Download Plant fitness in a rapidly changing world

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Plant fitness in a rapidly changing world
Author for correspondence:
Jill T. Anderson
Tel: +1 706 542 0853
Email: [email protected]
Jill T. Anderson1,2
1
Department Genetics, University of Georgia, Athens, GA 30602, USA; 2Odum School of Ecology, University of Georgia, Athens,
GA 30602, USA
Received: 17 June 2015
Accepted: 25 August 2015
Contents
Summary
81
IV. Evolutionary consequences
84
I.
Introduction
81
V.
Conclusions
85
II.
Fitness landscapes
82
Acknowledgements
85
III.
Recommendations for future studies
84
References
85
Summary
New Phytologist (2016) 210: 81–87
doi: 10.1111/nph.13693
Key words: climate change, climatic
manipulation, evolution, fecundity, fitness,
germination, meta-analysis, migration.
Modern reliance on fossil fuels has ushered in extreme temperatures globally and abnormal
precipitation patterns in many regions. Although the climate is changing rapidly, other agents of
natural selection such as photoperiod remain constant. This decoupling of previously reliable
environmental cues shifts adaptive landscapes, favors novel suites of traits and likely increases
the extinction risk of local populations. Here, I examine the fitness consequences of changing
climates. Meta-analyses demonstrate that simulated future climates depress viability and
fecundity components of fitness for native plant species in the short term, which could reduce
population growth rates. Contracting populations that cannot adapt or adjust plastically to new
climates might not be capable of producing sufficient migrants to track changing conditions.
I. Introduction
Climate change brings to the forefront a long-standing question at
the interface of ecology and evolution: what are the evolutionary
consequences of rapid environmental change? The answer will shape
conservation priorities, shed light on the genetic and phenotypic
fates of communities, and enhance our understanding of evolution.
Climate change has already disrupted phenology and physiology,
and altered community dynamics (Elmendorf et al., 2012; Leonardi
et al., 2012; CaraDonna et al., 2014). Species as diverse as plants,
arthropods, birds and fish have experienced recent range contractions and expansions (Chen et al., 2011). However, distributional
Jill Anderson was a finalist for the 2015 New Phytologist Tansley Medal for
excellence in plant science, which recognises an outstanding contribution to
research in plant science by an individual in the early stages of their career; see
the Editorial by Lennon & Dolan, 210: 5
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shifts do not always occur in the predicted direction of higher
elevations or poleward latitudes (VanDerWal et al., 2013; Rapacciuolo et al., 2014). Additionally, the ranges of some species are
contracting on both cooler and warmer edges, as evinced by narrower
latitudinal distributions of seedlings than adult trees in contemporary landscapes (Zhu et al., 2012). Many species will not be able to
disperse fast enough to track rapidly changing climates (Loarie et al.,
2009), and extensive habitat fragmentation will obstruct migration
(Kremer et al., 2012). Adaptive evolution, gene flow and phenotypic
plasticity could buffer populations from climate change (Nicotra
et al., 2010; Gonzalez et al., 2013; Carlson et al., 2014).
High fecundity, large population sizes, broad geographic
distributions, spatially extensive dispersal, plasticity and rapid
generation times could enable population persistence (Aitken et al.,
2008; Alsos et al., 2012). A burgeoning literature explores ecoevolution in the context of climate change, the genetic basis of
climatic adaptation, and conservation in a changing world
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(Gienapp et al., 2008; Hoffmann & Sgro, 2011; Shaw & Etterson,
2012; Aitken & Whitlock, 2013; Alberto et al., 2013; Franks et al.,
2014). Yet we lack a comprehensive analysis of how changing
climates influence fitness in natural populations. If climate change
diminishes fitness, it could reduce the adaptive and migratory
potential of populations. As shifting range dynamics have been
discussed in depth (Valladares et al., 2014), my objectives are to
evaluate shifting fitness landscapes in native plant populations in
the core portions of their ranges, to discuss methods that could
improve the predictive power of climate change experiments and to
examine the evolutionary significance of novel selective regimes.
