Download Intraspecific genetic variation and species coexistence in plant

Downloaded from http://rsbl.royalsocietypublishing.org/ on May 14, 2017
Community ecology
rsbl.royalsocietypublishing.org
Intraspecific genetic variation and species
coexistence in plant communities
Bodil K. Ehlers1, Christian F. Damgaard1 and Fabien Laroche2,3,4
1
Review
Cite this article: Ehlers BK, Damgaard CF,
Laroche F. 2016 Intraspecific genetic variation
and species coexistence in plant communities.
Biol. Lett. 12: 20150853.
http://dx.doi.org/10.1098/rsbl.2015.0853
Received: 8 October 2015
Accepted: 4 January 2016
Subject Areas:
ecology, evolution
Keywords:
adaptive traits, plant – plant interactions,
competition, facilitation
Author for correspondence:
Bodil K. Ehlers
e-mail: [email protected]
Electronic supplementary material is available
at http://dx.doi.org/10.1098/rsbl.2015.0853 or
via http://rsbl.royalsocietypublishing.org.
Department of Bioscience, Aarhus University, Vejlsøvej 25, Silkeborg 8600, Denmark
CEFE UMR 5175, CNRS-Université de Montpellier-Université Paul Valéry Montpellier-EPHE,
1919 route de Mende, Montpellier 34293, France
3
IRSTEA, U.R. Ecosystèmes Forestiers, Domaine des Barres, Nogent-sur-Vernisson 45290, France
4
Sveriges Lantbruksuniversitet, Ekologicentrum, Ulls väg 16, Ultuna, Uppsala, Sweden
2
Many studies report that intraspecific genetic variation in plants can affect community composition and coexistence. However, less is known about which traits
are responsible and the mechanisms by which variation in these traits affect the
associated community. Focusing on plant–plant interactions, we review empirical studies exemplifying how intraspecific genetic variation in functional traits
impacts plant coexistence. Intraspecific variation in chemical and architectural
traits promotes species coexistence, by both increasing habitat heterogeneity
and altering competitive hierarchies. Decomposing species interactions into
interactions between genotypes shows that genotype genotype interactions
are often intransitive. The outcome of plant–plant interactions varies with
local adaptation to the environment and with dominant neighbour genotypes,
and some plants can recognize the genetic identity of neighbour plants if they
have a common history of coexistence. Taken together, this reveals a very
dynamic nature of coexistence. We outline how more traits mediating plant–
plant interactions may be identified, and how future studies could use
population genetic surveys of genotype distribution in nature and methods
from trait-based ecology to better quantify the impact of intraspecific genetic
variation on plant coexistence.
1. Introduction
The question of what maintains species coexistence is central to ecology and evolution. Numerous studies document that intraspecific genetic variation in plants
affects both ecological structure and species diversity of communities at different
trophic levels (arthropods, soil fungi and epiphytes [1–3]). However, intraspecific
genetic variation in plants can also affect community structure and coexistence
at the same trophic level. A recent meta-analysis [4] found that the impact of
intraspecific genetic variation in plants on the associated plant communities
depends on whether the estimates of genetic diversity depict neutral or nonneutral variation, with a positive relation between genetic diversity and species
diversity for non-neutral genetic variation. Recent reviews [5,6] also stress that
the effect of genetic variation on ecological interactions depends on the genetic
variation that underlies adaptive phenotypic variation. However, so far little
emphasis has been given to documenting which adaptive traits specifically
impact plant–plant interaction, and the mechanisms by which these traits affect
plant coexistence. Here, to fill that gap, we review studies explicitly focusing on
the effects of intraspecific genetic variation in known phenotypic traits, and
when possible emphasize the mechanism by which variation in these traits affects
coexistence with other plant species.
First, we briefly summarize the theory for coexistence mechanisms. Given
the vast literature on this topic, we do not review the theory comprehensively
but rather we sketch the major mechanisms promoting coexistence and how
they can be affected by intraspecific genetic variation. Second, we review
& 2016 The Author(s) Published by the Royal Society. All rights reserved.
Downloaded from http://rsbl.royalsocietypublishing.org/ on May 14, 2017
2. Plant species coexistence: insight from theory
5
2
6
3
7
1
4
Figure 1. Niche variation hypothesis. Axes represent niche axes (amount of
resources, climatic factors, etc.). Continuous shapes: fundamental niche of a
species with low (black) or high (grey) genotype richness. Dotted shapes:
fundamental niche of individual genotypes. Niche expansion arises via
increased variation among individual genotypes rather than via increased
niche breadth within individual genotypes.
act as benefactors for inferior resource competitors [13].
