology presents.

The IUCN (2016) has set out broad, voluntary guidelines for de-extinction projects to ensure their safety and ecological value. The governance of assisted evolution remains largely uncharted territory. Like most other discussions and policy proposals surrounding synthetic biology (Redford et al. 2013b; Taylor et al. 2017), the IUCN and CBD reports endorse increased reflection, more deliberation with more stakeholders, and greater transparency but shy away from heavy regulation.

In contrast, Friends of the Earth et al. (2012)—in response to the Presidential Commission for the Study of Bioethical Issues (2010)—released Principles for the Oversight of Synthetic Biology. The report, which 115 civil society organizations have signed, argues that the Commission’s faith in corporate self-regulation is misplaced and that a moratorium on the release and commercial use of bioengineered organisms should be put in place until increased transparency, corporate accountability, and governmental regulation employing the precautionary aprinciple is instituted.

The call for a moratorium has not gained much traction. Whether existing institutions can be adapted to govern Nature 4.0 technologies or whether new agencies, laws, rules, and norms are required remains an open question. The Secretariat for the CBD is the most likely venue to assume the challenge. Whether and how it does so will largely depend on the continued input from governments, scientists, the business sector, and civil society organizations. The questions and conundrums posed below are meant to serve as a preparatory exercise for such stakeholders.

Foremost, any effort to develop and deploy Nature 4.0 technologies should confront the inevitability of unintended consequences. There are many to consider. Genetically engineered plants and animals may introduce novel disease vectors and pathogens into biomes, threatening existing species. Genetically improved organisms might outcompete their legacy versions in the wild, contributing to the extinction of their natural forebears and erstwhile conspecifics. A more likely outcome is the genetic contamination (hybridization) of conspecifics, which may amount to much the same thing—the decline of a Nature 1.0 species owing to the introduction of a Nature 4.0 version of it. De-extincted organisms may become invasive paleo-exotics, disrupting ecosystems and, in the long term, causing an overall decline in biodiversity. That seems unlikely for the woolly mammoth. But other resurrected species might not be so easy to monitor, contain, and, if they prove ecologically destructive, re-extinct. Other pernicious impacts of Nature 4.0 are to be expected and require forecasting. This is no easy task.

When future harms become manifest, it may be too late for a remedy. This brings us to the problem of lock-in, also known as the “technology control dilemma” (Collingridge 1980). Often the adverse impacts of a technology remain unknown when it is new and controllable. Once harms become apparent, societal dependence on the technology precludes cost-efficient corrections. Likewise, by the time Nature 4.0 harms become evident, it may be too costly or ecologically damaging to remove the engineered organisms. And any attempt to revert to the status quo ante by reintroducing Nature 1.0 species could prove as hapless as inserting decade-old software into the latest electronic device. For ecological systems colonized by synthetic life-forms, there may be no going back. As harms develop and accumulate, ever more SynBio patches would become necessary. We would become locked into a Nature 4.0 world.

Prohibiting all Nature 4.0 interventions would preclude lock-in. But the probability of a successful ban or moratorium is very low. And what would be the justification for endorsing traditional ecological restoration projects while forbidding those involving synthetic biology? Why is it acceptable to engage in captive breeding programs, the extirpation of invasive exotics, the translocation of regionally endangered species to more hospitable environments, and back-breeding, for example, but not to clone threatened species to increase their numbers and genetic diversity?

Katz (2012, 67, 74) argues that all ecological restoration projects, including those employing traditional methods, effectively replace a natural phenomenon with an artifact. Interacting with such a “forgery” cannot produce an “authentic” experience. Notwithstanding any benefits they might confer, Katz concludes, all ecological restoration projects manifest the “human domination of nature.” But there is little of nature left in the Anthropocene that has not been impacted by humans. So, if the contemporary natural world is simulacra in any case, why not opt for high-tech forgeries?