Mid-elevation
common garden
B
A
Fitness
82 Review
II. Fitness landscapes
Climate change decouples agents of selection
Natural populations evolve in response to complex suites of abiotic
and biotic conditions. Climatic factors such as temperature and
precipitation shape evolution (Kim & Donohue, 2013), influence
population growth rates (Dalgleish et al., 2011) and govern species
distributions (Chen et al., 2011). Plants also adapt locally to
variation in nonclimatic factors, including herbivores (Garrido
et al., 2012), pollinators (Boberg et al., 2014), mycorrhizal fungi
(Johnson et al., 2010), edaphic conditions (Gould et al., 2014) and
photoperiod (Friedman & Willis, 2013).
Human activities are simultaneously modifying multiple abiotic
and biotic agents of selection, and decoupling linked cues including
photoperiod and temperature that trigger phenological transitions
(Bradshaw & Holzapfel, 2008), resulting in growing discrepancies
between current and optimal phenotypes (Etterson, 2004). By altering
selection on genetically correlated traits (Etterson & Shaw, 2001),
climate change could depress fitness (Kingsolver et al., 2013) and
cause widespread local maladaptation in the short term (Fig. 1)
(Wilczek et al., 2014). Even species that migrate rapidly will encounter
biotic and abiotic conditions in their expanded ranges to which they
are not currently adapted (Brown & Vellend, 2014). The question
remains whether adaptation can keep pace with rapid climate change
(Gonzalez et al., 2013) or whether declining fitness could lead to
extinction of local populations (Valladares et al., 2014).
Individual plant performance links demography and evolution:
fitness components and vital rates include germination success,
survival, flowering success and fecundity (Morris et al., 2008). If
climate change reduces the average fitness of individuals, population
growth rates may decline (Clark et al., 2012), leading to lower effective
population sizes. Contracting populations are susceptible to demographic stochasticity, loss of genetic diversity and adaptive potential,
and further reductions in fitness from inbreeding depression (Bijlsma
& Loeschcke, 2012; Gossmann et al., 2012). Importantly, even if the
proportion of seeds and pollen that disperse out of a local population
remains constant, fewer seeds and pollen grains will emigrate from
shrinking populations. Simulations demonstrate that low abundance
can inhibit emigration (Nabel et al., 2013). Small populations attract
fewer pollinators (Duffy et al., 2013), reducing plant fecundity and
the extent of gene flow via pollen. Long-distance dispersal is typically
considered to be rare (Nathan, 2006), and could become even less
frequent if climate change decreases seed production. Reductions in
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Contemporary climate
Future climate
Elevation of origin (m)
Fig. 1 Climate change could disrupt local adaptation. Climate change exposes
natural populations to novel combinations of climatic and nonclimatic
conditions, which likely causes fitness landscapes to shift. Migrants that
disperse to upslope elevations or poleward latitudes could remain within their
historical climatic niche, but will likely confront nonclimatic factors to which
they are not adapted. Researchers can transplant seeds and seedlings of
genotypes from across the range of a species into common gardens to evaluate
the extent of local adaptation to climate in a forestry approach known as
provenance trials (e.g. Wang et al., 2010). By pairing this approach with
climatic manipulations, researchers can assay fitness not only in current
conditions, but also in response to simulated climate change to test whether
climate change disrupts local adaptation by favoring genotypes that evolved
under warmer and drier conditions. This hypothetical example assesses fitness
as a function of provenance elevation (a proxy for climate) for genotypes
transplanted into a mid-elevation common garden (indicated with a star) in a
species that has populations distributed across a broad elevational gradient.