Thus asymmetric facilitation maintains species diversity
when the superior competitors reduce the mortality rate of
inferior competitors [13,14]. Facilitation can act as a stabilizing
mechanism—especially in harsh environments—because the
overall increased species abundance around benefactors
favours rare species by reducing their risk of stochastic extinction [15]. However, facilitation may indirectly decrease local
coexistence when plant density increases around the benefactor,
causing the beneficiary species to experience more intense
competition from other species [16].
(a) Adding intraspecific genetic variation to coexistence
theory
Intraspecific genetic variation can impact species coexistence in
several ways. First, genotypic diversity of a species determines
its fundamental niche, and a species’ fundamental niche can
be understood as the union of niches of the different genotypes
([17], figure 1). Decomposing species interactions into interactions between genotypes illustrates how the outcome of an
interaction may depend on the genotype identity rather than
species identity (figure 2). Because genetic variation for resource
optima allows species to diversify into different niches, coexistence can occur if at least one genotype of each species can be
stably maintained locally. Variation in competitive ability
among genotypes can lead to intransitive competitive hierarchies at a local scale allowing coexistence of competitors at
larger scales [18,19]. Second, genetic variation can affect species
interactions differently depending on the ecological role that
individual plant species play in the community. For numerically
dominant or for so-called foundation species (i.e. species instrumental in shaping their habitat), the impact of intraspecific
genetic variation may affect a larger number of subordinate
species. Genotype diversity in dominant species generates
spatial heterogeneity [18], which can promote species coexistence at a larger spatial scale by favouring different plant
species in different micro-environments. Lastly, presence of
intraspecific genetic variation is a prerequisite for evolutionary
adaptation. Local adaptation increases species coexistence if
competitively inferior species benefit most from this adaptation,
Biol. Lett. 12: 20150853
The ecological success of plant species and the means by
which they coexist in a community can be seen as ultimately
determined by four main processes: speciation, migration,
demographic stochasticity and ecological differences between
species [7]. Various coexistence paradigms have been proposed
that attribute different weights to these four pillars. The neutral
theory of biodiversity [8] suggests that migration, stochasticity
and speciation can explain species abundance distributions in
speciose communities without need of considering ecological
differences among species. However, patterns predicted by
the neutral theory could also readily emerge with mechanisms
involving ecological differences [9]. Therefore, understanding
the causes of coexistence cannot be based on inferences of mechanisms from patterns only and should also directly address the
interaction mechanisms among species.
A paradigm well-suited for such direct inquiry is the
stabilizing–equalizing framework introduced by Chesson
[10]. This framework focuses on ecological differences among
competing species and how these differences enable coexistence—or not. Here, species interactions are conceptually
understood by their amount of overlap in a multidimensional
niche space made up of resources, natural enemies, time and
space. When species show large niche overlap, their coexistence
is challenged by the competitive exclusion principle, which
predicts the extinction of the inferior competitor. The mechanisms promoting coexistence between species that overlap in
their fundamental niche can be divided between equalizing
and stabilizing mechanisms [10]. Equalizing mechanisms are
those that reduce the mean fitness differences between interacting species, thereby delaying a competitively deterministic
winner and promoting long-term coexistence. Stabilizing mechanisms are those that favour species when they become rare and
increase intraspecific competition relative to interspecific competition. Niche differences will act as a stabilizing mechanism
between two competing species because species will ultimately
limit their own population growth more than others’.
When species interactions involve more than two plant
species, intransitive competitive hierarchies promote coexistence even when species show large overlap in their niche
requirements [11,12]. Intransitive dynamics can be understood
as the well-known rock–scissors–paper game, where species
A outcompetes species B, species B outcompetes species C,
and species C outcompetes species A. Such dynamics act as
a stabilizing mechanism as they will disfavour the most
common species by favouring rapid population growth of
the species that outcompetes it.
To date, most theory on plant species coexistence focuses
exclusively on competitive interactions. However, a few theoretical studies also include facilitative interactions [13–16].
These models predict that, under some conditions, facilitation
can maintain species-rich communities. For instance, facilitation
increases coexistence, even for species competing for the same
limiting resource, when superior resource competitors also
2
rsbl.royalsocietypublishing.org
empirical studies documenting how genetic variation in
plants for known adaptive traits impacts their interaction
and coexistence with other plant species. Finally, we outline
how future empirical research can add more insights into the
role that intraspecific genetic variation plays in determining
among-species coexistence.
Downloaded from http://rsbl.royalsocietypublishing.org/ on May 14, 2017
(a)
(b)
3
sp. 1
sp. 1
rsbl.royalsocietypublishing.org
g. 1X
g. 1X
sp. 2
sion
g. 2X
lu
exc
g. 1Y
coex.
ion
clus
ex
coex.
g. 1Y
sp. 1
g. 1X
g. 2Y
sp. 2
g. 2Y
Figure 2. Decomposing competition between two species (species 1 and 2) to the genotypic scale. Abiotic niche space is represented as a two-dimensional space.
