A predictive model of community assembly that incorporates intraspecific trait variation

Community assembly involves two antagonistic processes that select functional traits in opposite directions. Environmental filtering tends to increase the functional similarity of species within communities leading to trait convergence, whereas competition tends to limit the functional similarity of species within communities leading to trait divergence. Here, we introduce a new hierarchical Bayesian model that incorporates intraspecific trait variation into a predictive framework to unify classic coexistence theory and evolutionary biology with recent trait‐based approaches. Model predictions exhibited a significant positive correlation (r = 0.66) with observed relative abundances along a 10 °C gradient in mean annual temperature. The model predicted the correct dominant species in half of the plots, and accurately reproduced species' temperature optimums. The framework is generalizable to any ecosystem as it can accommodate any species pool, any set of functional traits and multiple environmental gradients, and it eliminates some of the criticisms associated with recent trait‐based community assembly models.     

Why intraspecific trait variation matters in community ecology

Natural populations consist of phenotypically diverse individuals that exhibit variation in their demographic parameters and intra- and inter-specific interactions. Recent experimental work indicates that such variation can have significant ecological effects. However, ecological models typically disregard this variation and focus instead on trait means and total population density. Under what situations is this simplification appropriate? Why might intraspecific variation alter ecological dynamics? In this review we synthesize recent theory and identify six general mechanisms by which trait variation changes the outcome of ecological interactions. These mechanisms include several direct effects of trait variation per se and indirect effects arising from the role of genetic variation in trait evolution.     

A trait-based approach predicting community assembly and dominance of microbial invasive species

Understanding the mechanisms underlying community assembly helps to define success and susceptibility to biological invasions. Here, we explored phytoplankton community assembly following niche and neutral paradigms and using a trait-based approach. Under the hypothesis that the morphology-based functional groups (MBFG) clusters species with similar niche, we analysed how trait-related differences in fitness influence dominance of an invasive species. This was based on literature review, field data and model simulations. We predict that invading species can be dominant if: 1) do not belong to the local MBFG but use unexploited areas of the niche, or 2) belong to the resident MBFG but exhibit a higher fitness due to a particular combination of traits. The invasive dinoflagellate Ceratium furcoides was used as the model species to evaluate these hypotheses, its morphological (e.g. volume) and physiological (e.g. growth rates) traits were compared with species from the same (V: photosynthetic flagellates) and different (VII: colonial cyanobacteria) MBFG. Fitness was estimated using models parametrized with MBFG rates (R*, ability to draw down phosphate) under different environmental conditions (i.e. flushing). Results contributed to support both hypotheses. First, the alternation of C. furcoides and cyanobacteria dominance was explained by the use of different niches. Secondly, species from MBFG V were dominant under similar environments. Within this group V C. furcoides showed higher fitness under low flushing and high predation, advantage provided by a distinctive combination of traits. The application of trait-based approaches to represent the niche and estimate fitness along environmental gradients was useful to evaluate community assembly and can be used to predict the dominance of microbial species invasions.     

Robust hypothesis tests for independence in community assembly

The extent to which competition affects the distributions of species at large spatial scales is unclear. To evaluate this question, hypothesis tests that do not depend on parametric assumptions are needed. Here, we develop a broadly applicable test that requires only one parametric assumption. Letting i and j denote the ith and jth colonists to arrive at a site, respectively, and [i j] the event that i and j belong to the same "unit" (e.g., functional group, genus), we show how colonists will be partitioned into units if for all i and j, [i j] is independent of whether i and j share unit membership with the other colonists, conditional on other information about shared units. Our distribution of partitions is useful for inferring competitive effects, because these effects predict that for at least one i and j, P ([i j]) will be less when i and j share unit membership than when they do not.     

