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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 pressures, and (4) contribute to the restoration of ecosystem structure and function.
Front Ecol Environ 2009; doi:10.1890/080028
A
s a matter of policy, scientists and land managers
sometimes emphasize protection and sustainability
of lands that have been only minimally altered by anthropogenic influences. The goal, with these less altered
ecosystems, is to maintain endemic genotypes. On the
other hand, many ecosystems have been drastically
altered (ie domesticated), leaving very few truly wild
places on Earth (Kareiva et al. 2007). Previous generations of conservationists have written off lands impacted
by humans as “lost causes”, yet the discipline of restoration ecology has emerged, with the goal of restoring
ecosystem processes to such lands (MacMahon 1997).
Many scientists believe that these domesticated systems
must be managed at some point (Gallagher and
Carpenter 1997). Hobbs et al. (2006) suggest managing
highly modified systems for utilitarian purposes when a
In a nutshell:
• Indigenous genetic material may no longer be adapted in modified ecosystems that have crossed ecological thresholds
• Genetically manipulated plant materials developed to overcome common biotic and abiotic stresses are useful for restoring
ecosystem structure, function, and biodiversity in modified
ecosystems
• Considering both empirical performance and geographic origin
is important when fashioning plant materials to assist evolution
along a desirable trajectory
USDA-Agricultural Research Service, Forage and Range Research
Laboratory, Utah State University, Logan, UT *(thomas.jones@
ars.usda.gov)
© The Ecological Society of America
return to their previous state is not feasible. Kareiva et al.
(2007) challenge scientists to manage these landscapes
by balancing trade-offs between ecosystem services.
Ultimately, to be successful, management objectives must
be based on pragmatism (Hobbs et al. 2006) and sound
scientific principles (Gallagher and Carpenter 1997).
Here, we consider issues surrounding the development
and choice of plant propagation materials for restoring
domesticated ecosystems. First, as an example of a domesticated landscape, we describe the modification of western North America’s sagebrush steppe by an invasive
plant–wildfire cycle. Next, we make the argument for
plants that restore evolutionary and ecological processes
under such dramatic circumstances. Finally, we contend
that human-assisted evolution offers the best hope for
repairing ecosystem structure and function when landscapes have become domesticated. We use the term “ecological restoration” in the broad sense – that is, “the
process of assisting the recovery of an ecosystem that has
been degraded, damaged, or destroyed”, as defined by the
Society for Ecological Restoration International Science
and Policy Working Group (SER 2004).
A controversial topic: options for restoration plant
materials
Two paradigms have long vied for the allegiance of scientists who develop plant materials for restoration. The
“evolutionary” paradigm seeks to restore putative natural
patterns of genetic variation, in order to generate an evolutionary trajectory as similar as possible to that which
prevailed before the advent of any anthropogenic disturwww.frontiersinecology.or g
Assisted evolution in domesticated landscapes
bance, such as weed invasion or soil degradation. Great
importance is therefore placed on genetic identity. In
contrast, the “resource” paradigm depends on the delivery
of economic products and ecosystem services, with minimal regard for species or genotype. These two models
have arisen within scientific traditions with contrasting
attitudes toward the conservation of biological resources
and with distinct philosophical beliefs as to how the
world should be. In the US, this distinction corresponds
to the historic division between the biocentric philosophy of John Muir and the anthropocentric philosophy of
Gifford Pinchot. These contrasting viewpoints influence
the choice of seeds used in restoration projects; indeed,
there has long been a healthy diversity of opinions
regarding standards for the genetic identity of plant materials with the ecosystem restoration community.
But what is the best approach in choosing plants for the
restoration of modified environments where domesticated nature is the most viable remaining option? Vast
landscapes in the North American Intermountain West,
for example, are increasingly being modified by plant
invasions, degradation of soil and hydrological processes,
and loss of biodiversity. Under such conditions, the evolutionary paradigm alone will not be able to overcome
the problems encountered when modified conditions render local populations less adapted than before. Here, we
suggest that both paradigms have an important role in the
restoration of damaged wildlands. Wise land managers
will try to combine principles from both traditions to
effectively realize their restoration objectives.