Some environmentalists want to limit technological impacts but are unsure where to draw the line. Wapner (2014, 46–49) aspires to a “middle way” in the face of climate change. The development of carbon-free, hydroelectric power systems is endorsed, for example, while seeding of the ocean with iron to enhance the growth of carbon-absorbing phytoplankton constitutes the illegitimate domination of nature. Unfortunately, the only criterion provided for this distinction is that the former manifests a “humility” absent in the latter. Advocates of dam removal and free-flowing rivers, of course, would beg to differ. The unanswered question is where, when, and how to draw the line between humility and hubris. To be sure, scores of technologies—everything from airplanes to X-rays—were thought hubristic before they became humble features of everyday life.

De-endangerment might appear an acceptably humble endeavor given its restricted scope and the harsh fact that traditional conservation measures are not stemming the tide of extinction. But if a line in the sand is not drawn between traditional conservation and genetic de-endangerment, can one be drawn between the latter and de-extinction, since both endeavors aim to preserve biodiversity and restore ecological health by way of bioengineering?

The Audubon Center for Research on Endangered Species (ACRES) near New Orleans has cloned endangered African wildcats, the first successful effort with a wild carnivore. There are more than 500 other species in its “frozen zoo.” Assume that the work at ACRES advances, along with that of the San Diego Zoo (with more than 800 cryogenically preserved species) and the other dozen frozen zoos around the world. The somatic cells of many endangered species will be preserved, and no small number will be cloned, allowing the introduction of healthy, genetically diverse individuals into sparse native populations. Many endangered species will benefit from such efforts, and perhaps regain a nonthreatened status.

Other efforts will prove too little, too late. Many plants and animals will go extinct. Employing DNA from frozen zoos, however, these species might be resurrected at a later date, when resources are available and environmental conditions are better—perhaps a decade or century down the road. If this seems a reasonable approach to biodiversity conservation, then why not promote the resurrection of already extinct species, such as the passenger pigeon and the woolly mammoth? There seems to be no obvious stopping point on the road from de-endangerment to de-extinction.

Other slippery slopes will have to be navigated, including those between conservation and enhancement. Synthetic biology will provide opportunities not only to de-endanger and de-extinct species but to improve them (Shapiro 2015, 206). “Today we are at the point in science and technology,” Church observes, “where we humans can reduplicate and then improve what nature has already accomplished” (Church and Regis 2012, 12). Once Nature 1.0—the way things just happen to be absent human interference—is no longer a deciding normative value, technological know-how becomes the only barrier separating the preservation of a species from its upgrading. The conservation of nature may end with its wholesale redesign and replacement.

As many species appear incapable of adapting to anthropogenic climate change, their de-endangerment already constitutes an enhancement over the level of fitness provided by Nature 1.0. Proactive forms of assisted evolution, it follows, would simply make a species fitter before it becomes severely threatened, avoiding a crisis situation. In turn, the line separating an enhanced species from a wholly new one is rather blurry. Nature 1.0 regularly invents fitter forms of life, though they are always genetically contiguous with extant species. By and large, this natural speciation counterbalances the rate of extinction. Future conservationists keen on maintaining biodiversity may not shy away from artificial speciation. The key difference is that while natural speciation is always incremental—natura non facit saltus (nature does not make jumps)—synthesized and transgenic species need not closely resemble any single extant organism. Engineered life can be radically novel. And it can be created without the time lags and indeterminacies associated with Nature 2.0, which largely remains circumscribed by Nature 1.0 (reproductive) processes. The capacity of synthetic biology for accelerated, precisely controlled, and nonincremental interventions blurs the lines between conservation, enhancement, and artificial speciation.

Undoubtedly there will be advocates for enhancement. Biomes containing synthesized organisms may outperform naturally evolved ones in the provision of ecosystem services, such as carbon sequestration, pollution mitigation, and pollination. Indeed, the provision of such benefits may improve substantially while the biodiversity of native species simultaneously declines—in the same manner that the productivity of a newly automated factory might spike notwithstanding the layoff of its skilled human workers. If synthetically enhanced biomes more efficiently provide crucial ecosystem services, the justification for traditional biodiversity conservation might be imperiled (Redford et al. 2013a, 21).

