A Role for Assisted Evolution in Designing Native Plant Materials for Domesticated Landscapes TA Jones* and TA Monaco

CONCEPTS AND QUESTIONS A role for assisted evolution in designing native plant materials for domesticated landscapes TA Jones* and TA Monaco

Developers of native plant propagation materials for wildland restoration may emphasize naturally occurring genetic patterns or, in contrast, the material’s empirical performance in comparative field trials. We contend that both approaches have value and need not be mutually exclusive. Anthropogenic influences have pushed many ecosystems across ecological thresholds, to less desirable states, so that actively managing for “domesticated nature” – nature as modified, either intentionally or inadvertently, by humans – is more realistic and more likely to succeed than recreating the original ecosystem. Furthermore, when domesticated nature is the most reasonable objective, empirical performance, together with geographical origin, are plausible criteria for choosing restoration plant material. For altered ecosystems, we suggest that evolution should be assisted by the inclusion of plants that (1) reflect general historical evolutionary patterns, (2) are particularly suited to the modified environment, (3) are able to adapt to contemporary selection pres- sures, and (4) contribute to the restoration of ecosystem structure and function.

Front Ecol Environ 2009; doi:10.1890/080028

s a matter of policy, scientists and land managers return to their previous state is not feasible. Kareiva et al. A sometimes emphasize protection and sustainability (2007) challenge scientists to manage these landscapes of lands that have been only minimally altered by anthro- by balancing trade-offs between ecosystem services. pogenic influences. The goal, with these less altered Ultimately, to be successful, management objectives must ecosystems, is to maintain endemic genotypes. On the be based on pragmatism (Hobbs et al. 2006) and sound other hand, many ecosystems have been drastically scientific principles (Gallagher and Carpenter 1997). altered (ie domesticated), leaving very few truly wild Here, we consider issues surrounding the development places on Earth (Kareiva et al. 2007). Previous genera- and choice of plant propagation materials for restoring tions of conservationists have written off lands impacted domesticated ecosystems. First, as an example of a domes- by humans as “lost causes”, yet the discipline of restora- ticated landscape, we describe the modification of west- tion ecology has emerged, with the goal of restoring ern North America’s sagebrush steppe by an invasive ecosystem processes to such lands (MacMahon 1997). plant–wildfire cycle. Next, we make the argument for Many scientists believe that these domesticated systems plants that restore evolutionary and ecological processes must be managed at some point (Gallagher and under such dramatic circumstances. Finally, we contend Carpenter 1997). Hobbs et al. (2006) suggest managing that human-assisted evolution offers the best hope for highly modified systems for utilitarian purposes when a repairing ecosystem structure and function when landscapes have become domesticated. We use the term “ecological restoration” in the broad sense – that is, “the In a nutshell: process of assisting the recovery of an ecosystem that has • Indigenous genetic material may no longer be adapted in mod- been degraded, damaged, or destroyed”, as defined by the ified ecosystems that have crossed ecological thresholds Society for Ecological Restoration International Science • Genetically manipulated plant materials developed to over- and Policy Working Group (SER 2004). come common biotic and abiotic stresses are useful for restoring ecosystem structure, function, and biodiversity in modified ecosystems A controversial topic: options for restoration plant • Considering both empirical performance and geographic origin materials is important when fashioning plant materials to assist evolution along a desirable trajectory Two paradigms have long vied for the allegiance of scientists who develop plant materials for restoration. The “evolutionary” paradigm seeks to restore putative natural USDA-Agricultural Research Service, Forage and Range Research patterns of genetic variation, in order to generate an evo- Laboratory, Utah State University, Logan, UT *(thomas.jones@ lutionary trajectory as similar as possible to that which ars.usda.gov) prevailed before the advent of any anthropogenic distur-