The full experiment would be conducted simultaneously in multiple common
gardens. In contemporary conditions, genotypes that evolved in climates
similar to that of the common garden have optimal fitness. In simulated future
climates, individuals experience a combination of new climatic conditions plus
historical nonclimatic environments. Global change could depress short-term
fitness because of the decoupling of climatic and nonclimatic agents of
selection (arrow A), favoring genotypes from warmer regions over local
ecotypes (arrow B). This shift would lead to local maladaptation, as genotypes
would no longer occur where they have the greatest fitness. These experiments
can be conducted in gardens across any relevant climatic gradients, including
latitude, longitude and elevation. To generate realistic fitness curves, seeds and
seedlings would be planted with minimal disturbance to the natural
community, and would not be supplemented with water or other resources
after the risk of transplant shock subsides.
fitness caused by climate change could diminish the potential for
populations to migrate to areas with favorable climates, and could
underlie recent observations that distributions are not simply shifting
poleward or upslope (Zhu et al., 2012).
Short-term fitness consequences of climate change
To test the hypothesis that climate change depresses plant fitness in
the short-term, I conducted a phylogenetically controlled metaanalysis of field studies that manipulated one or more climatic
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(a) Binary fitness components
Log odds ratio
3
2
[CO2]:
2 studies
13 species
Passive
warming
Reduced
water
Snow
removal
Infrared
heating
Warming +
drought
9 studies
21 species
5 studies
6 species
5 studies
19 species
5 studies
38 species
2 studies
7 species
1
0
–1
–2
–3
(b) Fecundity fitness components: individual level
Log response ratio
[CO2]:
4
1 study
1 species
Passive
warming
Reduced
water
Infrared
heating
[CO2] +
warming
12 studies
30 species
8 studies
12 species
3 studies
11 species
1 study
1 species
2
0
–2
–4
(c) Fecundity fitness components: population level
[CO2]:
Log response ratio
factors (see Supporting Information Methods S1 for details on
methods, results and diagnostics, and Notes S1–S5 for datasets). The
meta-analysis focused on 157 native plant species in core populations
in 60 studies that quantified fitness for at least one life history stage,
from germination to survival to fecundity. The most recent metaanalysis on this topic suggested that warming may enhance
reproductive success for tundra plants, but did not present viability
data or include studies from other ecosystems (Arft et al., 1999).
Field studies test fitness responses in plants exposed to novel
climates and historical nonclimatic agents of selection; these
experiments more realistically reflect the decoupling of environmental signals that natural populations will confront than do
studies in controlled conditions. Experiments included in the metaanalyses simulated climates projected to occur within the next
century (Methods S1). For many systems, manipulations fall
within the range of current climatic variability, such as 0.32–4.0°C
increase in growing season temperature, or 15–50% reduction in
precipitation. Several studies in Mediterranean climates simulated
historical conditions via supplemental watering, documenting
declines in plant fitness in response to increasing drought frequency
(Matesanz et al., 2009; Pratt & Mooney, 2013).
Three manipulations depressed viability (germination, seedling
establishment, and juvenile and adult survival): warming via
infrared heaters (z = 2.28, P = 0.023), snow removal (z = 2.44,
P = 0.015) and warming plus drought (z = 2.64, P = 0.0084);
however, there was no effect of elevated CO2 concentration,
drought or warming via open top chambers (Fig. 2a). The
fecundity meta-analysis revealed that infrared heaters reduced
individual-level fitness (number of reproductive structures per
individual plant, z = 2.53, P = 0.011, Fig. 2b) and that drought
stress reduced population-level fitness (number of reproductive
structures per unit area, z = 2.01, P = 0.045, Fig. 2c). Infrared
heating lamps mimic climatic projections for many regions over the
next century (Dunne et al., 2003; Pfeifer-Meister et al., 2013). The
key result is that germination and survival are particularly
susceptible to multiple climate change factors, and that studies
focused entirely on fecundity will underestimate fitness consequences of climate change. Similarly, a recent meta-analysis
indicated that intense and frequent floods projected under climate
change reduced survival of riparian plants during intense and
frequent floods projected under climate change (Garssen et al.,
2015). In concert, these results suggest that novel climatic regimes
could depress recruitment even in established populations
(Pe~
nuelas et al., 2004), and that conservation efforts should be
aimed at increasing viability. Future studies should aim to quantify
vital rates across multiple life history stages to project population
growth under various climate scenarios.