Phylogenetic and trait-based assembly of arbuscular mycorrhizal fungal communities

Both competition and environmental filtering are expected to influence the community structure of microbes, but there are few tests of the relative importance of these processes because trait data on these organisms is often difficult to obtain. Using phylogenetic and functional trait information, we tested whether arbuscular mycorrhizal (AM) fungal community composition in an old field was influenced by competitive exclusion and/or environmental filtering. Communities at the site were dominated by species from the most speciose family of AM fungi, the Glomeraceae, though species from two other lineages, the Acaulosporaceae and Gigasporaceae were also found. Despite the dominance of species from a single family, AM fungal species most frequently co-existed when they were distantly related and when they differed in the ability to colonize root space on host plants. The ability of AM fungal species to colonize soil did not influence co-existence. These results suggest that competition between closely related and functionally similar species for space on plant roots influences community assembly. Nevertheless, in a substantial minority of cases communities were phylogenetically clustered, indicating that closely related species could also co-occur, as would be expected if i) the environment restricted community membership to single functional type or ii) competition among functionally similar species was weak. Our results therefore also suggest that competition for niche space between closely related fungi is not the sole influence of mycorrhizal community structure in field situations, but may be of greater relative importance than other ecological mechanisms.     

The effect of intraspecific variation and heritability on community pattern and robustness

Intraspecific trait variation is widespread in nature, yet its effects on community dynamics are not well understood. Here we explore the consequences of intraspecific trait variation for coexistence in two‐ and multispecies competitive communities. For two species, the likelihood of coexistence is in general reduced by intraspecific variation, except when the species have almost equal trait means but different trait variances, such that one is a generalist and the other a specialist consumer. In multispecies communities, the only strong effect of non‐heritable intraspecific variation is to reduce expected species richness. However, when intraspecific variation is heritable, allowing for the possibility of trait evolution, communities are much more resilient against environmental disturbance and exhibit far more predictable trait patterns. Our results are robust to varying model parameters and relaxing model assumptions.     

A trait-based approach to community assembly: partitioning of species trait values into within- and among-community components

Plant functional traits vary both along environmental gradients and among species occupying similar conditions, creating a challenge for the synthesis of functional and community ecology. We present a trait-based approach that provides an additive decomposition of species' trait values into alpha and beta components: beta values refer to a species' position along a gradient defined by community-level mean trait values; alpha values are the difference between a species' trait values and the mean of co-occurring taxa. In woody plant communities of coastal California, beta trait values for specific leaf area, leaf size, wood density and maximum height all covary strongly, reflecting species distributions across a gradient of soil moisture availability. Alpha values, on the other hand, are generally not significantly correlated, suggesting several independent axes of differentiation within communities. This trait-based framework provides a novel approach to integrate functional ecology and gradient analysis with community ecology and coexistence theory.     

A stochastic dispersal-limited trait-based model of community dynamics

I present a model of stochastic community dynamics in which death occurs randomly in the community, propagules disperse randomly from a regional pool, and recruitment of new individuals of a species is proportional to the species local abundance multiplied by its local competitive ability. The competitive ability of a species is assumed to be determined by a function of one trait of the species, and I call this function the environmental filtering function. I show that information on local species abundances in a network of plots, together with trait data for each species, enables the inference of both the immigration rate and the environmental filtering function in each plot. I further study how the diversity patterns produced by this model deviate from the neutral predictions, and how this deviation depends on the characteristics of the environmental filtering function. I show that this inference framework is more powerful at detecting trait-based environmental filtering than existing statistical approaches based on trait distributions, and discuss how the predictions of this model could be used to assess environmental heterogeneity in a plot, to detect functionally meaningful trade-offs among species traits, and to test the assumption that there exists a simple relationship between species traits and local competitive ability.     