© The Ecological Society of America www.frontiersinecology.org Assisted evolution in domesticated landscapes TA Jones and TA Monaco bance, such as weed invasion or soil degradation. Great When are genetically manipulated plants an importance is therefore placed on genetic identity. In appropriate choice? contrast, the “resource” paradigm depends on the delivery Anthropogenic disturbances may cause plant communi- of economic products and ecosystem services, with mini- ties to cross one or more ecological thresholds, which will mal regard for species or genotype. These two models be difficult or impossible to reverse. We suggest that the have arisen within scientific traditions with contrasting decline of local genotypes under such conditions indicates attitudes toward the conservation of biological resources that the primary RGP is no longer as well adapted to the and with distinct philosophical beliefs as to how the local environment as it once was, and that this decline is world should be. In the US, this distinction corresponds a consequence of natural selection, a process that under to the historic division between the biocentric philoso- “natural” circumstances is considered desirable (Meffe phy of John Muir and the anthropocentric philosophy of and Carroll 1997). The anthropogenic perturbation of the Gifford Pinchot. These contrasting viewpoints influence sagebrush–steppe ecosystem is unnatural, but the biologi- the choice of seeds used in restoration projects; indeed, cal response to the perturbation is in accordance with the there has long been a healthy diversity of opinions normal workings of nature (Botkin 1990). regarding standards for the genetic identity of plant mate- Although the “local is best” assumption (Johnson et al. rials with the ecosystem restoration community. 2004) that underpins the general preference for the pri- But what is the best approach in choosing plants for the mary RGP is arguably valid when thresholds have not yet restoration of modified environments where domesti- been crossed, we contend that, for altered ecosystems, cated nature is the most viable remaining option? Vast this debate may be moot. Instead, the appropriate ques- landscapes in the North American Intermountain West, tion becomes, “is local still good enough to confer for example, are increasingly being modified by plant acceptable ecological function now that novel evolution- invasions, degradation of soil and hydrological processes, ary forces are at work?”. We believe that local may no and loss of biodiversity. Under such conditions, the evo- longer be good enough, based on simple observation; that lutionary paradigm alone will not be able to overcome is, if local was still good enough, we would not have an the problems encountered when modified conditions ren- invasive plant problem. The essential question then der local populations less adapted than before. Here, we becomes, “can we design better plant materials for the suggest that both paradigms have an important role in the monumental challenge sitting on our doorstep?”. restoration of damaged wildlands. Wise land managers will try to combine principles from both traditions to Costs and risks effectively realize their restoration objectives. We developed the Restoration Gene Pool (RGP) con- If we are to pursue a comprehensive plant materials cept (Jones 2003; Jones and Monaco 2007) to clarify approach, such as that described above, the associated plant options for restoration. The four RGPs – primary, costs and risks must be considered. The first cost results secondary, tertiary, and quaternary – are placed in from the research infrastructure required to develop the descending order of preference to the restoration practi- plants. A multidisciplinary, problem-solving approach tioner. The primary RGP includes materials that are and a long-term commitment are essential. Specific goals indigenous to the restoration site and to ecologically sim- for improving ecological function in western North ilar sites, as well as material from sites that are genetically America include controlling wildfire, inhibiting invasive connected to the site. Typically, seeds are either collected plant populations, and restoring soil structure and nutri- directly from the site or propagated under cultivation ent dynamics. To be successful, plant ecologists, physiolo- from wildland seed collections. The secondary RGP con- gists, soil scientists, rangeland scientists, seed scientists, sists of target-species material that is disqualified from the geneticists, plant breeders, weed scientists, and engineers primary RGP, based on the definition given above. must all work together to confront the problem at various Typically, secondary RGP materials are intended for ecological scales. The research objective must be to broader geographical use than are primary RGP materials; develop seeding technologies, weed management proto- they are often “releases”, either cultivars or pre-variety cols, and plant materials that may be prescribed for reha- germplasms (propagating material that has not yet been bilitating the land and restoring ecological structure, released as a variety), meaning that they have undergone function, and diversity. an administrative approval process based on evaluation of Prerequisites for success include an understanding of adaptive performance before distribution to seed growers how desirable species interact with invasive plants at all for commercial production. The tertiary RGP consists of life stages, and how these interactions may favorably material that has been intentionally manipulated enhance the population demographics of desirable through hybridization across a natural genetic barrier, in species. It is also important to understand how these com- order to introduce traits of adaptive or economic impor- munities assemble (Nuttle et al. 2004). In this regard, a tance. The quaternary RGP is composed of functional sur- good working knowledge of (1) functional groups and the rogate species that are used when the target species is no concomitant redundancy among species and (2) the traits longer adapted to the modified environment. that confer such functional attributes is useful, especially www.frontiersinecology.org © The Ecological Society of America TA Jones and TA Monaco Assisted evolution in domesticated landscapes