Experiments in the meta-analysis occurred within natural
communities: changes in fitness resulted from direct and indirect
effects of altered climates. Indirect effects of global change on
species interactions have profound consequences for eco-evolutionary dynamics (Lau et al., 2014). For example, drought-adapted
soil microbial communities attenuated reductions in fecundity in
response to drought in Brassica rapa (Lau & Lennon, 2012). By
contrast, drought stress increased floral herbivory on Hypericum
perforatum, depressing fecundity (Fox et al., 1999). Direct and
Tansley insight
2
1
3 studies
3 species
Passive
warming
Reduced
water
Infrared
heating
5 studies
8 species
2 studies
3 species
1 study
7 species
0
–1
–2
–3
Fig. 2 Results of two separate meta-analyses examining the fitness
consequences of climatic manipulations under field conditions for native
plant species. I initially screened titles and abstracts of 546 papers, of which
28 studies (92 species total) contained suitable data for binary fitness
components (germination, seedling establishment, juvenile survival and
adult survival; Table S1a within Supporting Information Methods S1) and 37
studies (86 species total) contained data on reproductive components of
fitness (Table S1b within Methods S1). Manipulations included reduced
water availability (generally via rainout shelters), passive warming (typically
controlled via open-top chambers), active warming (infrared heaters), snow
removal, elevated [CO2], and warming + reduced water availability. In
snow-dominated regions (high elevation and high latitude), warming
winters reduce snowpack, and warming springs cause snow to melt early
(Hewitson et al., 2014); snow removal efficiently simulates these changing
dynamics (Anderson & Gezon, 2015). Effect sizes are reported as the natural
log of odds ratios for binary fitness components (a) and natural log of
response ratios for continuous fecundity variables (b, c) in treatment relative
to control groups. Values < 0 indicate that fitness was lower under simulated
climate change (treatment) than contemporary conditions (control) in the
field. Symbols represent mean effect sizes and bars are 95% confidence
intervals. (a) Meta-analysis of binary fitness components showed that snow
removal, infrared heating lamps, and warming plus drought depressed
germination success, seedling establishment, and juvenile and adult survival.
(b, c) Fecundity data were available at the level of the individual plant (e.g.
number of flowers, fruits or seeds per individual) for 55 records (species by
study combinations). For the remaining 40 records, fecundity data were
presented on a population level, either per unit area (e.g. number of seeds or
seed biomass per m2) or per plot (e.g. fecundity per experimental block). The
fecundity meta-analysis revealed a significant interaction (P = 0.0015)
between climatic factor and the level of the data (individual or population).
(b) Infrared heating lamps depressed fecundity, but other climatic
manipulations had no overall effect on flower, fruit or seed production on
individual plants. (c) Drought stressed reduced population-level fecundity.
Population data integrate across survival and fecundity, and provide a more
nuanced perspective on population-level consequences of specific climatic
manipulations.
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indirect effects can be either positive or negative, and remain to be
examined explicitly in most systems. Intense precipitation events
have been linked to expansion of woody plants into semi-arid
ecosystems (Kulmatiski & Beard, 2013), and shrubs have
encroached into alpine, tundra, grassland and savannah habitats
(Eldridge et al., 2011; Formica et al., 2014). Climate change could
induce temporal or spatial mismatches with pollinators or other
mutualists (Gordo & Sanz, 2005), and increased prevalence of
herbivory or disease (de Sassi & Tylianakis, 2012) beyond what is
seen in the spatiotemporal scale of climate change experiments.
Nonanalog climates will likely reshape biotic interactions.