Evaluating intraspecific variation in insect trait analysis

1. Intraspecific variation plays important roles in ecology and evolution. Yet, information on how species and populations vary remains scarce, particularly for insects and regarding functional traits. This lack of knowledge can be problematic in trait‐based ecology because traditional approaches assume negligible intraspecific variation, even for analyses that assess highly variable taxa.
2. We measured 291 Arctic fritillary butterflies (Boloria chariclea) to assess the intraspecific variation in one population of this species, evaluating (i) how wingspan of Arctic fritillaries varies in relation to the other species of its community, and (ii) how well wingspan, a measure of body size, predicts weight, a measure of body mass.
3. Wingspan of Arctic fritillaries varied between 2.62 and 4.07 cm, with the 95% interval range, including ～33% (14/42) of the species in the community, and ～30% (84/279) of the butterflies of Canada. The relationship between wingspan and weight was significant (β_wingspan = 0.002, SE = 0.0008, P < 0.001), but relatively weak (R²_adj = 0.31, F_2,288 = 67.82, P < 0.001).
4. We discuss our findings in relation to the assumption of species homogeneity and the use of proxies in the analysis of species traits, complementing our case study with simulations to illustrate how intraspecific and interspecific variation interact in determining when traditional trait analyses are robust. We suggest entomologists interested in trait analyses should critically evaluate how intraspecific variation could affect their inference, especially when evaluating species that are highly sexually dimorphic, phenotypically plastic, and/or distributed across broad environmental and spatial clines.

     

A spatially explicit trait-based approach uncovers changes in assembly processes under warming

The re-assembly of plant communities during climate warming depends on several concurrent processes. Here, we present a novel framework that integrates spatially explicit sampling, plant trait information and a warming experiment to quantify shifts in these assembly processes. By accounting for spatial distance between individuals, our framework allows separation of potential signals of environmental filtering from those of different types of competition. When applied to an elevational transplant experiment in the French Alps, we found common signals of environmental filtering and competition in all communities. Signals of environmental filtering were generally stronger in alpine than in subalpine control communities, and warming reduced this filter. Competition signals depended on treatments and traits: Symmetrical competition was dominant in control and warmed alpine communities, while hierarchical competition was present in subalpine communities. Our study highlights how distance-dependent frameworks can contribute to a better understanding of transient re-assembly dynamics during environmental change.     

The evolution of intraspecific variation in social organization

Many species show intraspecific variation in their social organization (IVSO), which means the composition of their social groups can change between solitary living, pair living, or living in groups. Understanding IVSO is important because it demonstrates species resilience to environmental change and can help us to study ultimate and proximate reasons for group living by comparing solitary and group‐living individuals in a single species. It has long been realized that the environment plays a key role in explaining the occurrence of IVSO. IVSO is expected to have evolved in variable environments and can thus be a key adaptation to environmental change. It has previously been suggested that four different mechanisms relying on the environment exist that can lead to IVSO: environmental disrupters, genetic differentiation, developmental plasticity, and social flexibility. All four mechanisms depend on the environment such that focusing only on environmental factors alone cannot explain IVSO. Importantly, only three represent evolved mechanisms, while environmental disrupters leading to the death of important group members induce nonadaptive IVSO. Environmental disrupters can be expected to cause IVSO even in species where IVSO is also an adaptive response. Here, we focus on the questions of why IVSO occurs and why it evolved. To understand IVSO at the species level, it is important to conduct continuous long‐term studies to differentiate between nonadaptive and adaptive IVSO. We predict that IVSO evolves in environments that vary in important ecological variables, such as rainfall, food availability, and population density. IVSO might also depend on life history factors, especially longevity. IVSO is predicted to be more common in species with a short life span and that breed only for one breeding season, being selected to respond optimally to the prevailing environmental situation. Finally, we emphasize the importance of accounting for IVSO when studying social evolution, especially in comparative studies, as not every species can be assigned to one single form of social organization. For such comparative studies, it is important to use data based on the primary literature.     