Oregon Idaho Oregon Idaho

Burns Idaho Falls Burns Idaho Falls Boise Boise

Twin Falls Twin Falls Klamath Falls Klamath Falls

Elko Elko Salt Lake City Salt Lake City

Reno Nevada Utah Reno Nevada Utah Ely Ely California California

Cedar City Cedar City

Las Vegas Las Vegas

(a) (b) M Pellant/BLM Figure 1. Maps of the floristic Great Basin showing (a) BLM-administered lands (yellow) and (b) sagebrush–steppe rangelands (green). following disturbance. The ultimate objective is to restore A second concern is the maladaptation of novel plant native plant populations in order to maximize resource use material over the long term. In fact, restoration is necessi- over time and space in order to assemble weed-resistant tated because the indigenous plants have proven to be mal- plant communities (Sheley and Carpinelli 2005). adapted in the short term. Conversely, some researchers To place plant material development efforts on an eco- consider genetically altered materials to be too well logical footing, we integrate them with the successional adapted and therefore potentially invasive, but this argu- management model developed by Pickett et al. (1987). ment does not hold in stressful or competitive environ- This model identifies three general causes of succession: ments, where unaltered genetic material of the same site availability, species availability, and species perfor- species has been unsuccessful in coping with abiotic stress mance. Sheley et al. (2006) provided data to support the or competition. Finally, because of serious concerns regard- hypothesis that establishment and persistence of desirable ing the genetic integrity of threatened and endangered native plants are enhanced when weed management pro- species, genetic manipulation of closely related plants tocols address factors that modify or repair processes that must be avoided, to preclude undesirable hybridization. influence Pickett et al.’s (1987) three causes of succession. Some biologists believe that the release of novel genetic Ecosystem degradation in the sagebrush steppe material is inherently risky. For example, outbreeding depression (ie offspring from crosses between individuals The US Department of the Interior’s Bureau of Land from different populations have lower fitness than offspring Management (BLM) administers 73 million acres of from crosses between individuals from the same popula- rangeland in the 135 million-acre floristic Great Basin tion) may result when seeded material hybridizes with rem- (Figure 1a). Fifty-seven million acres (54%) in this region nants of naturally occurring populations (Hufford and are occupied by sagebrush–steppe ecosystems, with the Mazer 2003). This potential risk is reduced by choosing iconic big sagebrush (Artemisia tridentata Nutt) as the pri- plant materials that reflect the most current scientific mary sagebrush species (Figure 1b). understanding of infraspecific taxonomy and metapopula- Invasive annual grasses, particularly cheatgrass (Bromus tion structure. It is also important to remember that when tectorum), are an increasing threat to the integrity of outbreeding depression is expressed in initial hybridization these wildlands. Cheatgrass has come to dominate large products, it may still be overcome as a result of the areas of this region, and even more extensive areas are processes of natural selection and/or introgression of small believed to be at risk of future invasion (Wisdom et al. portions of one genotype into another (Carney et al. 2000), 2005; Bradley and Mustard 2006; Figure 2). Cheatgrass ultimately resulting in adapted plant material. can adapt to novel environments, possibly because its

(92 000), and 2004 (17 000), highlighting the vacillating nature of the problem. Whisenant (2002) provides a three-stage model that reflects this ecosystem degradation. Degradation increases, initially, as a biotic threshold is crossed (A¡B) and, subse- quently, as an abiotic threshold is crossed (B¡C; Figure 4). At stage A, recovery of damaged ecosystem function is facilitated by removal of the causal agent (eg excessive graz- ing pressure). After crossing the biotic threshold from stage A to B, manipulation of biota – seeding, for instance – is required, but abiotic function remains mostly intact. Large expanses of the sagebrush–steppe ecosystems have crossed the biotic threshold (A¡B) as a result of cheatgrass invasion (Figure 5). After crossing the abiotic threshold from stage B to C, biotic processes are severely impaired, and abiotic processes (eg soil stabil- ity, hydrology, and nutrient dynamics; King and Hobbs 2006) recover only with intensive human intervention. Emerging evidence sug- gests that cheatgrass dominance is moving sagebrush–steppe ecosystems across an abiotic threshold (B¡C) as soil structure (Norton et al. 2007) and nutrient dynamics (Saetre and Stark 2005) are altered. Resource managers Cheatgrass risk recognize that distinct seral stages are a conse- Decile N Low 0 200 400 quence of the current disturbance regime