This brings us to the issue of moral hazard: the lack of incentive to guard against damage or danger because one is protected from its consequences. Nature 4.0 effectively provides an insurance policy that shields us from damages associated with the loss of biodiversity and ecosystem services. As such, it may impede traditional conservation efforts and perhaps even stimulate human activities that contribute to the decline of biodiversity. Minteer (2014, 261) observes that de-extinction “reflects a new kind of Promethean spirit that attempts to leverage our boundless cleverness and powerful tools for conservation.” The real challenge, however, is “to live more lightly on the land and to address the moral and cultural forces that drive unsustainable and ecologically destructive practices” (261). Nature 4.0 presents the moral hazard of significantly shifting the challenges we can and should squarely face.

As a practical matter, Nature 4.0 projects may siphon funds away from traditional conservation projects. It is questionable whether we are really faced with a zero-sum game (Church 2013). Still, conservation funding is not wholly elastic and remains in relatively short supply. De-extinction start-ups, for example, might draw philanthropic funding away from existing conservation programs. These redirected resources, in turn, may increasingly be targeted to the revival of charismatic species that serve entertainment rather than conservation purposes. Many people would happily pay a hefty sum to see a woolly mammoth at a zoo. But they would decline to contribute to the much more expensive restoration of thousands of these ecological proxies on northern tundra lands. De-extinction and de-endangerment projects may follow the money. It is reasonable to worry about moral hazard, as Nature 4.0 initiatives may absorb the intellectual and economic resources that otherwise would be directed to Nature 1.0 conservation.

The aforementioned concerns highlight ecological risks and costs. While Nature 4.0 projects are (ostensibly) non-anthropocentric, however, their impacts on human beings also require attention. As the global loss of coral reefs jeopardizes the livelihoods of hundreds of millions of people (Anthony et al. 2017, 1421), for example, their successful assisted evolution would benefit many communities. Of course, there will also be associated risks and costs. Minimally, we must ask the following questions about the social and political impacts of Nature 4.0: Which individuals or groups in society will primarily gain and which will suffer from the deployment of Nature 4.0? Will risks, burdens, and benefits be equitably shared? Who will be included in relevant decision-making, particularly given the complexity of the issues involved, which arguably disenfranchises much of the lay population and undercuts democratic participation? Will Nature 4.0 projects reinforce or alter existing power structures and patterns of resource distribution? Will private and corporate ownership of synthetic life constrain or undermine the public benefits of Nature 4.0, as de-endangered and de-extincted species may become corporate property—at least in countries (e.g., the United States, but not Canada) where biologically complex, engineered organisms are patentable?

Cultural issues also loom large (Sandler 2017). Nature 4.0 might have the most significant impact not on the biomes of the planet but on the culture and psyche of its most innovative inhabitant. After careful deliberation, the Presidential Commission for the Study of Bioethical Issues (2010, 139, 140) stated that it “was not persuaded by concerns that synthetic biology fails to respect the proper relationship between humans and nature.” What the proper relationship is, or should be, the Commission never addressed. For conservationists, an anthropogenic sixth extinction crisis clearly does not reflect a proper relationship between humans and nature. But what does it mean for humans to forgo restraining and mourning the degradation and destruction of nature so they might engage their most powerful technologies to renovate, resurrect, and improve it?

The prospects of Nature 4.0 should prompt us to ask fundamental questions about “who we are and how we want to live in this world” (Wray 2017, 251). The moral terrain is treacherous. If we have an ethical obligation to prevent the decline of biodiversity, some argue, we are also obliged to promote the growth of biodiversity—and this positive, moral duty entails de-extincting species whenever possible (Gyngell and Savulescu 2017; Jebari 2016). Contrariwise, Minteer (2014, 261) writes that “attempting to revive lost species is in many ways a refusal to accept our moral and technological limits in nature. … That is why there is great virtue in keeping extinct species extinct. Meditation on their loss reminds us of our fallibility and our finitude.” Attending to the ecological risks, benefits, and costs of synthetic biology is crucial. But we should also ask, anthropocentrically, what Nature 4.0 means for us and what it might do to us. Answers to such questions will not be easy, uniform, or unchanging.

