WEWeb EcologyWEWeb Ecol.1399-1183Copernicus PublicationsGöttingen, Germany10.5194/we-17-51-2017The ecology of subindividual variability in plants: patterns, processes, and
prospectsHerreraCarlos M.herrera@ebd.csic.eshttps://orcid.org/0000-0003-2452-3888Department of Evolutionary Ecology, Estación Biológica de
Doñana, CSIC, Avda. Americo Vespucio 26, Isla de La Cartuja,
41092 Seville, SpainCarlos M. Herrera (herrera@ebd.csic.es)8December201717251648November20175December2017This work is licensed under the Creative Commons Attribution 4.0 International License. To view a copy of this licence, visit https://creativecommons.org/licenses/by/4.0/This article is available from https://we.copernicus.org/articles/17/51/2017/we-17-51-2017.htmlThe full text article is available as a PDF file from https://we.copernicus.org/articles/17/51/2017/we-17-51-2017.pdf
Diversification of ecology into subdisciplines that run from macroecology to
landscape, community, and population ecology largely reflects its
specialization on different segments of the spatial gradient over which
recognizable ecological patterns and processes occur. In all these cases, the
elemental units involved in the patterns and processes of interest to
ecologists are individuals from the same or different species. No distinct
flavor of ecology has yet emerged that focuses on patterns and processes
revolving around the lowermost end of the spatial gradient, which in the case
of plants corresponds to the within-individual domain. Intraindividual
heterogeneity in organ traits, however, is quantitatively important and has
multiple consequences for plant individuals, populations, and communities,
and for animal consumers as well. This paper first provides an overview of
current knowledge on plant traits that vary subindividually, the magnitude of
subindividual variation, and its spatial patterning. Examples will then be
presented on the consequences of subindividual variation for plants and
animal consumers at individual, population, or community levels. Finally, the
recently emerging links between genetics, epigenetics, subindividual
variation, and population ecology will be illustrated using results on
variation in seed size, a functional plant trait playing an important role in
plant population dynamics. Further observational and experimental studies are
needed which link ecological and phenotypic measurements of plants to their
epigenetic and genetic characteristics, in order to understand the three-way
relationships between subindividual variability, genetic features, and
epigenetic mosaicism. Another proposed line of inquiry should focus on
evaluating whether subindividual epigenetic mosaics eventually translate into
epigenetically heterogeneous progeny, thus contributing to the maintenance of
population and community functional diversity.
Introduction
Following its formal definition by Ernst Haeckel as the science that studies
the relationships between organisms and the environment, ecology steadily
experienced a process of diversification that eventually led to the
appearance of a series of distinct subdisciplines. To a considerable extent,
the historical diversification of ecology into subdisciplines reflects a
progressive specialization on different segments of the broad gradient of
spatial scales on which pertinent ecological patterns and processes can be
identified and studied. At the high end of the spatial-scale gradient, the
mission of macroecology is to describe and understand the causes and
consequences of ecological processes on very large spatial scales (say,
106–107 m) such as, e.g., biome differences in productivity or
planetary-scale patterns in biodiversity. At progressively smaller spatial
scales, landscape ecology focuses, among other things, on the ecology of
metapopulations and metacommunities at the regional level
(104–105 m), while community ecology and population ecology are
mostly concerned with the functioning at local scales (101–103 m)
of multi-species assemblages or single-species populations, respectively.
Common to all these subdisciplines is the fact that, irrespective of spatial
scale, the elemental units that build up the patterns and participate in the
processes of interest to ecologists are individuals from the same (population
ecology) or different species (rest of the subdisciplines). No coherent
subdiscipline or distinct flavor of ecology has so far emerged whose focus is
placed on the ecological significance of patterns and processes that take
place around the lowermost end (100–101 m) of the macroscopic
spatial gradient envisaged above. This segment of the spatial scale would
roughly correspond to within-individual variation, and its predominant
neglect is well exemplified by the unambiguous subtitle, “From individuals
to ecosystems”, on the cover of one of the most authoritative ecology
textbooks (Begon et al., 2006). In recent years, however, increasing evidence
has shown that such very small-scale, intraindividual variation may have
manifold ecological consequences for the population and community ecology of
both animals and plants (Herrera et al., 2015; Alonso et al., 2017;
Arceo-Gómez et al., 2017, and references therein).
In most animals, subindividual variation of ecological relevance is mostly
sequential in nature, as it generally arises from ontogenetic and/or seasonal
changes in the organismal features of individuals. Sequentiality of
subindividual variation means that, at different moments or ontogenetic
stages in an animal's adult life, a given individual will exhibit variable
states of functional or structural features (e.g., behavior, coloration,
digestive organ size; Piersma and Lindström, 1997; Delhey and Kempenaers,
2006; Stamps et al., 2012). Plants differ from animals with respect to
within-individual variation in a most profound way. As noted long ago by
Lloyd (1984, p. 379), “a plant produces a considerable number of structures
of one kind [and] this simple feature can explain a major difference in the
variation patterns exhibited by plants and animals.” Although plants and
animals share the sequential (seasonal or ontogenetic) component of
subindividual variation (e.g., contrasting leaf size and shape between
juveniles and adults in some heterophyllous plants), vascular plants stand
uniquely apart because of the existence of a strong simultaneous
component of subindividual variation that arises naturally from their modular
construction.