High Kilometers (Allen-Diaz and Bartolome 1998). M Pellant/BLM Figure 2. Map of risk of cheatgrass distribution, based on soil, elevation, and precipitation variables. Restoration plans in relation to evolutionary and ecological processes substantial genetic diversity is highly correlated with its habitat and ecological traits (Ramakrishnan et al. 2006). Many have lamented that restoration plans commonly Moreover, it has a high degree of phenotypic plasticity fail to consider evolutionary processes, particularly for (Novak et al. 1991). drastically altered, domesticated ecosystems (Smith and Wildfire frequency has greatly increased in the floristic Bernatchez 2008). Ashley et al. (2003) discuss the advis- Great Basin, as a result of cheatgrass invasion (Figure 3). ability of permitting evolution to confer adaptation to Cheatgrass generates horizontally continuous fuels with sur- disturbed habitats, a relatively rapid process referred to by face-to-volume and fuel-packing ratios that favor ignition Hendry and Kinnison (1999) as “contemporary evolu- and perpetuate a cheatgrass–wildfire cycle (Brooks et al. tion”. A functional, altered state may be preferred over 2004). This cycle results in conversion of sagebrush–steppe the predisturbance state, when the latter is problematic ecosystems to cheatgrass-dominated annual grasslands that because of an ongoing need for human intervention experience frequent wildfires, resulting in extirpation of (Ashley et al. 2003), financial limitations, or shifting pri- local populations of fire-intolerant shrubs, such as big sage- orities (Schlaepfer et al. 2005). Ashley et al. (2003) brush (Whisenant 1990). attribute preference for the predisturbance state to typo- From 1990 to 2007, over 16 million acres burned in the logical thinking – that is, the idea that species are fixed Great Basin region, and nearly 2 million of these involved entities. This viewpoint seems to be motivated by the repeated burns of the same acreage (M Pellant pers comm). equilibrium (“balance of nature”) paradigm, a view of The most extensive fire years in this period have been 1996 nature that has lost favor in recent years (Botkin 1990; (2.2 million acres), 1999 (2.7 million), 2000 (1.9 million), Pickett et al. 1992). 2001 (1.6 million), 2006 (1.8 million), and 2007 (2.7 mil- We propose a comprehensive view for plant materials lion). On the other hand, in some years, fire in the region is development for the greatest restoration challenges – relatively infrequent, eg 1993 (43 000 acres), 1997 those domesticated landscapes that have moved to a per- www.frontiersinecology.org © The Ecological Society of America TA Jones and TA Monaco Assisted evolution in domesticated landscapes manently altered state, as has occurred in the floristic Great Basin. Our comments are based Montana on this region as a case study and must not be construed as generally applicable to more mal- Oregon leable environments that are relatively respon- Boise sive to restoration treatments; nevertheless, our remarks may apply to other, highly modi- Idaho fied systems. In order to determine whether they apply to some other recalcitrant systems, we suggest posing the following questions: Are undesirable modifications reversible? Is it possible to restore species composition, ecological Salt function, and successional and evolutionary Lake City processes that prevailed prior to disturbance? If Carson so, B¡A conversion may be achieved by rein- City troduction of the primary RGP. Under such Nevada circumstances, we believe that it is appropriate to focus on genetic identity when choosing Utah plant materials. In contrast, when ecosystem functions and California services targeted for restoration have been Fresno severely impaired, the primary RGP may be inadequate to effect a successful restoration (Jones 2003). The primary aim, then, is to Las Vegas

trigger natural processes that re-establish M Pellant/BLM ecosystem form and function, such as in Figure 3. Burn areas of the floristic Great Basin from 1990 to 2007, with Whisenant’s (2002) stage B and especially 1990 to 2006 in orange and 2007 in red. stage C, commonly referred to as “rehabilita- tion”. Because a C¡B conversion is more difficult than a longer well adapted. Rice and Emery (2003) concurred, B¡A conversion, the former may require use of the ter- recommending the use of a mixture of genotypes from tiary or quaternary RGPs, whereas the primary or sec- multiple indigenous populations from a region with a ondary RGPs may suffice for the latter. similar climate (primary RGP), with genotypes from the When the intent is to mirror historical genetic patterns, fringe of the species’ distribution (secondary RGP). the primary RGP is naturally preferred, because of its asso- Such a strategy balances the needs for current and future ciation with historical (long-term) evolutionary processes adaptation. (Meffe and Carroll 1997). Nevertheless, as demonstrated experimentally by Kinnison et al. Increasing degradation (2008) with respect to fitness-related traits in Chinook salmon (Oncorhynchus tshawytscha), contemporary evolution acting on non-local Biotic Abiotic genetic material may rescue threatened popu- threshold threshold lations (Stockwell et al. 2003). Projects that Primary processes fully functional place a priority on increasing effective popula- Primary processes tion size and precluding selection often fail to partially functional consider that adaptation entails selective loss Primary processes nonfunctional of genetic variation, increased inbreeding among individuals with higher fitness, and ini- (A) (B) (C) tial reductions in effective population size Ecosystem function (Kinnison et al. 2007). Improved Physical management Manipulation of modification Microevolutionary processes may generate required biota required required site-adapted genotypes from generally adapted ones (Moritz 2002). Priming these processes with sizable quantities of adaptive Time or disturbance intensity genetic variation may be more beneficial than insisting on conformity to naturally Figure 4. Three stages of degradation of ecosystem function (A, B, and C) occurring genetic arrays (ie the primary separated by biotic (A¡B) and abiotic (B¡C) thresholds. Modified from RGP), particularly if such material is no Whisenant (2002).

