The ecology of de‐extinction

Functional Ecology 2017, 31, 992–995 doi: 10.1111/1365-2435.12856 EDITORIAL The ecology of de-extinction Philip J. Seddon* Department of Zoology, University of Otago, PO Box 56, Dunedin 9015, New Zealand Responses to technical innovations are varied, with some people engaging early with new technology and pushing the envelope to see what could be achieved, whereas others push back against change. Then there are those who are most interested in the implications of a new way of doing something. Often the reality of a technical advance means users are obliged to adjust; for example, to electronic money transfer (Freedman 2000). Sometimes, the mere promise or potential of something revolutionary is enough to force a reaction, for example, cold fusion (Close 1991). De-extinction, the resurrection of extinct species, sits in this second category. Not so much a single technical advance (though the new gene-editing tool CRISPR will be transformative), as a coming together of developing techniques that make a new application possible – and it is possible, make no mistake. The next decade will see the cloning or genetic reconstruction of some version of a formerly extinct species; one that will live long enough to breathe and shake its fur, feathers, or scales, or to unfurl a leaf. The technical challenges that remain are formidable, but so very much has already been achieved along the de-extinction pathway. I’m often asked, ‘Is this really possible?’ My answer is yes – de-extinction has moved from science fiction to science feasibility - and I point to the case of the successful cloning using tissue from the extinct Pyrenean ibex and a hybrid goat as a gestational surrogate (Folch et al. 2009). It was only 6 years ago that a New Zealand politician was mocked by his Parliamentary colleagues for mooting the idea of de-extincting (we still need to get the verb right) the moa (Smith 2014). Since then some serious and seriously smart people have been working towards resurrecting (a better word) the moa, the passenger pigeon, even the woolly mammoth. The prospect of de-extinction has stimulated the public debate and galvanized the media. True, they have to get past the obsession with mammoths, but at least, it is widely understood that dinosaurs are not on any de-extinction candidate lists. Much of the general discussion has dealt with ethical issues, revisiting the genetically modified organism (GMO) debate and questioning the hubris of ‘playing God’, our duty to right past wrongs, and the moral hazards of changing the public perceptions of the finality of species extinction (Sandler 2013). On the other side, much of the technical material concerns how de-extinction might be achieved, and there are many who *Correspondence author. E-mail: [email protected] feel that once the technical hurdles are passed, well, then we are away! But ‘away’ to what? What is all this for anyway? Phenotypic look-alikes, clones, and GE versions of extinct species will of course be the subject of intense scientific scrutiny, and no doubt, the more charismatic versions (think mammoths again) will generate huge revenues as public exhibits, but the creation of lab specimens and curiosities cannot be a defensible end goal for de-extinction. The conservation visionary Stewart Brand has eloquently framed the goals of de-extinction as ‘deep ecological enrichment’ (Brand 2012), meaning that populations of resurrected individuals should resume their roles in the natural environment, restoring ecosystem functions lost through extinctions. This seems intuitively both desirable, and fraught with risk and uncertainty. If de-extinction endeavours are to contribute to increasing biodiversity, restoring ecosystem functions, and enhancing ecosystem resilience, then we are looking at the release of resurrected individuals into suitable areas of habitat. This fundamental aspect of de-extinction has received relatively scant attention, but is arguably the most critical component of the whole venture. Introduction to the special feature The six papers presented in this special feature have been selected to be a first attempt to consider the feasibility, desirability, and the implications of the translocation (movement and release) of resurrected forms with the aim of achieving some conservation benefit. Beth Shapiro (2017) starts the feature by reviewing the three commonly understood pathways to de-extinction: back breeding, cloning, and genomic reconstruction, and discusses the current state-of-the-art, and importantly, the limitations of each. This is a critical starting point and the one that has not been fully explored, nor well-communicated to the media or public. The general and implicit assumption, encouraged by the term de-extinction itself, has been that some sort of technical wizardry will restore individuals of an extinct species in toto, for after all, you can clone your pet, can’t you? And a clone of a dog is still a dog, isn’t it? Well, yes, but. . . if you are trying to clone a dog when there are no more dogs in the world, you have to use frozen dog cells, and you have to find some surrogate host that is not a dog but some other species. Inter-species cloning might produce something that differs from the © 2017 The Author. Functional Ecology © 2017 British Ecological Society Editorial original in a number of important ways. Even placing philosophical concerns over the authenticity aside, and genetic, epigenetic, microbiomic, physiological, and behavioural differences between a resurrected form and the extinct original means that extinction, under our current technological capacity, remains a fundamental one-way threshold for many taxa. Ethically, this is critical because it preserves the case that extinction is to be avoided at all costs as the prospect of future ‘de-extinction’ will not fully restore what has been lost. Shapiro concludes more optimistically by reinforcing the case that a defensible conservation objective of de-extinction is the creation of functional proxies of an extinct species