The modular construction of plant bodies by continual organogenesis and
reiterated production of homologous, functionally equivalent structures is a
truly quintessential, ancestral feature of the body plan of vascular plants
(Herrera, 2009). The ecological consequences of plant modularity have been
addressed from three main angles. First, following White's (1979) pioneering
treatment of plant individuals as metapopulations of repeated modules,
demographically inspired investigations have dealt with the consequences of
differential growth and survival of modular subunits, particularly in
long-lived species characterized by extensive clonal proliferation. Second,
there are physiologically inspired studies that have examined the effects of
modularity on small-scale spatial patterns of within-plant distribution of
water, photosynthates and other products (Marshall, 1996; Price et al.,
1996), and the resulting compartmentalization of plant bodies into a series
of relatively independent “integrated physiological units” (Watson, 1986;
Orians and Jones, 2001). The third perspective on plant modularity, and the
one this paper will be exclusively concerned with, emphasizes the appearance
of a distinctive source of phenotypic variance, namely the within-plant or
subindividual component. An inevitable consequence of a multiplicity of
modules being simultaneously borne by individual plants is a certain
variability in the characteristics of the copies of the same organ (leaves,
flowers, fruits, seeds) produced in different modules of the same individual.
As first suggested by Suomela and Ayres (1994) and documented at length by
Herrera (2009), within-individual variability in organ traits is an emergent
property of plant individuals brought about by their modular construction
through reiteration of elemental subunits (metamers) and the associated
repetition of homologous structures that perform the same function (leaves,
flowers, fruits, seeds).
In this paper, I will first provide a concise review of current knowledge on
the nature of plant traits that vary subindividually, the magnitude of
subindividual variation relative to variation between individuals, and its
spatial patterning. Next I will highlight some of the ecological consequences
of subindividual variation for plants and their animal consumers at the
individual, population, and community levels. All the preceding aspects were
thoroughly reviewed by Herrera (2009); thus, whenever possible I will
consider here preferentially those findings obtained by more recent
investigations that complement, expand, or corroborate the conclusions of
that earlier review. Finally, I will consider the little explored connections
between subindividual variation, population ecology, genetics, and
epigenetics, which will be illustrated by results of recent investigations on
the epigenetic correlates of seed mass variation.
Traits and magnitude of subindividual variation
Studies on subindividual variation in plants have traditionally tended to
focus on the relatively infrequent instances of discontinuous variation
involving morphologically or functionally distinct variants of reiterated
homologous structures, typically leaves (heterophylly), fruits (heterocarpy),
and seeds (heteromorphism) (see Wells and Pigliucci, 2000, Imbert, 2002, and
Matilla et al., 2005, for reviews). Examples include the coexistence of
prickly and nonprickly leaves in the same crown of individual trees (Herrera
and Bazaga, 2013) or the simultaneous production by individual plants of
distinct seed morphs with contrasting dispersal ability (Imbert, 2002).
Ecologists interested in the evolution of plant gender and mating systems
have long scrutinized the causes and consequences of the production of
distinct floral sex morphs by the same individual (Barrett, 1998). In
contrast, continuous within-plant variation in quantitative traits of
homologous organs remains comparatively unexplored from an ecological
perspective despite being a quintessential plant feature (Herrera, 2009). I
will focus on this ubiquitous form of subindividual variation for the rest of
this paper.
Continuous subindividual variation is the rule for virtually every
conceivable continuous trait of any reiterated homologous structure (Herrera,
2009). Importantly, many of the traits that vary within individual plants are
known for their functional nature; i.e., they have potential effects on the
fitness of individuals or the environment (Pérez-Harguindeguy et al.,
2013). These include simple traits like leaf length, fruit size, or seed
mass, but also less apparent features such as concentration of nutrients and
secondary compounds in leaves, length of seed dormancy, or sugar
concentration in floral nectar or the pulp of berries. Recent studies have
continued furnishing examples of relatively cryptic continuous traits that,
when properly sampled, exhibit substantial subindividual variation. These
include, among other things, leaf stomatal traits (Herrera et al., 2015),
leaf nutrients (Wetzel et al., 2016), sugar composition of floral nectar
(Herrera et al., 2006; Canto et al., 2007; Zywiec et al., 2012), distance
between anthers and stigma (Dai et al., 2016; Arceo-Gómez et al., 2017),
tannin content of seeds (Shimada et al., 2015), fruit shape (Larrinaga and
Guitián, 2016), and global DNA cytosine methylation of the genome (Alonso
et al., 2017).
Subindividual variability in functional traits, however, is not ecologically
interesting in itself, since even tightly controlled industrial processes
fail to produce perfect copies of simple items due to minor stochastic
fluctuations in the production equipment. It is intuitive to postulate that
the greater the subindividual variability in a given trait, the more likely
it will be that a such variation may have some ecological relevance. One
method for assessing the extent of subindividual variation is to gauge it by
comparison with the extent of variation between individual means for the same
trait. This can be achieved, for instance, by estimating the proportion of
population-wide variance contributed by subindividual variation, or in other
words, by partitioning the population-wide variance of the trait of interest
into its within- and among-individual components (Herrera et al., 2015).