Conclusions

The story of conservation oozes doom and gloom. De-endangerment and de-extinction technologies promise to put some zoom into the narrative. The hope is to create a “future that is really better than today, not just one that is less bad than what we anticipate” (Shapiro 2015, 207). To be sure, “revive and restore” sounds a lot more hopeful than “postpone the inevitable.”

Over the coming decades, sustaining biodiversity will entail a great deal of monitoring, managing, restoring, and, perhaps, de-endangering and resuscitating. Though paradoxical, it is probable that wilderness in the future will be largely anthropogenic. In light of the current extinction crisis, it would be irresponsible flatly to reject all prospects for prudent, informed, widely endorsed, well-regulated, and properly targeted efforts to restore and maintain ecological health by means of synthetic biology. It would be equally irresponsible to proceed without the banister of governance.

When Craig Venter created the world’s first synthetic cell, officially known as Mycoplasma mycoides JCVI-syn1.0, but endearingly named Synthia, he inserted into its genome four “watermark” sequences containing strings of bases that spelled out in DNA an email address that would receive messages from all those clever enough to crack its code. In turn, the names of each of the creators of the first cell with a completely synthetic genome were included, along with a quotation from James Joyce’s A Portrait of the Artist as a Young Man: “To live, to err, to fall, to triumph, to recreate life out of life.” Also spelled out in Synthia’s DNA was an apothegm from the physicist Richard Feynman, who said, “What I cannot create, I do not understand.”

Actually, Venter’s team misquoted Feynman, substituting the words build for create and can for do. A harmless mistake, surely, easily explained by the plethora of misquotes and misattributions that plague the internet. Yet one wonders whether the slip-up might not be a harbinger of future errors in the codes of fabricated life. These errors—easy to make, difficult to detect, and impossible to foresee the consequences of—may leave our species prostrate rather than triumphant in the wake of its planetary management. Given our unquenchable thirst for knowledge and ineradicable urge to create, we appear poised to take the risk.

“De-extinction will be pursued” because it is “too sexy to ignore,” writes Philip Seddon (2017, 994), chair of the IUCN task force evaluating it. Barbara Kiser (2017, 331) concurs, writing in her book review section of Nature that “de-extinction is so hot a topic it sizzles.” To describe Nature 4.0 endeavors as sexy and sizzling bespeaks their irresistibility. The assumption is that our species, despite age-old taboos, will not be able to resist the opportunity to become godlike creators of life. Veneration of Nature 1.0 did not prevent its 2.0 and 3.0 iterations for self-interested reasons. Environmentalists and conservationists respect the natural world more than most—but this deference to nature likely will not prevent efforts to protect it, and remake it, by means of synthetic biology.

This century presents us with the responsibility to rethink conservation in the face of accelerating technological development and ecological degradation. This rethinking should grapple with the prospect that the most sophisticated efforts to save nature may prove ruinous, both ecologically and culturally. “We have deprived nature of its independence,” McKibben (1999, 58) argues, “and that is fatal to its meaning. Nature’s independence is its meaning.” Clearly biotechnologically assisted evolution and de-extinction, notwithstanding potential ecological benefits, constitute a harsh blow to nature’s independence, and hence to its meaning. The same is true for other ecological restoration technologies. That should give us pause.

Yet our pause cannot be long. The prospects for biodiversity in the face of climate change and other anthropogenic disturbances are quickly deteriorating, and technological capacities and opportunities are as swiftly advancing. A concern for sustainability necessitates that we conserve core values and relationships by managing the speed and scale of change (Thiele 2016). All available choices in this endeavor will be complex and compromised. Associated risks, benefits, and costs will be uncertain. As nature is a core value replete with core relationships, however, we cannot afford to neglect our responsibility to collectively govern ecological restoration technologies.

Notes

1. 

http://biohack.sourceforge.net/, last accessed April 27, 2020.

2. 

https://reviverestore.org/about-the-passenger-pigeon/, last accessed April 27, 2020.

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