We developed the Restoration Gene Pool (RGP) concept (Jones 2003; Jones and Monaco 2007) to clarify
plant options for restoration. The four RGPs – primary,
secondary, tertiary, and quaternary – are placed in
descending order of preference to the restoration practitioner. The primary RGP includes materials that are
indigenous to the restoration site and to ecologically similar sites, as well as material from sites that are genetically
connected to the site. Typically, seeds are either collected
directly from the site or propagated under cultivation
from wildland seed collections. The secondary RGP consists of target-species material that is disqualified from the
primary RGP, based on the definition given above.
Typically, secondary RGP materials are intended for
broader geographical use than are primary RGP materials;
they are often “releases”, either cultivars or pre-variety
germplasms (propagating material that has not yet been
released as a variety), meaning that they have undergone
an administrative approval process based on evaluation of
adaptive performance before distribution to seed growers
for commercial production. The tertiary RGP consists of
material that has been intentionally manipulated
through hybridization across a natural genetic barrier, in
order to introduce traits of adaptive or economic importance. The quaternary RGP is composed of functional surrogate species that are used when the target species is no
longer adapted to the modified environment.
www.fr ontiersinecology.or g
TA Jones and TA Monaco
When are genetically manipulated plants an
appropriate choice?
Anthropogenic disturbances may cause plant communities to cross one or more ecological thresholds, which will
be difficult or impossible to reverse. We suggest that the
decline of local genotypes under such conditions indicates
that the primary RGP is no longer as well adapted to the
local environment as it once was, and that this decline is
a consequence of natural selection, a process that under
“natural” circumstances is considered desirable (Meffe
and Carroll 1997). The anthropogenic perturbation of the
sagebrush–steppe ecosystem is unnatural, but the biological response to the perturbation is in accordance with the
normal workings of nature (Botkin 1990).
Although the “local is best” assumption (Johnson et al.
2004) that underpins the general preference for the primary RGP is arguably valid when thresholds have not yet
been crossed, we contend that, for altered ecosystems,
this debate may be moot. Instead, the appropriate question becomes, “is local still good enough to confer
acceptable ecological function now that novel evolutionary forces are at work?”. We believe that local may no
longer be good enough, based on simple observation; that
is, if local was still good enough, we would not have an
invasive plant problem. The essential question then
becomes, “can we design better plant materials for the
monumental challenge sitting on our doorstep?”.
Costs and risks
If we are to pursue a comprehensive plant materials
approach, such as that described above, the associated
costs and risks must be considered. The first cost results
from the research infrastructure required to develop the
plants. A multidisciplinary, problem-solving approach
and a long-term commitment are essential. Specific goals
for improving ecological function in western North
America include controlling wildfire, inhibiting invasive
plant populations, and restoring soil structure and nutrient dynamics. To be successful, plant ecologists, physiologists, soil scientists, rangeland scientists, seed scientists,
geneticists, plant breeders, weed scientists, and engineers
must all work together to confront the problem at various
ecological scales. The research objective must be to
develop seeding technologies, weed management protocols, and plant materials that may be prescribed for rehabilitating the land and restoring ecological structure,
function, and diversity.
Prerequisites for success include an understanding of
how desirable species interact with invasive plants at all
life stages, and how these interactions may favorably
enhance the population demographics of desirable
species. It is also important to understand how these communities assemble (Nuttle et al. 2004). In this regard, a
good working knowledge of (1) functional groups and the
concomitant redundancy among species and (2) the traits
that confer such functional attributes is useful, especially
© The Ecological Society of America
TA Jones and TA Monaco
Assisted evolution in domesticated landscapes
Oregon
Oregon
Idaho
Burns
Idaho
Burns
Idaho Falls
Idaho Falls
Boise
Boise
Twin Falls
Twin Falls
Klamath Falls
Klamath Falls
Elko
Elko
Salt Lake City
Nevada
Reno
Utah
Ely
Nevada
Utah
Ely
or
lif
Ca
a
ni
a
ni
or
lif
Ca
Cedar City
Cedar City
Las Vegas
Las Vegas
(a)
(b)
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
native plant populations in order to maximize resource use
over time and space in order to assemble weed-resistant
plant communities (Sheley and Carpinelli 2005).