Estimates of the within-individual variance component (VARwithin
hereafter) for a variety of flower, fruit, leaf, and seed traits are shown in
Fig. 1a. There was considerable spread of VARwithin within each
organ type, which reflects variation across species and also between
different traits for the same organ (Herrera et al., 2015). Despite the broad
spread, however, there was a clear trend for VARwithin to exceed
the variance between individual means for all organs except flowers. This
implies that most population-wide variance in functional organ traits occurs
within the restricted spatial domain of individual plants; that organ trait
value distributions for different individuals tend to overlap extensively
(Fig. 1b); and that neglecting subindividual variation to focus exclusively
on individual means is bound to miss a large fraction of the range of
functional variation represented in plant populations. Insofar as the organ
traits concerned possess some ecological relevance, e.g., by influencing some
important ecological process or playing a role in the appearance of
ecological patterns, the preceding implications call for a consideration of
the ecological significance of subindividual variation. In the following
sections I will present a non-exhaustive review of ecological patterns and
processes, either established or putative, that are potentially under the
influence of subindividual variation in functional traits of reiterated
organs.
(a) Within-plant variability for a variety of continuously
varying flower, fruit, leaf, and seed traits, as estimated by the proportion of population-wide
variance in the trait that is accounted for by differences between organs
produced by the same plant. The horizontal dashed line denotes the level
above which subindividual variance is greater than variance between
individual means. Each dot corresponds to an independent estimate (N=95,
25, 23, and 84 estimates for flower, fruit, leaf, and seed traits,
respectively). Redrawn from Fig. 3.2 in Herrera (2009).
(b) Schematic comparison of hypothetical extremes of high (top) vs.
low (bottom) levels of subindividual variation in a continuously varying
organ trait for a given set of invariant individual means. Curves represent
within-plant frequency distributions of trait values for three different
individuals (color coded). Individual means are the same in the upper and
lower graphs.
Spatial patterns: microgradients and environmental grain
Subindividual variation in organ trait values is often related to some
spatial reference system, such as height above ground or compass direction,
and in these cases such relationships will give rise to distinct
microspatial gradients. Long known examples include predictable
relationships between height above ground and the size, photosynthetic
capacity, specific area, and nitrogen and phosphorus content of leaves in
individual trees (Ellsworth and Reich, 1993; Casella and Ceulemans, 2002;
Osada et al., 2014). For example, leaves from upper positions in the crown
consistently have a lower water content than those from lower positions in
the deciduous tree Prunus mahaleb (Fig. 2). In other cases, within-crown gradients in leaf
composition and water content are related to compass orientation (Le Roux et
al., 1999; Perica, 2001; Herrera, 2009). In Olea europaea trees, functional leaf traits
related to light interception and photosynthetic performance vary according
to orientation and position within the crown (Escribano-Rocafort et al.,
2016, 2017). Spatial microgradients will also arise when organ trait values
vary regularly along nodal positions of linear supporting structures such as
branches or inflorescences. Traits that vary predictably along these linear
plant axes include anatomical features and chemical composition of leaves,
nutritional characteristics of seeds, and structural and functional floral
traits (Bennett et al., 2003; Guitián et al., 2004; Young et al., 2010;
Austen et al., 2015; Herrera et al., 2015). For example, in the perennial
herb Helleborus foetidus, leaf stomatal density increases, and mean stomatal size decreases,
from basal to distal nodal positions along vegetative ramets (Herrera et
al., 2015).
Vertical gradients in leaf water content within the crowns of
Prunus mahaleb trees. Each line connects mean values for water
content in leaves from the top and bottom positions of an individual (N=25 trees). Based on data from Alonso (1997, and unpublished).
Irrespective of the specific details on how it is spatially organized within
individual plants or plant parts, subindividual variation in functional
traits of organs will have the crucial ecological consequence of altering
environmental grain size for ecologically relevant parameters. It will
promote “fine-grainedness”, or small-scale “granularity”, of the
environment relative to a hypothetical situation where within-plant
homogeneity prevailed, as proposed schematically in Fig. 3. Very low and very
high VARwithin values for a trait will correspond by definition to
situations where organs resemble strongly and weakly, respectively, other
organs in the same plant with regard to that trait (i.e., high and low
intraclass correlations, respectively). Strong trait correlations between
organs in the same plant will produce coarser grained environments than weak
correlations, and the corresponding variograms will also differ widely
(Fig. 3).
Schematic representation of two extreme situations in which most
population-wide variance in a given quantitative trait of a reiterated organ
occurs between (left, %VARwithin≅0) and within (right,
%VARwithin≅100) individual plants. Trait values are denoted by
variable color intensities. Hypothetical maps of spatially autocorrelated
variation in trait values and its associated variogram plots are shown for
the two situations. The variogram function for lag distance h, γ(h), is the average squared difference of values separated by h. Blue
areas denote the interval of distances between points within which trait
values are spatially autocorrelated.
Frequency distributions of within-plant coefficients of variation
(standard deviation/mean, a measurement of variability) for four functional
leaf traits in a sample of N=138 individuals of the perennial herb
Helleborus foetidus. Data from Herrera et al. (2015).