Each species has two genotypes, X and Y, and genotypes have different fundamental niches (dotted shapes). (a) Grey zone represents fundamental niche overlap too
prominent to allow stable coexistence. Overlaps in white are narrow enough to allow coexistence. (b) Coexistence depends on fitness of individual genotypes. 1X is
assumed to be always fitter than 2X. Upper graph: 1Y excludes 2Y, leading to exclusion of species 2. Lower graph: 2Y excludes 1Y, leading to stable coexistence of
both species.
thereby equalizing fitness differences between species. However, local adaptation can decrease coexistence if adaptation
increases the fitness of the competitively superior species [6].
3. Impact of intraspecific genetic variation on
plant species coexistence: insight from
empirical studies
on associated plants [26]. The coyote bush, Baccharis, is a dominant species in the coastal dunes of California. It has a genetic
dimorphism for plant architecture, with co-occurrence of
plants having either a prostrate or an erect morphology. Species
richness and plant cover differ between the two morphs, with
the erect form supporting more species [27]. Differences in light
availability, and soil properties underneath these two morphs
were suggested to explain the difference in their ability to support colonizing species.
(a) Intraspecific genetic variation in dominant species
as a source of micro-environmental variation
(b) Intraspecific genetic variation can promote both
stabilizing and equalizing coexistence mechanisms
Genetic variation for the production of chemical compounds
that are leached to the local environment by some foundation
species can affect species coexistence by creating small-scale
differences in local environments among different chemical
types. For instance, genetic variation in Scots pine for chemical
diversity of terpenes correlates with species richness and composition of the vegetation under the pine trees [20,21]. Genetic
variation in monoterpene composition of the essential oils produced by the dominant wild thyme also impacts species
richness and composition of the local vegetation around
thyme plants [22]. The possible mechanisms for how variation
in chemical phenotypes impacts the community of associated
species include variation in the allelopathic effects of the different chemicals combined with different sensitivity to these
allelochemicals of associated plant species [23,24] and, as
found for soil under Populus, via differences in litter composition and soil nutrition under chemically different tree
genotypes [25].
Phenotypic variation in plant architecture also impacts
species coexistence. For instance, intraspecific variation in the
cushion morphology among nurse plants differs in their effects
Experiments performed at Sheffield University by Booth and
Grime have contributed extensively to unravelling how
intraspecific genetic variation impacts species coexistence in
grassland vegetation. They created 36 experimental communities, each consisting of the same number of species but
varying in the level of genotypic diversity within species.
After five growing seasons, more species were retained in the
communities with multiple genotypes [28]. Pairwise interactions
between two abundant species from these communities (a grass
and a sedge) showed that the outcome varied with genetic identity of the plant neighbour and that the competitively dominant
genotype varied between high and low fertility environments
[29]. In a different set of experimental communities but using
the same site and species and a subset of the genotypes, it was
again found that relative performance of genotypes varied
with environment (G E) and genetic identity of competitor
(G G). Moreover, increasing genotypic diversity decreased
the overall intensity of interspecific competition. Thus, in genetically diverse communities both G E and G G interactions
played a role in maintaining species coexistence by equalizing
fitness differences between interacting species [30].
Biol. Lett. 12: 20150853
sion
lu
exc
Downloaded from http://rsbl.royalsocietypublishing.org/ on May 14, 2017
Mounting empirical evidence shows that some plant species
can recognize the identity of a neighbour plant and alter their
root growth depending on either previous encounter with
heterospecifics or genetic relatedness of conspecifics [35]. Root
exudates may be one mechanism by which plants recognize
their neighbour. In Deschampsia caespitosa plants, growing
with root exudates from unrelated individuals increased their
root length compared with plants growing with root exudates
from genetically related individuals. Moreover, plants grown
with root exudates from unrelated individuals originating
from the same populations grew longer roots than those
grown with root exudates from individuals originating from
a different population [36]. This suggests that response to a
plant neighbour depends on the coevolutionary history of
the interacting genotypes rather than fixed species-specific
responses [37]. Genetically similar plants are expected to also
be similar in resource requirements, and competition with kin
should therefore be stronger than with non-kin. However,
some species exhibit a kind of kin-facilitation where plants
reduce their competitive effects towards kin relative to unrelated
conspecifics [38,39]. With kin-facilitation, individuals perform
better when interacting with kin compared with a non-related
conspecific. Depending on how frequently kin interactions
(d) Local adaptation impacts species coexistence
Populations can adapt evolutionarily to their local environment on a time scale equivalent to that of ecological
processes [40], thereby affecting present day species interactions. For instance, facilitative plant–plant interactions
prevail in stressful habitats, where the presence of a benefactor
plant ameliorates local growing conditions, allowing the
establishment and growth of other plants. However, whether
or not an environment is perceived as stressful depends on
the level of local adaptation in the beneficiary plants. The facilitative effect of the shrub Gymnocarpos decander varied between
two ecotypes of the annual grass Brachypodium distachyon. One
ecotype was adapted to the arid study site, whereas the other
was not. Unlike the locally adapted ecotype, the maladapted
ecotype could only survive and reproduce under the canopy
of the benefactor shrub [41]. A similar result was found for
Plantago ecotypes that varied in their adaptation to serpentine
soil [42]. The importance of facilitation for beneficiary plants
varies with their level of adaptation to the local abiotic conditions, and importantly facilitation may account for the
coexistence with maladapted species.