To place plant material development efforts on an ecological footing, we integrate them with the successional
management model developed by Pickett et al. (1987).
This model identifies three general causes of succession:
site availability, species availability, and species performance. Sheley et al. (2006) provided data to support the
hypothesis that establishment and persistence of desirable
native plants are enhanced when weed management protocols address factors that modify or repair processes that
influence Pickett et al.’s (1987) three causes of succession.
Some biologists believe that the release of novel genetic
material is inherently risky. For example, outbreeding
depression (ie offspring from crosses between individuals
from different populations have lower fitness than offspring
from crosses between individuals from the same population) may result when seeded material hybridizes with remnants of naturally occurring populations (Hufford and
Mazer 2003). This potential risk is reduced by choosing
plant materials that reflect the most current scientific
understanding of infraspecific taxonomy and metapopulation structure. It is also important to remember that when
outbreeding depression is expressed in initial hybridization
products, it may still be overcome as a result of the
processes of natural selection and/or introgression of small
portions of one genotype into another (Carney et al. 2000),
ultimately resulting in adapted plant material.
© The Ecological Society of America
A second concern is the maladaptation of novel plant
material over the long term. In fact, restoration is necessitated because the indigenous plants have proven to be maladapted in the short term. Conversely, some researchers
consider genetically altered materials to be too well
adapted and therefore potentially invasive, but this argument does not hold in stressful or competitive environments, where unaltered genetic material of the same
species has been unsuccessful in coping with abiotic stress
or competition. Finally, because of serious concerns regarding the genetic integrity of threatened and endangered
species, genetic manipulation of closely related plants
must be avoided, to preclude undesirable hybridization.
Ecosystem degradation in the sagebrush steppe
The US Department of the Interior’s Bureau of Land
Management (BLM) administers 73 million acres of
rangeland in the 135 million-acre floristic Great Basin
(Figure 1a). Fifty-seven million acres (54%) in this region
are occupied by sagebrush–steppe ecosystems, with the
iconic big sagebrush (Artemisia tridentata Nutt) as the primary sagebrush species (Figure 1b).
Invasive annual grasses, particularly cheatgrass (Bromus
tectorum), are an increasing threat to the integrity of
these wildlands. Cheatgrass has come to dominate large
areas of this region, and even more extensive areas are
believed to be at risk of future invasion (Wisdom et al.
2005; Bradley and Mustard 2006; Figure 2). Cheatgrass
can adapt to novel environments, possibly because its
www.frontiersinecology.or g
M Pellant/BLM
Reno
Salt Lake City
M Pellant/BLM
Assisted evolution in domesticated landscapes
Cheatgrass risk
Decile
Low
High
TA Jones and TA Monaco
N
0
200
400
Kilometers
Figure 2. Map of risk of cheatgrass distribution, based on soil, elevation, and
precipitation variables.
substantial genetic diversity is highly correlated with its
habitat and ecological traits (Ramakrishnan et al. 2006).
Moreover, it has a high degree of phenotypic plasticity
(Novak et al. 1991).
Wildfire frequency has greatly increased in the floristic
Great Basin, as a result of cheatgrass invasion (Figure 3).
Cheatgrass generates horizontally continuous fuels with surface-to-volume and fuel-packing ratios that favor ignition
and perpetuate a cheatgrass–wildfire cycle (Brooks et al.
2004). This cycle results in conversion of sagebrush–steppe
ecosystems to cheatgrass-dominated annual grasslands that
experience frequent wildfires, resulting in extirpation of
local populations of fire-intolerant shrubs, such as big sagebrush (Whisenant 1990).
From 1990 to 2007, over 16 million acres burned in the
Great Basin region, and nearly 2 million of these involved
repeated burns of the same acreage (M Pellant pers comm).