Individual-centered patterns: variability as an individual property
From an ecological perspective, an important aspect of subindividual
variation in functional organ traits is that conspecific individuals in a
population differ in the degree of internal heterogeneity. In other words,
subindividual variability should be considered in itself as an individual
property, because “individual plants not only have their characteristic
means, but their characteristic standard deviations” as well (Haldane, 1957,
p. 312; see also Haldane, 1959, Roy, 1959, Paxman, 1956, and Suomela and
Ayres, 1994, for further antecedents to this view). This general principle
was named the “Haldane-Roy conjecture” by Herrera (2009), where data for a
broad variety of functional organ traits from many species were gathered
which unequivocally supported the generality of the phenomenon in plant
populations. In addition, a within-plant variability continuum was shown to
occur in most species, with populations generally comprising phenotypically
constant to highly variable individuals, which ultimately means that the
component of population-wide variance in an organ trait caused by
within-plant variation is not distributed equally among individuals. Recent
studies have corroborated and expanded these conclusions by showing that
conspecific individuals differ in variability of leaf functional traits
(Herrera et al., 2015), seed mass (Herrera et al., 2014; Shimada et al.,
2015), fruit size (Sobral et al., 2013), seed tannin content (Shimada et al.,
2015), and stigma–anther separation of flowers (Dai et al., 2016;
Arceo-Gómez et al., 2017). In a large sample of plants of the perennial
herb Helleborus foetidus, the within-plant coefficient of variation
(within-plant standard deviation/individual mean) for stomatal index,
stomatal density, stomatal length, and specific leaf area all ranged widely
between plants (Fig. 4), thus denoting considerable individual variation in
the magnitude of subindividual functional heterogeneity.
Ecological effects of subindividual variation
Internal heterogeneity of individual plants in functional features of
reiterated organs is apt to have a variety of ecological consequences. The
importance of the effects will simultaneously depend on the magnitude of the
variability, the latter's ultimate impact on spatial “graininess” of trait
values, and the nature of the ecological process(es) in which the organs and
the traits are involved. As the examples provided in the following sections
will show, ecological effects of subindividual variation can take place not
only at the individual level, but also at the plant population and plant
community levels. In other words, subindividual plant variation possesses
some explanatory value for the interpretation of ecological patterns that
occur in populations and communities. A thorough review of the ecological
consequences of subindividual plant variation was presented for the first
time by Herrera (2009). Here I will put forward a brief selection of examples
with the aim of illustrating the variety of mechanisms whereby within-plant
heterogeneity in organ traits can impinge in complex ways on individual
fecundity and performance, population dynamics, plant community
functionality, and the behavior of animal consumers. Just for convenience of
presentation, these effects will be split into two classes, namely those
predominantly related to the plants themselves (e.g., effects on individual
fecundity or population dynamics) and those impinging on the animals that
exploit plant-based resources, such as, e.g., pollinators, seed predators, or
herbivores. Drawing such a demarcation line between the two categories of
effects, however, will often prove difficult in real-world scenarios, where
effects on plants and animals will be in many instances closely intertwined
(Herrera, 2009).
Simplified path diagram quantifying the effects of within-plant
variability in four functional leaf traits on the fecundity (number of seeds
produced) of Helleborus foetidus plants (N=138). Arrow widths
are proportional to the magnitude of path coefficients (shown beside arrows;
**P<0.01). Continuous and discontinuous lines reflect direct and
inverse relationships, respectively. Based on data from Herrera et al. (2015)
and M. Medrano and C. M. Herrera (unpublished).
Geographical distribution of Helleborus foetidus
populations sampled by Herrera et al. (2015) in the Sierra de Cazorla,
southeastern Spain (left), and relationship across populations between mean
individual fecundity (seeds produced per plant, log transformed) and mean
within-individual variability (coefficient of variation, CV) of specific leaf
area (SLA; right). Based on data from Herrera et al. (2015) and M. Medrano
and C. M. Herrera (unpublished).
Effects on plant individuals, populations, and communities
Within-plant variation in leaf, flower, fruit, or seed characteristics can
affect diverse aspects of plant vegetative (e.g., growth rate, carbon
assimilation) and reproductive (e.g., fecundity) performance of individuals,
as shown by significant correlations across plants between subindividual
variability and diverse measurements of individual performance (Herrera,
2009). In the case of leaves, it has been frequently suggested that
subindividual variation in some of their functional traits may be
advantageous to individuals by enhancing whole-plant photosynthetic
performance and optimizing the exploitation of environmental variation (e.g.,
canopy light gradients; Givnish, 1988; Hollinger, 1996; Osada et al., 2014).
For the perennial herb Helleborus foetidus, Herrera et al. (2015)
suggested that variation in size, specific leaf area, and stomatal traits
across leaves borne in different nodal positions along ramets could influence
the water economy and carbon assimilation efficiency of whole plants, and
suggested possible mechanisms in support of this explanation. Indirect
support for their interpretation is provided by the significant relationships
existing across individuals between seed fecundity and within-plant leaf
variability (Fig. 5). The broad differences between individuals in
subindividual variability of stomatal index, stomatal density, stomatal
length, and specific leaf area illustrated in Fig. 4 collectively account for
13 % of the variance in seed fecundity (Fig. 5). The higher the
within-plant variability in stomatal index, stomatal length, and specific
area, and the lower the variability in stomatal density, the higher was the
total number of seeds produced by individual plants, perhaps as a consequence
of improved water economy and/or carbon assimilation. Relationships between
subindividual variability and fecundity can also hold across populations of
the same species, as exemplified by the significant nonlinear relationship
between mean individual fecundity and mean subindividual variability in
specific leaf area across the populations of Helleborus foetidus
sampled by Herrera et al. (2015) (Fig. 6).