In the species-rich Mediterranean garrigue, the aromatic
shrub wild thyme (Thymus vulgaris) is a dominant component
of the vegetation. Wild thyme has a genetic polymorphism for
the production of dominant monoterpene in its essential oil.
Some monoterpenes are of a phenolic type and others of a
non-phenolic type. The competitively strong perennial grass
Bromus erectus shows adaptation to growing with local nonphenolic thymes, but not with its phenolic type [43]. In a
large vegetation survey [22] comprising several communities
dominated by thyme that varied in chemical phenotype, the
presence and abundance of B. erectus was significantly lower
around phenolic thyme, i.e. the chemical type that it was not
adapted to. Moreover, plant species richness around phenolic
thyme was relatively higher than around non-phenolic thyme.
The lower abundance of brome—a strong competitor—
around phenolic thyme plants may be one reason why species
richness, particularly small annual herbs, is higher. The differences in adaptation of brome to thyme chemical types may
explain why brome abundance is only reduced in phenolic
thyme sites and suggests that a ‘competitor release’ effect
varies among thyme plants producing different monoterpenes.
Variation in adaptation to metal-rich soils also creates
variation in competitive and facilitative interactions among
metal-accumulating plants and their surrounding neighbours. Some plants are known to extract metals from soil
(i.e. phytoextraction). In metal-rich soils, these metal-accumulating plants can facilitate the presence of non-metal-tolerant
species by locally alleviating the toxic effects of metals by
reducing their concentration in the soil [44]. However,
metal-accumulating plants also accumulate these metals in
non-contaminated soils (where the concentration is much
lower) and via leaching create a higher concentration of
metals in the soil around these plants than away from them.
For instance, the soil around the selenium-accumulating
plants Astragalus bisulcatus and Stanleya pinnata is enriched in
4
Biol. Lett. 12: 20150853
(c) Plant recognition impacts coexistence
occur, kin-facilitation may switch the relative intensity of intraversus interspecific competition, thereby altering predictions
for coexistence. For plant species with limited dispersal,
the nearest neighbour is often a genetic relative, making the
distinction between kin and non-kin interactions relevant.
rsbl.royalsocietypublishing.org
Lankau and co-workers also found that genetic variation
impacts species coexistence. However, rather than equalizing
fitness differences among competing species, they found
evidence for a stabilizing mechanism driven by intraspecific
genetic variation in communities containing Brassica nigra.
Brassica nigra show a genetic variation for the concentrations
of sinigrin in leaves. Sinigrin acts as an allelochemical against
heterospecific species. Brassica genotypes of high sinigrin concentration are strong competitors against heterospecific, but
poor against conspecific genotypes. The reason for the negative impact of sinigrin on heterospecific plants can, at least
partly, be explained by the toxic effects of sinigrin on mycorrhizal fungi in the soil. Most heterospecifics benefit from
mycorrhiza association, whereas Brassica is non-mycorrhizal
and hence not affected by reduced mycorrhizae in the soil
[31]. High concentration genotypes are favoured when
B. nigra is rare and most often competes against heterospecifics but are disfavoured as B. nigra becomes more
abundant and increasingly competes against conspecifics.
This negative genetic correlation between intra- and interspecific competition creates cyclic dynamics across
generations, maintaining both species coexistence and genetic
variation for sinigrin concentration [32].
Clark and co-workers studied fecundity and growth
response to environmental variation over a decade in more
than 25 000 individuals belonging to 33 co-occurring tree
species in 11 forest stands in North America. Overall, the
different species responded similarly to environmental variation, suggesting that they were in strong competition.