Climatic experiments have been concentrated in alpine, arctic,
polar and temperate regions. Species in tropical ecosystems have a
much more restricted climatic tolerance (Kingsolver et al., 2013) and
lower climatic plasticity, yet there is a dearth of climate-change
studies of tropical plant species (Cavaleri et al., 2015). I found no
studies assessing plant fitness in tropical climate change experiments,
even though species with restricted climatic tolerances and limited
distributions could be particularly vulnerable to changing climates.
Field experiments mimic abrupt changes in climate and extreme
events that are projected to increase in frequency (Hansen et al.,
2012; Reyer et al., 2013); however, they might not capture
responses to gradually changing climates. Nevertheless, these
manipulations are relevant to population dynamics in an increasingly variable climate. In a study of vital rates in 36 plant and animal
species, Morris et al. (2008) found that increased interannual
variability in survival and reproduction depressed long-term
population growth, especially for short-lived species. Even if the
climate returns to baseline conditions following perturbation,
extreme events could reduce long-term population growth (but see
Koons et al., 2009). Finally, short-term manipulations can reflect
longer-term responses of natural communities to climate change
(Harte et al., 2015).
fitness consequences of global change (Shaw & Etterson, 2012;
Kim & Donohue, 2013). The provenance trial approach (Fig. 1)
often reveals that fitness declines with increasing climatic distance
between the source population and the experimental garden (Wang
et al., 2010; Wilczek et al., 2014). However, nonclimatic agents of
selection vary spatially and distort inferences about adaptation to
climate change. Combining transplant experiments with climatic
manipulations increases realism and predictive power (PfeiferMeister et al., 2013), enabling researchers to address the implications of climate change for fitness, adaptation and selection in local
populations, and the performance of (transplanted) migrants in
contemporary and simulated future climates. Studies designed to
estimate genetic variance in fitness under various climates could
examine the adaptive potential of populations (Shaw & Shaw,
2014). Evolutionary field studies can test whether climate change
will outpace adaptation (Wilczek et al., 2014), and dissect the
factors that constrain migration (Brown & Vellend, 2014).
Few published field studies simultaneously manipulate multiple
global change factors (but see Matesanz et al., 2009). Multifactorial
studies impose treatments that more closely resemble climate
change scenarios than single factor studies (Beier et al., 2012).
Additionally, regression-based manipulations enable researchers to
examine fitness across multiple levels of climatic factors to achieve a
more precise estimate of how climate affects fitness (Marchin et al.,
2014). Researchers have begun to simulate extreme events,
exposing experimental individuals to fluctuations in the severity
of warming or drought stress (Jentsch et al., 2007). Furthermore,
by recreating historical climates in the field through manipulations
such as supplemental precipitation (Matesanz et al., 2009), studies
could illuminate the extent to which climate change has already
altered eco-evolutionary dynamics. Results of these studies will
highlight when intervention, such as assisted migration/gene flow
(Aitken & Whitlock, 2013), is needed to conserve species.
Plant fitness through time
IV. Evolutionary consequences
Longitudinal studies that assess vital rates in relation to temporal
variation in climate (Clark et al., 2011) can identify responses to
gradually changing climates. Such studies have documented droughtinduced mortality in adult trees over the past century (Bigler et al.,
2007), and found that increasingly prevalent water stress diminishes
juvenile recruitment (Pe~
nuelas et al., 2004). Plant populations could
be particularly susceptible in regions where drought frequency and
intensity are projected to increase. Furthermore, Willis et al. (2008)
found that species that did not adjust their flowering phenology to
changing climates declined in abundance from the 1850s to the
2000s. Such studies require a long time horizon, historical data or
archived seeds (Franks et al., 2008). Funding cycles might not
support the lengthy periods of data collection required to detect
longitudinal trends. Field experiments increase our ability to identify
species and regions vulnerable to climate change.