Subindividual variability in flower, fruit, and seed traits may also
influence the reproductive success of individuals, as illustrated by
correlations across conspecific individuals between variability and some
measurement of reproductive performance. For example, in plants of the
southern Spanish violet Viola cazorlensis, subindividual variability
in length of floral spur was related to fruit set (Herrera, 2009). In the
tropical tree Ipomoea wolcottiana and the vine Passiflora incarnata, differences between plants in subindividual variability of
anther–stigma separation were correlated with differences in fruit set and
seed mass (Arceo-Gómez et al., 2017; Dai et al., 2017). In European
populations of the bird-dispersed tree Crataegus monogyna, the
magnitude of within-tree variation in fruit size was significantly related to
the number of seeds effectively dispersed (Sobral et al., 2013). Further
examples can be found in Herrera (2009).
Insofar as most organ traits involved in subindividual variation have some
functional implications, variation within individuals will be consequential
for the functional ecology of plant populations and communities. It is
currently acknowledged that individual variation in functional traits
broadens the ecological breadth of species (Sides et al., 2014) and is an
important factor enhancing community-wide functional diversity (Siefert et
al., 2015). In the same way that the incorporation of measurements of
individual differences into trait-based plant ecology has improved our
understanding of the role of trait variation in species distribution and
plant community organization (Violle et al., 2012; Sides et al., 2014), I
contend that the incorporation of subindividual variability into trait-based
ecological studies will help to further sharpen the focus of, and lend
biological realism to, functional ecology investigations. Subindividual
variation will contribute to expanding the range of the biotic and abiotic
resources which can be successfully exploited by single individuals (Herrera,
2009), and its neglect will tend to exaggerate the importance of individual
differences as a source of total population- or community-wide functional
diversity. To date, however, the subindividual component remains virtually
unexplored from the perspective of its contribution to the functional
diversity and trait-based organization of plant communities (Herrera et al.,
2015). In the few studies where leaf trait variances between species, between
individuals within species, and within individuals were quantified
simultaneously for a plant community, the contribution of subindividual
variation to total community-wide variance was sometimes comparable or even
superior to that of individual variation (Auger and Shipley 2013; Kang et
al., 2014).
Effects on animal consumers
In most terrestrial habitats, the aerial parts of modularly constructed
plants provide the major structural scaffold for the establishment and
trophic support of communities of heterotrophic organisms. From the
perspective of animal consumers, therefore, an immediate consequence of
subindividual plant variation in traits of homologous organs will be the
appearance of a very small-scale component in the spatial distribution of
some important resource parameters such as, e.g., concentration of water,
nutrients and secondary compounds in leaves, amount and quality of the
pollinator rewards available in flowers, nutritional quality of fleshy
fruits, or size and defensive features of individual seeds (Herrera et al.,
2006; Canto et al., 2007; Gijbels et al., 2014; Shimada et al., 2015). This
low-level source of variation has two main implications for phytophagous
animals of all sorts. First, since in most instances the size of animal
consumers substantially exceeds the size of the individual plants with which
they interact, animal consumers will have an opportunity to discriminate
among not only individual plants, but also among the multiplicity of
non-identical organs borne by each of them. And second, since individual
plants differ not only in the mean value of organ traits, but also in the
variance as noted earlier, consumer discrimination and choice among
individual plants will also be influenced by individual differences in
variability levels.
Within-plant variation in reiterated structures is generally comparable to or
even greater in magnitude than variation among plants, as noted above.
Therefore, discrimination and selection by animal consumers among organs that
differ in morphological, chemical, or nutritional properties are likely to be
the rule rather than the exception. This will apply equally to situations in
which animals maintain predominantly antagonistic and predominantly
mutualistic
relationships with plants. It is well known, for instance, that after
approaching a plant pollinators eventually visit only a subset of the flowers
available, probing preferentially the most rewarding flowers and skipping the
least rewarding ones (Duffield et al., 1993; Møller, 1995; Harder et al.,
2004). Small-scale flower selection exerted by pollinators can be strong,
with individual foragers rejecting up to 10–25 % of approached flowers
(Heinrich, 1979; Kadmon et al., 1991). Following arrival at a plant,
frugivorous vertebrates also discern and respond to within-plant variation in
fruit features related to energetic reward such as pulp mass or pulp-to-seed
mass ratio (Wheelwright, 1985; Sallabanks, 1993; Palacio et al., 2017).
Likewise, egg-laying females of invertebrate fruit and seed predators
discriminate between the fruits borne by a plant on the basis of their size,
number of enclosed seeds, or other traits potentially influencing the
viability of their progeny (Herrera, 1984; Nalepa and Grissell, 1993).
Similarly, leaf miners, sap feeders, or folivorous insects tend to select
those particular leaves in a plant crown that provide greater nutritional
reward and/or a lower load of toxic or deterrent compounds (Roslin et al.,
2006; Young et al., 2010). In short, animal consumers generally do not treat
individual plants as homogeneous feeding patches, but rather discriminate
between organs borne on the same plant on the basis of differences in
quality.
In addition to influencing the behavioral responses of animal consumers at
the within-plant level, subindividual variation in organ traits will also
impinge on foraging decisions that imply discrimination among plants. This
important effect can be accounted for by the variance-sensitive behavior of
animal consumers, for which within-patch variance in resource quality is
equally or more important than within-patch mean value as a determinant of
patch selection. Behavioral models have long predicted that such
variance-sensitive, or “risk-sensitive”, behaviors should evolve when
animals are regularly confronted with environmental patches that differ in
the uncertainty (variance) of resource quality and fitness returns (Kacelnik
and Bateson, 1996; Smallwood, 1996). One would therefore expect that,
everything else being equal, relative preferences of animal consumers for
individual plants should be inversely related to subindividual variability.