However, neighbour trees of the same species responded
more similarly to local environmental variation than heterospecific neighbour trees. This suggests that, at the local scale,
intraspecific competition was stronger than interspecific
competition. Intraspecific genetic variation was not assessed,
but the phenotypic variation in environmental response
within and among species was spatially structured such that
it contributed to stabilizing species coexistence [33,34].
Downloaded from http://rsbl.royalsocietypublishing.org/ on May 14, 2017
The studies reviewed here show examples of how intraspecific
genetic variation impacts species coexistence on a local scale
via both stabilizing and equalizing mechanisms. Intraspecific
genetic variation could also impact coexistence at larger spatial
scale when the variation in dominant species increases
environmental heterogeneity, allowing more species to
co-occur by favouring different species in different microenvironments. Maintenance of genetic variation then becomes
essential for the long-term positive effects on plant species
richness. If intraspecific genetic variation in foundation
species is eventually lost due to intraspecific competition
between genetic variants [48], or other processes reducing
genetic variation in foundation species, the positive effects on
species coexistence may be short lived.
Because plants are sessile, genetic variation within a given
species can be conceptually viewed as a form of environmental
variation for neighbour plants. One route to further understand how variation in traits impacts coexistence is, then, to
explore how these traits affect local abiotic (such as concentration and composition of phytochemicals in soil, nutrient
and light availability) and biotic (abundance and composition of competitors and mutualist partners) environments
(i.e. their interspecific indirect genetic effects [49]). Viewing
intraspecific genetic variation as a source of environmental
variation emphasizes the dynamic nature of plant coexistence
as neighbour species may—depending on their own genetic
variation—progressively adapt to dominant neighbour
genotypes (or the environment they create).
Although many studies document genotype-dependent outcomes of plant–plant interactions, fewer have identified the trait
mediating these interactions. Depending on the species,
genome-wide molecular polymorphisms might be available
but this still requires the hard task of assessing what polymorphism underlies the relevant phenotype variation. Though
advancement in eco-genomics makes this gradually more feasible [50], we believe an approach starting from a candidate
ecological trait and revealing its genetic basis by quantitative
trait locus (QTL) analysis or classical quantitative genetics
designs still remains a fruitful strategy. This review found
mostly examples showing that genetic variation in chemical
and architectural traits influence plant–plant interactions
(electronic supplementary material, table). These traits may
therefore be promising candidates for adaptive traits mediating
Competing interests. We declare we have no competing interests.
5
Biol. Lett. 12: 20150853
4. Gaining further insight into plant species
coexistence
genotype-specific interactions. Plants produce a vast amount of
secondary compounds with known phytochemical properties
(e.g. terpenoids, glucosinolates, phenolic acids and flavonoids).
Variation in production of these compounds can be studied
using gas chromatography–mass spectroscopy and combined
with studies estimating how heritable this variation is. Experimental studies using genotypes that vary in the production of
phytochemicals can inform how variation in these compounds
impacts plant interaction: do they contribute to increase habitat
heterogeneity—thereby producing more niche space? Can
phytotoxic effects alter local competition hierarchies? Or are
negative frequency-dependent interactions—as demonstrated
for sinigrin production in Brassica—common and generally
instrumental for species coexistence?
Future studies on genotype-dependent interactions should
include information from surveys of the natural frequency and
spatial distribution of genotypes. This can determine how
likely it is that a given species encounter the different genotypes that show trait variation and allow design of realistic
experiments that manipulate genotype identity and frequency
to match those found in natural plant communities. This is
important as a mismatch between genetic and environmental
variation in experimental studies may artificially boost the
importance of either one. Moreover, it allows results from
controlled experiments to be convincingly validated by
‘in natura’ observations of covariation in species richness and
composition associated with specific genotypes.
By stressing the importance of specific traits for species
coexistence, our approach echoes ‘trait-based’ community
ecology [51], which in line with classic niche theory, envisions a strict competitive hierarchy among phenotypes in a
given environment. Species coexistence is ultimately
explained by fine-scale environmental heterogeneity that
allows different phenotypes belonging to different species
to be maintained. However, most of the adaptive traits discussed in this review are not the functional traits typically
used to quantify community structure (e.g. specific leaf
area, plant height, root depth, drought and shade tolerance).
The plant traits more typically studied in functional ecology
could be further candidates for traits for which variation
within species could impact among-species coexistence.
The studies reviewed here illustrate that competition is
often intransitive instead of hierarchical and emphasize the
importance of both facilitation and genotype-dependent interactions—aspects that extend the classic trait-based ecology.
Including these aspects may significantly improve the predictive
power of trait-based community ecology. Reciprocally, studies
on genotype-dependent interactions demonstrate effects on coexistence at a very local scale but the relative impact of such
interactions on large-scale coexistence needs to be explored.