to restore lost ecological functions (sensu IUCN 2016), thus a precise replicate of an extinct species is not essential (Shapiro 2017). The other papers in the special feature proceed with this understanding, but use the term de-extinction in its general sense for simplicity since the points the authors make are valid whether we talk of functional proxies or true facsimiles of extinct species. The rest of the contributions to the special feature explore the feasibility, implications, and challenges of deextinction for conservation benefit, taking as their starting point the defensible objective of restoring lost ecosystem functions through the creation of functional proxies of extinct species and their (re)introduction into suitable areas of habitat, assuming there are no suitable extant species that could act as ecological replacements. The first key point of concern is one shared with the reintroduction of extant species, namely the constitution of appropriate founder groups with the potential to establish relatively large and genetically diverse populations. Tammy Steeves and her co-authors frame this challenge in terms of conservation genetics and argue the need to preserve evolutionary potential to enable reintroduced populations of resurrected species to adapt to changing environments (Steeves, Johnson & Hale 2017). They identify a number of genetic bottlenecks that carry a risk of re-extinction, including preextinction bottlenecks that limit the variety of the genetic material available for cloning or genomic engineering; captivity bottlenecks in the pre-release stages that could lead to unequal founder representation, and translocation bottlenecks arising because not all founders will survive to contribute to future generations. Steeves, Johnson & Hale (2017) highlight that ongoing genetic supplementation is likely to be a requirement for any de-extinction project. De-extinction efforts tend to be concentrated either on creating phenotypic facsimiles or mimicking the biology of extinct species, but less attention has been paid to whether proxy forms will resurrect the lost ecology of an extinct species. Douglas MacCauley and colleagues take up this point and review the challenges and opportunities in recovering function through de-extinction, applying their ideas to two high-profile case studies, woolly mammoth and passenger pigeon. They conclude that recently extinct species, from groups with low-functional diversity, and with the potential to be restored to ecologically meaningful 993 densities, will make the best de-extinction candidates (McCauley et al. 2017). Interestingly, neither the mammoth nor the passenger pigeon ranks as good candidates against these criteria. Alexandre Robert et al. aim to understand how the evolutionary processes might influence the dynamics of populations of resurrected species, for the first time considering de-extinction from micro- and macro-evolutionary conservation perspectives (Robert et al. 2017). Extinction marks a discontinuity of biological processes and essentially removes the extinct organism from exposure to the selection pressures of future environmental change. Robert argues therefore, that de-extinction efforts to restore lost functions could be jeopardized by maladaptation of the proxy form, which might anyway fail to find a niche in a community where changes in the functionality have been provided by extant species. Robert suggests that conservation benefits from de-extinction are thus most likely to accrue if little time has passed since extinction. This would place the emphasis on selecting de-extinction candidates from the recent extinctions, and these candidates would also be those species for which cloning, rather than genomic engineering, would be feasible. Robert points out a paradox arising from a focus on evolutionarily distinct species as the best candidates to restore lost ecosystem functions because they have no extant replacements; such species might prove to be the hardest to resurrect because of an absence of egg donors, host surrogates, or reference species for genome reconstruction (Robert et al. 2017). The take-home message is that, whilst ecological roles might be restored through de-extinction, the evolutionary loss caused by extinction is irreversible. There is justified concern that the release of resurrected species might have deleterious impacts on recipient systems because of ecosystem changes since extinction. For extinctions in the distant past, we lack direct information about the ways in which species interacted, making it challenging to anticipate the consequences of reintroducing lost components. Jamie Wood and co-authors demonstrate how palaeoecological investigations can assess the potential ecosystem-level impacts of prehistoric de-extinction candidates, enabling ranking of candidates in relation to their likely ecological contribution (Wood, Perry & Wilmshurst 2017). They use the case study of New Zealand birds to construct an ecological interaction network into which they introduce two species of extinct moa, but point out that whilst habitat and dietary features are most readily understood, the palaeoecological record is silent on interactions driven by social structure and learnt behaviour. Critically, they also highlight the potential mismatch between what the palaeoecological record can tell us, and the state of current environments that have been subject to change and the arrival of invasive species and novel interactions since extinction (Wood, Perry & Wilmshurst 2017). The technical potential for de-extinction is clearly not the only consideration; the papers discussed above make it clear that a number of considerable challenges remain in © 2017 The Author. Functional Ecology © 2017 British Ecological Society, Functional Ecology, 31, 992–995 994 Editorial seeking conservation benefit from the environmental release of resurrected species. Extinction marks an irreversible break in the eco-evolutionary trajectory of a species (Robert et al. 2017); there is a need to preserve the evolutionary