Studies on floral visitors, frugivores, seed predators, and leaf eaters have
provided substantial support for this prediction. For example, when insect
and vertebrate nectarivores are offered a choice between feeding patches with
contrasting variance in food reward (volume or concentration of sugar
solutions), they most often develop variance-averse behaviors which lead them
to prefer the least variable patches (Herrera, 2009; Nakamura and Kudo,
2016). In the fleshy-fruited tree Crataegus monogyna, inverse
relationships linking within-plant variability in fruit and seed mass, on the
one hand, and proportional fruit removal by frugivorous birds and seed
predation by rodents, on the other, have been reported (Sobral et al., 2013,
2014). Likewise, within-plant variances in the mass and tannin content of
seeds in the oak Quercus serrata were significantly related to
between-tree differences in seed removal by rodents (Shimada et al., 2015).
Variable chemical defenses within plants will also have a negative impact on
the performance of insect herbivores and favor the evolution of
variance-driven host selection behaviors (Tenhumberg et al., 2000; Shelton,
2004; Wetzel et al., 2016).
Evolutionary implications of subindividual variation: a canonical
perspective
The ecological processes associated with within-plant variation described
above, particularly those related to the discriminating behavior of animals
toward individual plants, can also have some evolutionary repercussions
(Herrera, 2009). The two most important of these can be easily formulated
using conventional tools from the realm of population genetics, and their
consequences inferred from ordinary concepts of quantitative genetics and
phenotypic selection models: subindividual variability will constrain
responses to selection on individual organ traits, and phenotypic selection
will operate not only on individual means, but also on within-individual
variances.
Simple quantitative genetics considerations reveal that within-plant
variation in a given organ trait will generally act by constraining the
responses to selection by the environment, including animals, on that trait.
Repeatability (r) of any organ trait in a plant population will
approximately equal 1 – VARwithin, and will set an upper-bound
estimate to the trait's broad-sense heritability (H2), or the fraction
of the total phenotypic variance that has a genetic basis, both additive and
nonadditive. Broad-sense heritability, in turn, sets an upper limit to
narrow-sense heritability (h2), a central element in the familiar
breeder's equation Δμ=h2S, where Δμ is the response
to selection across generations and S is the selection differential (see,
e.g., Falconer and MacKay, 1996, and Lynch and Walsh, 1998, for further
details). By setting an upper limit on h2, repeatability of a trait will
thus set an upper limit to the response to selection across generations. With
the predominantly high values of VARwithin that characterize
variation in the majority of organ traits (Fig. 1), repeatabilities for leaf,
fruit, and seed traits will often be low enough to predict low heritabilities
and thus intrinsically small responses to selection.
The most interesting and consequential evolutionary implication of
within-plant variation in organ traits is that it opens the possibility for
animals or the abiotic environment to exert selection on levels of
within-plant variance through some of the mechanisms mentioned earlier.
Selection on subindividual variability can be inferred from some results
reviewed above (e.g., the relationship between leaf variability and
individual fecundity in Helleborus foetidus plants shown in Fig. 5).
More explicit tests, however, can be undertaken by expanding phenotypic
selection models developed for evaluating selection on quantitative traits
(Kingsolver and Pfennig, 2007) to incorporate subindividual variabilities
just as another set of descriptors of a plant's phenotype in addition to
customarily used means. Application of these “variability-aware”, expanded
phenotypic selection models to different plant species, organ traits, and
types of plant–animal interactions has revealed the existence of significant
directional selection on subindividual variability even in cases where
selection on individual means was not evident (Herrera, 2009; Sobral et al.,
2014; Arceo-Gómez et al., 2017; Palacio et al., 2017). Furthermore,
function-valued trait analyses have revealed that the shape of gradients of
variation in flower traits along inflorescences is also subject to phenotypic
selection (Kulbaba et al., 2017).
Phenotypic selection on within-plant variability by biotic or abiotic agents
acquires particular evolutionary relevance in the light of reports showing
that within-plant trait variability has a genetic basis and, therefore, can
respond adaptively to selection. Independent lines of experimental and
correlative evidence point to a genetic basis for subindividual variability.
Classical population genetics experiments have unequivocally shown that
subindividual variabilities of parents and offspring are significantly
correlated for a variety of leaf, flower, and seed traits (Paxman, 1956;
Sakai and Shimamoto, 1965; Seyffert, 1983; Bagchi et al., 1989; Biere, 1991;
Winn, 1996). On the other hand, two recent studies using genetic markers have
found significant heritability for subindividual variability in flower
developmental rates (Kulbaba et al., 2017) and significant associations
across individuals between genetic markers and subindividual leaf trait
variability (Herrera et al., 2015). To assess whether differences between
Helleborus foetidus plants in leaf trait variability were related to
their genetic features, Herrera et al. (2015) looked for statistically
significant associations across plants between amplified fragment length
polymorphism (AFLP) markers and the within-plant coefficients of variation
for each of eight leaf traits. Significant relationships were found between
the magnitude of subindividual variability in leaf traits and up to 11
different AFLP markers. Between 1 and 4 AFLP markers were associated with the
within-plant variability level of each leaf trait. Although genetic
marker–trait associations are unable to provide conclusive proofs of
causality (Platt et al., 2010), these results are clearly compatible with the
hypothesis that differences between H. foetidus plants in
subindividual variability in leaf features might have a causal genetic basis.