The most extensive fire years in this period have been 1996
(2.2 million acres), 1999 (2.7 million), 2000 (1.9 million),
2001 (1.6 million), 2006 (1.8 million), and 2007 (2.7 million). On the other hand, in some years, fire in the region is
relatively infrequent, eg 1993 (43 000 acres), 1997
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(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, subsequently, 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 grazing 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 stability, hydrology, and nutrient dynamics; King
and Hobbs 2006) recover only with intensive
human intervention. Emerging evidence suggests 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
recognize that distinct seral stages are a consequence of the current disturbance regime
(Allen-Diaz and Bartolome 1998).
Restoration plans in relation to
evolutionary and ecological processes
Many have lamented that restoration plans commonly
fail to consider evolutionary processes, particularly for
drastically altered, domesticated ecosystems (Smith and
Bernatchez 2008). Ashley et al. (2003) discuss the advisability of permitting evolution to confer adaptation to
disturbed habitats, a relatively rapid process referred to by
Hendry and Kinnison (1999) as “contemporary evolution”. A functional, altered state may be preferred over
the predisturbance state, when the latter is problematic
because of an ongoing need for human intervention
(Ashley et al. 2003), financial limitations, or shifting priorities (Schlaepfer et al. 2005). Ashley et al. (2003)
attribute preference for the predisturbance state to typological thinking – that is, the idea that species are fixed
entities. This viewpoint seems to be motivated by the
equilibrium (“balance of nature”) paradigm, a view of
nature that has lost favor in recent years (Botkin 1990;
Pickett et al. 1992).
We propose a comprehensive view for plant materials
development for the greatest restoration challenges –
those domesticated landscapes that have moved to a per© The Ecological Society of America
Assisted evolution in domesticated landscapes
Ecosystem function
manently altered state, as has occurred in the
Montana
floristic Great Basin. Our comments are based
on this region as a case study and must not be
Oregon
construed as generally applicable to more malBoise
leable environments that are relatively responsive to restoration treatments; nevertheless,
our remarks may apply to other, highly modiIdaho
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
Lake
function, and successional and evolutionary
City
processes that prevailed prior to disturbance? If
Carson
City
so, B¡A conversion may be achieved by reintroduction 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
Fresno
services targeted for restoration have been
severely impaired, the primary RGP may be
inadequate to effect a successful restoration
Las
(Jones 2003). The primary aim, then, is to
Vegas
trigger natural processes that re-establish
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 “rehabilitation”. 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
similar climate (primary RGP), with genotypes from the
ondary RGPs may suffice for the latter.
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
Abiotic
Biotic
genetic material may rescue threatened poputhreshold
threshold
Primary processes
lations (Stockwell et al. 2003). Projects that
fully functional
place a priority on increasing effective populaPrimary processes
partially functional
tion size and precluding selection often fail to
Primary processes
consider that adaptation entails selective loss
nonfunctional
of genetic variation, increased inbreeding
among individuals with higher fitness, and ini(A)
(C)
(B)
tial reductions in effective population size
Improved
Physical
(Kinnison et al. 2007).
management
modification
Manipulation of
Microevolutionary processes may generate
required
required
biota required
site-adapted genotypes from generally
adapted ones (Moritz 2002). Priming these
Time or disturbance intensity
processes with sizable quantities of adaptive
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).
© The Ecological Society of America
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M Pellant/BLM
TA Jones and TA Monaco
Assisted evolution in domesticated landscapes
TA Jones and TA Monaco
(d)
(a)
M Pellant/BLM
M Pellant/BLM
USDA-NRCS
ural selection operates; (2) subjecting
populations that reflect primary RGP
boundaries, as established by phylogeographic, 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
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)
and long-term evolutionary potential
(f)
(c)
(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.
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.
Genetically manipulated material, based on local geno Conclusions
types, 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 catbelieve 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 reclamationenvironmental 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 compresence 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 (represenpredict the plant material’s prospects for success.
tation) and genetic variation for adaptive traits (persisFor 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.fr ontiersinecology.or g
© The Ecological Society of America
TA Jones and TA Monaco
under particular circumstances and deserves serious consideration as an option for restoration.
Acknowledgments
The contributions of S Knick (USGS) and M Pellant
(BLM) and the helpful critiques of M Kinnison, P Adler,
E Leger, B Roundy, and A Svejcar are gratefully acknowledged.
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