Although non-neutral processes shaped by intraspecific variation may determine local-scale coexistence, it is still not
known if these local processes will scale up to the level of
meta-community, or if stochastic processes override their importance. Future studies could apply methods of trait-based
community ecology (like partitioning of trait variance within
and among communities [52]) to the adaptive traits identified
and use the spatial genotypic composition as environmental gradient. This may help quantify how much variation in community
structure is explained by intraspecific variation and if variation in
specific traits has similar effects across communities.
rsbl.royalsocietypublishing.org
selenium, and the selenium concentration in plants growing in
the vicinity of these hyper-accumulators is increased by
10–20-fold relative to the concentration in plants grown away
from these plants [45]. Plants that are adapted to this element
are facilitated by the selenium-accumulators as the increased
concentration of selenium in their plant tissue reduces herbivory, whereas plants that are not adapted to selenium show
impaired growth on soil near selenium-accumulators, possibly
due to the negative allelopathic effects of increased selenium
[46]. Hyper-accumulators may show genetic variation for
metal accumulation [47] and non-accumulators show genetic
variation for metal tolerance. Hence, the plant interactions
between accumulators and non-accumulators can shift from
negative to positive depending on the level of adaptation and
whether or not the soil is contaminated with metals.
Downloaded from http://rsbl.royalsocietypublishing.org/ on May 14, 2017
Funding. The work was supported by a research grant from the Villum
Foundation (VKR 021800) to B.K.E.
Acknowledgements. The authors thank A. Tack, S. Bailey, T. Bataillon,
References
1.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15. Xiao S, Michalet R, Wang G, Chen SY. 2009 The
interplay between species’ positive and negative
interactions shapes the community biomass–
species richness relationship. Oikos 118, 1343–
1348. (doi:10.1111/j.1600-0706.2009.17588.x)
16. Bulleri JF, Bruno JF, Silliman BR, Stachowicz JJ. 2015
Facilitation and the niche: implications for
coexistence, range shift and ecosystem functioning.
Func. Ecol. 30, 70 –78. (doi:10.1111/1365-2435.
12528)
17. van Valen L. 1965 Morphological variation and
the width of the ecological niche. Am. Nat. 99,
377 –390. (doi:10.1086/282379)
18. Vellend M, Geber MA. 2005 Connections between
species diversity and genetic diversity. Ecol. Lett. 8,
767 –781. (doi:10.1111/j.1461-0248.2005.00775.x)
19. Taylor DR, Aarssen LW. 1990 Complex competitive
relationships among genotypes of three perennial
grasses: implications for coexistence. Am. Nat. 136,
305 –327. (doi:10.1086/285100)
20. Iason GR, Lennon JJ, Pakeman RJ, Thoss V, Beaton
JK, Sim DA, Elston DA. 2005 Does chemical
composition of individual Scots pine trees
determine the biodiversity of their associated
ground vegetation? Ecol. Lett. 8, 364 –369. (doi:10.
1111/j.1461-0248.2005.00732.x)
21. Pakeman JR, Beaton JB, Thoss V, Lennon JJ,
Campbell DC, White D, Iason RG. 2006 The
extended phenotype of Scots pine Pinus sylvestris
structures the understorey assemblage. Ecography
29, 451– 457. (doi:10.1111/j.2006.0906-7590.
04617.x)
22. Ehlers BK, Charpentier A, Grøndahl E. 2014 An
allelopathic plant facilitates species richness in the
Mediterranean garrigue. J. Ecol. 102, 176 –185.
(doi:10.1111/1365-2745.12171)
23. Jensen C, Ehlers B. 2010 Genetic variation for
sensitivity to a thyme monoterpene in associated
plant species. Oecologia 162, 1017–1025. (doi:10.
1007/s00442-009-1501-z)
24. Linhart YB, Gauthier P, Keefover-Ring K, Thompson
JD. 2015 Variable phytotoxic effects of Thymus
vulgaris terpenes on associated species. Int. J. Plant
Sci. 176, 20 –30. (doi:10.1086/678772)
25. Madritch M, Donaldson J, Lindroth R. 2006 Genetic
identity of Populus tremuloides litter influences
decomposition and nutrient release in a mixed
forest stand. Ecosystems 9, 528–537. (doi:10.1007/
s10021-006-0008-2)
26. Schöb C, Armas C, Guler M, Prieto I, Pugnaire FI.
2013 Variability in functional traits mediates plant
interactions along stress gradients. J. Ecol. 101,
753 –762. (doi:10.1111/1365-2745.12062)
27. Crutsinger GM, Strauss SY, Rudgers JA. 2010 Genetic
variation within a dominant shrub species
28.
29.
30.
31.
32.
33.
34.
35.
36.
37.