potential of resurrected species by overcoming genetic bottlenecks at every stage of a project (Steeves, Johnson & Hale 2017); there is some uncertainty around whether a resurrected species might ever be restored to functionally meaningful densities (McCauley et al. 2017), and our knowledge of past ecosystems will be incomplete for all but recent extinctions, making it difficult to predict the implications and impacts of attempts to restore the ecological interactions that have been lost with extinction (Wood, Perry & Wilmshurst 2017). But let’s assume that we have been able successfully to resurrect through interspecies cloning, sufficient numbers of sufficiently genetically diverse individuals of a reasonable proxy of a species that went extinct relatively recently, and that its reintroduction has the potential to restore, within a largely intact and well-understood ecosystem, some ecological function lost through extinction. Surely then we can be assured of achieving some conservation benefit? Not necessarily, as we must also consider the flip side to conservation benefit and ask the question: is there any risk or impact of this action on extant species? Impacts might be direct (e.g. predation) or indirect (e.g. competition), but are not only ecological. One of the criticisms levelled at the de-extinction enterprise has been the diversion of scarce resources away from the conservation of extant biodiversity (Donlan 2014). This concern has been countered by the suggestion that funding for species resurrection would tap into new sources, engaging those sponsors and granting agencies which would not otherwise be interested in supporting conservation (Jones 2014). This might be so, but commentators tend to focus only on costs of the technical processes of de-extinction; de-extinction is not cost neutral. If the purpose of de-extinction is conservation benefit, then resurrected species need to be released into natural systems, and as soon as they are released they become the responsibility of the managers of those systems. The expenditure of resources does not cease at that point, instead the costs will transfer to those charged with management of biodiversity, or rather with attempts to slow the rates of biodiversity loss – a battle we are not currently winning globally (WWF 2016). Gwen Iacona and co-authors take up this point and advocate for the use of well-tested conservation prioritization frameworks to explore how de-extinction efforts might influence the management of extant species. Iacona et al. (2017) model de-extinction as a reversible link in what was once a one-way path from extant to extinct, and demonstrate that this can change how resources should be allocated to recovery efforts. It has been argued before that the release of a resurrected species is a reintroduction (Seddon, Moehrenschlager & Ewen 2014), and we see from Steeves, Johnson & Hale (2017) that the release of large numbers of suitable founders will be one requisite of restoration success. Intensive post-release monitoring will also be required to track outcomes, in terms of both focal species population establishment and growth, and the ecological consequences for other ecosystem components. This is likely even to be a legislative requirement, given that the process of resurrection will result in the GMOs (Shapiro 2017) that will thus be subject to particular scrutiny. Resources expended on monitoring and managing resurrected species might be the resources not being applied to managing threats to extant species. Application of decision science can be used to inform the selection of appropriate deextinction candidates, heading off ill-considered efforts to restore species that will carry unacceptably high risks to the management of extant biodiversity. De-extinction will be pursued – the reality of the idea is too sexy to ignore, and it could be driven by aesthetic, commercial, scientific, or some other hitherto unanticipated imperatives and motivations. A defensible objective for de-extinction is to seek some conservation benefit, and a realistic conservation benefit is the restoration of lost ecosystem functions. But, seeking benefits is not the same as achieving them. Discussions in the literature to date have focused on the considerable ethical and technical challenges involved in producing even one living version of an extinct species, but potentially even greater challenges lie in the processes of restoring viable populations of resurrected species to areas of intact habitat. The contributions to this special feature consider the deeper implications of the ‘ecology of de-extinction’, when things move from the lab to the field. There seem to be two principal messages arising from these papers. The first is that the risks and the uncertainties involved will be hugely reduced, and hence the likelihood of achieving a conservation benefit from the production and release of resurrected species will be enhanced, if de-extinction candidates are drawn from the most recent extinctions. Second, and perhaps most importantly, extinction of any species marks a significant threshold that once crossed, cannot be fully reversed, despite the apparent promise of powerful new technologies. Our primary conservation objective must therefore be, as it always has been, avoiding species loss, and one the most significant contributions to be made by ‘de-extinction technology’ might well be to prevent extinctions in the first place. Acknowledgements I would like to thank Ken Thompson for proposing that Functional Ecology would be an excellent venue for a de-extinction special feature, Jennifer Meyer for her assistance with the editorial process, the great many anonymous reviewers, and Gwen Iacona, Doug McCauley, Alex Robert, Beth Shapiro, Tammy Steeves, Jamie Wood, and all their co-authors, for responding to my requests by producing the insightful contributions that make up this special feature. Ryan Phelan kindly commented on an early version of this paper. References Brand, S. 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