If natural populations do not have sufficient genetic variation to adapt
to changing local conditions or to a new habitat in a shifted
geographic range, the average fitness of populations could decline
rapidly, depressing emigration rates and increasing extinction risk. If
climate change-mediated selection drives genetically correlated traits
in antagonistic directions, evolutionary response could be negligible
or even maladaptive (Etterson & Shaw, 2001), and adaptive
evolution could lag far behind global change (Wilczek et al., 2014).
Adaptational lag could be especially pronounced for species with
small effective population sizes subject to abruptly changing
conditions (Gonzalez et al., 2013), which are likely to occur more
frequently under increased climatic variability (Hansen et al., 2012).
If reductions in fitness coincide with reductions in genetic variance in
fitness, climate change could exacerbate adaptational lags.
Adaptation and plasticity could counteract the negative shortterm effects of global change. Phenotypic plasticity may enable
populations to persist in situ or establish in new habitats (Chevin
et al., 2013; Anderson & Gezon, 2015), and increased climatic
variation could selectively favor plasticity (Nicotra et al., 2010).
Micro-environmental variation within sites could also buffer local
III. Recommendations for future studies
Transplanting propagules into sites that mirror climatic projections
(e.g. lower elevations) could provide insight into the long-term
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populations from immediate fitness reductions (De Frenne et al.,
2013). If selection is strong and genetic constraints minimal,
adaptive evolution could track climate change in species that
maintain high genetic variation and effective population sizes
(Franks et al., 2014; Gould et al., 2014; Ravenscroft et al., 2014).
For example, Thompson et al. (2013) demonstrated an adaptive
reduction in winter freezing tolerance of wild thyme populations in
response to warming from the 1970s to 2010. Gene flow could
promote adaptation to novel suites of environments if alleles
adapted to elevated temperatures, drought, reduced snowpack or
other conditions associated with climate change become introgressed into locally adapted populations in upslope or poleward
locations (Aitken & Whitlock, 2013). If natural populations
rapidly adapt to novel climates, global change models might
overestimate extinction risks and generate unreliable future
distribution maps.
V. Conclusions
Climate change has already altered selection on traits in natural
populations. Novel suites of climatic and nonclimatic conditions
may reduce viability and fecundity components of fitness, and
hinder the adaptive and migratory potential of local populations.
Species that cannot keep pace with environmental change risk
extinction (Willis et al., 2008). However, some plants are capable
of rapid adaptation to novel climates (Franks et al., 2007; Nevo
et al., 2012; Thompson et al., 2013) and some populations could
adjust plastically (Anderson & Gezon, 2015). Future studies
should combine data on fitness under climate change scenarios
with estimates of the spatial extent of seed and pollen dispersal.
Emerging modeling techniques can incorporate population
dynamics and plasticity into global change models to forecast
extinction risks (Fordham et al., 2012; Valladares et al., 2014).
Ultimately, population persistence could be greatest for those
species capable of tracking shifting adaptive landscapes via a
combination of migration of propagules, gene flow, adaptation and
plasticity.
Acknowledgements
I thank Thomas Pendergast and Monica Geber for discussion and
comments on a previous version, Craig Osenberg for advice on
meta-analysis, and three anonymous reviewers for critiques.
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Supporting Information
Tansley insight
Review 87
Methods S1 Methodological details, statistical models, diagnostics
and publications underlying the meta-analyses.
Notes S1 Full data file for meta-analysis of binary components of
fitness; this file can be opened with a text editor program.
Notes S2 Reduced data file for meta-analysis of binary components
of fitness; this file can be opened with a text editor.
Notes S3 Newick phylogeny file for meta-analysis of binary
components of fitness; this file can be opened with a text editor.
Notes S4 Data file for meta-analysis of fecundity components of
fitness; this file can be opened with a text editor.
Notes S5 Newick phylogeny file for meta-analysis of fecundity
components of fitness; this file can be opened with a text editor.
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