38.
39.
40.
determines plant species colonization in a coastal
dune ecosystem. Ecology 91, 1237 –1243. (doi:10.
1890/09-0613.1)
Booth RE, Grime JP. 2003 Effects of genetic
impoverishment on plant community diversity.
J. Ecol. 91, 721 –730. (doi:10.1046/j.1365-2745.
2003.00804.x)
Fridley JD, Grime JP, Bilton M. 2007 Genetic identity
of interacting neighbours mediates plant responses
to competition and environmental variation in a
species rich grassland. J. Ecol. 95, 908– 915.
(doi:10.1111/j.1365-2745.2007.01256.x)
Fridley JD, Grime P. 2010 Community and ecosystem
effects of intraspecifc genetic diversity in grassland
microcosms of varying species diversity. Ecology 91,
2272– 2283. (doi:10.1890/09-1240.1)
Lankau RA, Wheeler E, Bennett AE, Strauss SY. 2011
Plant –soil feedbacks contribute to an intransitive
competitive network that promotes both genetic
and species diversity. J. Ecol. 99, 176–185. (doi:10.
1111/j.1365-2745.2010.01736.x)
Lankau RA, Strauss SY. 2007 Mutual feedbacks
maintain both genetic and species diversity in a
plant community. Science 317, 1561–1563.
(doi:10.1126/science.1147455)
Clark JS. 2010 Individuals and the variation
needed for high species diversity in forest trees.
Science 327, 1129– 1132. (doi:10.1126/science.
1183506)
Clark JS, Wolosin M, Dietze M, Ibanez I, LaDeau S,
Welsh M, Kloeppel B. 2007 Tree growth inference
and prediction from diameter censuses and ring
widths. Ecol. Appl. 17, 1942 –1953. (doi:10.1890/
06-1039.1)
Chen BJW, During HJ, Anten NPR. 2012 Detect thy
neighbor: identity recognition at the root level in
plants. Plant Sci. 195, 157–167. (doi:10.1016/j.
plantsci.2012.07.006)
Semchenko M, Saar S, Lepik A. 2014 Plant root
exudates mediate neighbour recognition and trigger
complex behavioural changes. New Phytol. 204,
631–637. (doi:10.1111/nph.12930)
Thorpe AS, Aschehoug ET, Atwater DZ, Callaway RM.
2011 Interaction among plants and evolution.
J. Ecol. 99, 729 –740. (doi:10.1111/j.1365-2745.
2011.01802.x)
Murphy GP, Dudley SA. 2009 Kin recognition;
competition and cooperation in Impatiens
(Balsaminaceae). Am. J. Bot. 96, 1990–1996.
(doi:10.3732/ajb.0900006)
Biernaskie JM. 2010 Evidence for competition and
cooperation among climbing plants. Proc. R. Soc. B
278, 1989– 1996. (doi:10.1098/rspb.2010.1771)
Fussmann GF, Loreau M, Abrams PA. 2007 Ecoevolutionary dynamics of communities and
Biol. Lett. 12: 20150853
2.
Crutsinger GM, Collins MD, Fordyce JA, Gompert Z,
Nice CC, Sanders NJ. 2006 Plant genotypic diversity
predicts community structure and governs an
ecosystem process. Science 313, 966 –968. (doi:10.
1126/science.1128326)
Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ,
Lonsdorf EV, Whitham TG, Hart SC. 2008 Plant –
soil –microorganism interactions: heritable
relationship between plant genotype and associated
soil microorganisms. Ecology 89, 773–781. (doi:10.
1890/07-0337.1)
Davies C, Ellis CJ, Iason GR, Ennos RA. 2014
Genotypic variation in a foundation tree (Populus
tremula L.) explains community structure of
associated epiphytes. Biol. Lett. 10, 20140190.
(doi:10.1098/rsbl.2014.0190)
Whitlock R. 2014 Relationships between adaptive
and neutral genetic diversity and ecological
structure and functioning: a meta-analysis. J. Ecol.
102, 857–872. (doi:10.1111/1365-2745.12240)
Hughes AR, Inouye BD, Johnson MT, Underwood N,
Vellend M. 2008 Ecological consequences of genetic
diversity. Ecol. Lett. 11, 609– 623. (doi:10.1111/j.
1461-0248.2008.01179.x)
Lankau RA. 2011 Rapid evolutionary change and
the coexistence of species. Annu. Rev. Ecol. Evol.
Syst. 42, 335 –354. (doi:10.1146/annurev-ecolsys102710-145100)
Vellend M. 2010 Conceptual synthesis in community
ecology. Q. Rev. Biol. 85, 183–206. (doi:10.1086/
652373)
Hubbel SP. 2001 The unified neutral theory of
biodiversity and biogeography. Princeton, NJ:
Princeton University Press.