Emerging connections: epigenetics and subindividual variation
The evolutionary and ecological implications of within-plant variation in
continuous traits of reiterated structures will ultimately depend on its
underlying causes and maintenance mechanisms. A combination of position along
growth axes, developmental history, short-term responses to the external
environment, and developmental stochasticity has been proposed as a major
proximate cause of subindividual variation, but its mechanistic basis is far
from being well established (Herrera, 2009). Genetic mosaicism
(i.e., within-plant heterogeneity in DNA sequences) caused by the vegetative
propagation within individuals of somatic mutations was once proposed as a
major driver of subindividual heterogeneity in plants (Whitham and
Slobodchikoff, 1981). The rarity of documented instances of genetic mosaicism
in wild plants, however, makes it unlikely that this will provide a universal
mechanism for ubiquitous subindividual variation in plant communities
(O'Connell and Ritland, 2004; Herrera, 2009; Padovan et al., 2013; Ranade et
al., 2015). Nevertheless, genetic
mosaicism is not the only possible mechanism causing stable or metastable
subindividual genomic heterogeneity in plants. One further, hitherto almost
unexplored source of genomic heterogeneity within plants is
epigenetic mosaicism. A handful of studies have shown that the
genomes of homologous organs in the same plant may differ in their patterns
of DNA cytosine methylation despite homogeneity in the DNA sequence (Bitonti
et al., 1996, 2002; Gao et al., 2010; Bian et al., 2013; Spens and
Douhovnikoff, 2016; Ahn et al., 2017). Cytosine methylation is a major
epigenetic mechanism in plants that plays important roles in gene expression
and plant growth and development (Finnegan et al., 2000; Cokus et al., 2008;
Lister et al., 2008), and it is well established that DNA methylation
variants independent of DNA sequences are causally related to individual
differences in continuous traits (Zhang et al., 2013; Cortijo et al., 2014;
Hu et al., 2015; Kooke et al., 2015). Extrapolating from the
between-individual to within-individual domains, the hypothesis has been
recently formulated that subindividual heterogeneity in patterns and extent
of DNA methylation can sometimes account for within-plant variation in organ
traits (Herrera and Bazaga, 2013; Alonso et al., 2017). The few tests of this
hypothesis conducted so far support a relationship between epigenetic
mosaicism and subindividual heterogeneity in both discontinuously and
continuously varying organ traits.
Individual holly trees (Ilex aquifolium) often bear a mixture of
nonprickly and prickly leaves, the latter being produced facultatively as a
plastic response to browsing by mammals (Obeso, 1997). By comparing genomic
DNA methylation profiles in pairs of contiguous prickly and
nonprickly leaves on the same branchlets using a methylation-sensitive
amplified fragment polymorphism (MSAP) method, Herrera and Bazaga (2013)
found that adjacent nonprickly and prickly leaves differed significantly in
their genome-wide patterns of DNA methylation. Methylation differences
between leaf types did not occur randomly across the genome, but affected
predominantly some specific markers whose methylation probability declined
significantly from nonprickly to contiguous prickly leaves. In this case,
therefore, spatial correspondence within tree crowns between epigenotypes and
leaf phenotypes was consistent with the hypothesis of epigenetic mosaicism as
a contributing factor to subindividual variation.
Seeds are one of the most subindividually variable structures in plants, and
in the vast majority of instances the within-plant component of
population-wide variance in seed mass exceeds the variance between
individuals (Fig. 1). The ecological significance of the large variation in
seed mass occurring within crops was emphasized long ago by
Janzen (1977a, b), and largely stems from the manifold implications of seed
mass for population persistence and community dynamics through its pervasive
effects on seed predation, seed dispersal, and seedling emergence and
survival (Harper, 1977). The important ecological effects of seed mass
variation thus confer particular interest to some recent results which link
epigenetic mosaicism with subindividual variation in seed mass. In the
evergreen shrub Lavandula latifolia, analyses of global
DNA cytosine methylation levels
using a HPLC method revealed that leaves from different modules in the same
plant (one “module” = one inflorescence plus its associated set of
subtending leaves) differed in global DNA cytosine methylation (Alonso et
al., 2017). The magnitude of such epigenetic mosaicism was substantial, as
variance in DNA methylation among modules of the same shrub was greater than
variance between individuals. As predicted by the epigenetic mosaicism
hypothesis, subindividual variation in the size and number of seeds produced
per module was significantly related to subindividual variation in
genome-wide DNA cytosine methylation level (Alonso et al., 2017).
Links between epigenetic mechanisms and subindividual variation in seed mass
are probably far more complex than envisaged by the simple epigenetic
mosaicism hypothesis, extending beyond the coordinated variation within
individuals of methylation patterns and seed mass. This possibility was
suggested by correlations across plants of the perennial herb
Helleborus foetidus between DNA methylation transmissibility across
generations and magnitude of subindividual variability in seed size (Herrera
et al., 2014). In this species, individual plants differed in the fidelity
with which DNA methylation patterns were transmitted from adult plants to
descendant pollen. Such individual variation in methylation transmissibility,
which was associated with genetic differences, was also related to
within-plant variance in seed mass: individuals characterized by high
plant-to-pollen transmissibility of DNA methylation patterns was
characterized by low subindividual variance in seed mass, and vice versa
(Herrera et al., 2014).