(a) (d) ural selection operates; (2) subjecting populations that reflect primary RGP boundaries, as established by phylo- geographic, ecoregion, or seed-transfer zone research, to artificial selection to confer enhanced fitness; or (3) hybridizing indigenous material with non-indigenous material tolerant to biotic and/or abiotic stress. We are USDA-NRCS intrigued that such approaches have (b) (e) also been proposed for animal populations (Schlaepfer et al. 2005). In this vein, Ferrière et al. (2004) recommended harnessing the forces of evolution to restore domesticated ecosystems. Stockwell et al. (2006) have sought to link historically established genetic diversity (the past) with contemporary evolution (the present) M Pellant/BLM and long-term evolutionary potential (c) (f) (the future). They argue that gene flow influences evolutionary change and enhances long-term persistence and that the positive effects of reduced inbreeding depression, increased genetic variation, and greater potential for future adaptation balance the negative impacts of gene flow.

M Pellant/BLM Emphasizing empirical performance Figure 5. Four stages of degradation of a sagebrush–steppe ecosystem: (a) fully in addition to geographic origin is a functional, with big sagebrush and perennial bunchgrass components; (b) crossing the pragmatic approach that focuses on biotic threshold (stages A¡B), as triggered by overgrazing and resultant loss of the what is technically feasible, yet respects perennial bunchgrass component; (c) stage B – invasion by cheatgrass; (d) high wildfire naturally occurring genetic arrays. The frequency, the trigger of the abiotic threshold (stages B¡C); (e) resultant loss of the big result may be plant materials that are sagebrush component; and (f) stage C – a cheatgrass-dominated annual community. better suited to domesticated landscapes under current and future conditions. Conclusions Genetically manipulated material, based on local genotypes, may be incorporated into the Jones and Monaco Geographic origin is important because it confers adaptive (2007) flowchart as the primary-C RGP. The flowchart traits that are geographically relevant. Nevertheless, we already supports an analogous, genetically manipulated cat- believe that the tacit assumption that local material will egory for the secondary RGP, termed secondary-C. demonstrate optimal performance, adaptation, and fitness, Although this approach will not appeal to everyone, it is despite severe disturbance, is unwarranted. The critical less manipulative than other options mentioned by Brooks issue for restoration plant material must be its adaptation et al. (2004). These include creating novel ecosystems from to the modified environment, which encompasses both native species, corresponding to the quaternary RGP (Jones genetic identity and empirical performance. The questions 2003), or using exotics to suppress invasive plants (such as must be: Is the material physiologically able to tolerate the cheatgrass), corresponding to the category of reclamation- environmental conditions and disturbance regime of the grade material (Jones and Monaco 2007). Finally, we believe modified site? Is it able to establish and persist, despite the that assisted evolution for domesticated ecosystems is com- presence of other organisms, including invasive plants? patible with Moritz’s (2002) strategies that seek to maximize Does it have the adaptive genetic variation necessary to both representation and persistence of genetic diversity. allow natural selection to assemble site-adapted genotypes Moritz advocates both historical genetic variation for which as needed? In essence, the answers to these questions will adaptive importance is not immediately apparent (represen- predict the plant material’s prospects for success. tation) and genetic variation for adaptive traits (persis- For domesticated nature, assisted evolution is an attrac- tence). We advocate a mixture of caution and pragmatism, tive option. It is implemented by (1) augmenting genetic meaning the least obtrusive approach resulting in improved variation in locally adapted populations upon which nat- ecosystem function. Assisted evolution offers these qualities www.frontiersinecology.org © The Ecological Society of America TA Jones and TA Monaco Assisted evolution in domesticated landscapes under particular circumstances and deserves serious consid- Meffe GK and Carroll CR. 1997. What is conservation biology? eration as an option for restoration. In: Groom MJ, Meffe GK, and Carroll CR (Eds). Principles of conservation biology. 2nd edn. Sunderland, MA: Sinauer Associates. 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