Chave J, Muller-Landau HC, Levin SA. 2002
Comparing classical community models: theoretical
consequences for patterns of diversity. Am. Nat.
159, 1–23. (doi:10.1086/324112)
Chesson P. 2000 Mechanisms of maintenance of
species diversity. Annu. Rev. Ecol. Syst. 31,
343–366. (doi:10.1146/annurev.ecolsys.31.1.343)
Laird RA, Schamp BS. 2006 Competitive
intransitivity promotes species coexistence. Am. Nat.
168, 182–193. (doi:10.1086/506259)
Allesina S, Levine JM. 2011 A competitive network
theory of species diversity. Proc. Natl Acad. Sci. USA
108, 5638 –5642. (doi:10.1073/pnas.1014428108)
Gross K. 2008 Positive interactions among
competitors can produce species-rich communities.
Ecol. Lett. 11, 929–936. (doi:10.1111/j.1461-0248.
2008.01204.x)
Vellend M. 2008 Effects of diversity on diversity:
consequences of competition and facilitation. Oikos
117, 1075 –1085. (doi:10.1111/j.0030-1299.2008.
16698.x)
6
rsbl.royalsocietypublishing.org
J. Stachowicz and two anonymous reviewers for valuable feedback
on earlier drafts.
Downloaded from http://rsbl.royalsocietypublishing.org/ on May 14, 2017
42.
43.
49. Shuster SM, Lonsdorf EV, Wimp GM, Bailey JK,
Whitham TG. 2006 Community heritability measures
the evolutionary consequences of indirect genetic
effects on community structure. Evolution 60, 991 –
1003. (doi:10.1111/j.0014-3820.2006.tb01177.x)
50. Snoeren TAL, De Jong PW, Dicke M. 2007
Ecogenomic approach to the role of herbivoreinduced plant volatiles in community ecology.
J. Ecol. 95, 17 –26. (doi:10.1111/j.1365-2745.2006.
01183.x)
51. McGill BJ, Enquis BJ, Weiher E, Westoby M. 2006
Rebuilding community ecology from functional
traits. TREE 21, 178 –185. (doi:10.1016/j.tree.2006.
02.002)
52. Violle C, Enquist BJ, McGill BJ, Jiang L, Albert CH,
Hulshof C, Jung V, Messier J. 2012 The return of the
variance: intraspecific variability in community
ecology. TREE 27, 244–252. (doi:10.1016/j.tree.
2011.11.014)
7
Biol. Lett. 12: 20150853
44.
45. El Mehdawi AF, Quinn CF, Pilon-Smits EA. 2011
Effects of selenium hyperaccumulation on plant –
plant interactions: evidence for elemental
allelopathy? New Phytol. 191, 120–131. (doi:10.
1111/j.1469-8137.2011.03670.x)
46. El Mehdawi AF, Quinn CF, Pilon-Smits EAH. 2011
Selenium hyperaccumulators facilitate seleniumtolerant neighbors via phytoenrichment and
reduced herbivory. Curr. Biol. 21, 1440–1449.
(doi:10.1016/j.cub.2011.07.033)
47. Taylor SI, Macnair MR. 2006 Within and between
population variation for zinc and nickel
accumulation in two species of Thlaspi
(Brassicaceae). New Phytol. 169, 505–513. (doi:10.
1111/j.1469-8137.2005.01625.x)
48. Abbott JM, Stachowicz JJ. 2016 The relative
importance of trait vs. genetic differentiation for the
outcome of interaction among plant genotypes.
Ecology (in press).
rsbl.royalsocietypublishing.org
41.
ecosystems. Func. Ecol. 21, 465 –477. (doi:10.1111/
j.1365-2435.2007.01275.x)
Liancourt P, Tielbörger K. 2011 Ecotypic
differentiation determines the outcome of positive
interactions in a dryland annual plant species. Plant
Ecol. Evol. Syst. 13, 259 –264. (doi:10.1016/j.ppees.
2011.07.003)
Espeland EK, Rice KJ. 2007 Faciliatation across stress
gradients: the importance of local adaptation.
Ecology 88, 2404–2409. (doi:10.1890/06-1217.1)
Ehlers BK, Thompson J. 2004 Do co-occurring plant
species adapt to one another? The response of
Bromus erectus to the presence of different Thymus
vulgaris chemotypes. Oecologia 141, 511 –518.
(doi:10.1007/s00442-004-1663-7)
Koelbener A, Ramseier D, Suter M. 2008
Competition alters plant species response to nickel
and zinc. Plant Soil 303, 241 –251. (doi:10.1007/
s11104-007-9503-2)