Synthesis and perspectives
As noted by Herrera (2009, p. 339), “subindividual variation in plants seems
to have succumbed so far to the risk of looking and yet overlooking.” What
is one of the most obvious sources of phenotypic variation in plant
populations has been traditionally neglected, if not explicitly dismissed as
a statistical nuisance, on the misguided understanding that such variation is
the product of the same genotype and thus invisible to natural selection, or
on the unproven implicit assumption that it is devoid of ecological
relevance. Continuous subindividual variation is only rarely considered in
ecology textbooks, and it is not even considered among the levels of
biological diversity contributing to “biodiversity” (Contoli and Luiselli,
2015), an omission that will systematically underestimate the phenetic
component of biodiversity in populations and communities. The preceding
sections have summarized current knowledge on the magnitude, patterns, and
ecological effects of subindividual variation in functional traits of all
major classes of homologous, reiterated structures. Irrespective of the
particular structure considered, whenever subindividual variation has been
placed under the focus of ecological research and its correlates examined in
sufficient detail, it has been found to be quantitatively important and
ecologically significant at the population and community levels.
In addition to an immediate effect on the spatial structure of functional
plant traits by enhancing environmental “fine-grainedness”, the production
by plants of nonidentical homologous structures has a number of more subtle
ecological effects on both the plants themselves and their animal consumers.
On the plant side, effects include broadening the ecological breadth of
individuals and species; enhancing the functional diversity of populations
and communities; improving the exploitation of limiting resources such as
light or nutrients; modifying the outcome of interactions with antagonists
(e.g., herbivores) and mutualists (e.g., pollinators); coping with
environmental uncertainty in biotic and abiotic factors; and enhancing the
exploitation of biotically and abiotically heterogeneous environments through
“division of labor” effects (Herrera, 2009). Furthermore, differences
between conspecific plants in subindividual variability are correlated with
fitness surrogates and seem transgenerationally heritable, which lends
plausibility to the hypothesis that variable levels of subindividual
variability across populations may have been shaped by divergent natural
selection (Herrera et al., 2014). On the side of animal consumers, the main
predicted effect of subindividual variance in features of reiterated plant
structures will be to elicit variance-sensitive foraging behaviors and to
promote selectivity among plant individuals based on local trait variances
rather than, or in addition to, local trait means. In the case of mutualists
such as pollinators or seed dispersers, variance-averse behaviors will result
in selection against the most subindividually variable individuals, whereas
variance aversion by antagonists such as folivores or seed predators will
select for increased subindividual variability (Herrera, 2009). In either
case, in the long run the expected consequence for plants of such directional
selection will be to shape natural patterns of subindividual variation in
plant populations according to some organ-specific trade-off representing a
balance between the reduction promoted by plant–mutualist interactions and
the enhancement arising from plant–antagonist interactions. Future studies
aimed at understanding the ecological bases of population differentiation in
plants should therefore consider not only population differences in trait
means, but also population differences in subindividual trait variability and
how these relate to spatially variable selection exerted by mutualistic and
antagonistic animal consumers.
The experimental and observational studies conducted on wild populations of
Helleborus foetidus and Lavandula latifolia reviewed above
provide compelling evidence for a concerted action of both genetic
and epigenetic factors in the control of subindividual variability in leaf
and seed traits in these species. That epigenetic processes are apt to induce
phenotypically heterogeneous seed crops by individual plants has long been
known (McClintock, 1950; Banks and Fedoroff, 1989; Das and Messing, 1994),
although this has only infrequently been acknowledged. Comparable evidence
for subindividual variability in other reiterated organs such as flowers or
fruits is still lacking, so the generality of intertwined genetic and
epigenetic factors as jump-starters and drivers of that lowermost of all
levels of phenotypic variation in plant communities cannot yet be
ascertained. More generally, little is known about the ecological
implications of epigenetic variation in natural populations. Unsurprisingly,
looking for “the ecological causes and consequences of epigenetic
variation” was recently singled out as one fundamental ecological question
(Sutherland et al., 2013). Since then, studies on wild plants have documented
relationships between epigenetic variation and functional diversity within
and among individual plants (Alonso et al., 2014, 2017; Medrano et al., 2014;
Herrera et al., 2015); relationships between epigenetic differences and
ecological scenarios across conspecific populations that are largely
unrelated to genetic differences (Schulz et al., 2014; Herrera et al., 2017);
and the transgenerational transmission of patterns and extent of DNA
methylation from maternal parents to offspring (Herrera et al., 2018).
Additional observational and experimental studies are needed to establish the
relationships between ecological and phenotypic measurements of plants and
their epigenetic and genetic characteristics, in order to understand the
possible three-way relationships linking subindividual variability, genetic
features, and epigenetic mosaicism. One further line of inquiry should
consider whether genomic methylation patterns are inherited across
generations and subindividual epigenetic mosaics do eventually translate into
epigenetically heterogeneous progeny. Were these effects eventually proven,
epigenetic mosaicism and its associated subindividual phenotypic variation
would emerge as powerful, hitherto unrecognized factors contributing to the
short- and long-term dynamics and functional diversity of plant populations
and communities. And as a sequel, some ecology textbook would then choose
“From organs to ecosystems” as a subtitle.
See captions to Figs. 1, 2, 4, 5 and 6 for main data sources used in this paper.
The author declares that he has no conflict of interest.
Edited by: Daniel
Montesinos Reviewed by: two anonymous referees
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