Ecological consequences of intraspecific variation in lake Daphnia

1. Although populations harbour considerable diversity, most ecological studies still assume they are homogeneous. However, mounting evidence suggests that intraspecific diversity is not only common, but also important for interactions with community members. Here, intraspecific variation in Daphnia dentifera in haemoglobin content is shown to be a marker of hypolimnion use. 2. Hypolimnion use differed substantially within and among D. dentifera populations. Daphnia dentifera with haemoglobin resided primarily in the hypolimnion, while D. dentifera lacking haemoglobin migrated vertically. These ‘deep’ and ‘migratory’D. dentifera had different seasonal phenologies and dynamics. 3. Deep and migratory D. dentifera had qualitatively different relationships with an important competitor, Daphnia pulicaria. Deep D. dentifera density was negatively correlated with D. pulicaria density, whereas migratory density was not correlated with D. pulicaria density. 4. Given that D. pulicaria tends to reside in the hypolimnion, this negative correlation probably reflects competition between D. pulicaria and the deep D. dentifera. This pattern would have been missed if only the relationship between the overall lake populations of D. dentifera and D. pulicaria had been studied. 5. Abundances of deep D. dentifera and D. pulicaria were both correlated with the size of the hypolimnetic refuge from fish predation, but in opposite directions. Lakes with large refuges generally had high D. pulicaria and low deep D. dentifera densities.     

Nanostructure predicts intraspecific variation in ultraviolet-blue plumage colour

Evidence suggests that structural plumage colour can be an honest signal of individual quality, but the mechanisms responsible for the variation in expression of structural coloration within a species have not been identified. We used full-spectrum spectrometry and transmission electron microscopy to investigate the effect of variation in the nanostructure of the spongy layer on expression of structural ultraviolet (UV)-blue coloration in eastern bluebird (Sialia sialis) feathers. Fourier analysis revealed that feather nanostructure was highly organized but did not accurately predict variation in hue. Within the spongy layer of feather barbs, the number of circular keratin rods significantly predicted UV-violet chroma, whereas the standard error of the diameter of these rods significantly predicted spectral saturation. These observations show that the precision of nanostructural arrangement determines some colour variation in feathers.     

Lack of intraspecific variation in cpDNA in Trichocolea tomentella

Abstract

The Asian genus Struckia Müll.Hal. is reduced to a synonym of Plagiothecium Bruch &; Schimp. according to a phylogenetic analysis involving S. argentata (Mitt.) Müll.Hal., S. enervis (Broth.) Ignatov, T.J.Kop. &; D.G.Long and 13 representative boreal species of Plagiothecium. Two nuclear regions, ITS and partial gapC, and five chloroplast regions, rbcL, rps4-trnS, psaB, trnG and trnL-F, were utilized to reconstruct the phylogenetic relationship between Struckia and Plagiothecium. Bayesian, maximum parsimony, and maximum likelihood analyses resulted in a strongly supported clade including Struckia and Plagiothecium. Plagiothecium handelii Broth. and P. paleaceum (Mitt.) A.Jaeger, which share similar geographical ranges with Struckia and intermediate morphological traits between Struckia and Plagiothecium, grouped with the Chinese Struckia, and all of them appeared as sister to the ‘core’ of Plagiothecium. The accurate position of P. piliferum (Sw.) Schimp. remains unclear due to moderate support from all analyses, and we suggest that it is retained in Plagiothecium until further evidence is available.     

Plant age affects intraspecific variation in functional traits

Functional traits are often used to examine ecological patterns and processes. Ontogeny—changes that occur over time as the result of development—generates variation in traits within individual organisms. We aimed to quantify the role of ontogeny in structuring functional trait variation across a range of co-existing herbaceous perennial species and hypothesized that ontogenetic variation in traits would be greater in younger vs. older plants. We grew eight herbaceous perennial forb species common in tallgrass prairies from seed in a greenhouse in Madison, Wisconsin, USA to determine how and when time-related variation in functional traits is large relative to other sources of variation, such as differences between leaves and species. We destructively measured common functional traits on four individuals of each species every two weeks for 19 weeks, including leaf mass fraction, root mass fraction, stem mass fraction, specific leaf area, leaf dry matter content, and leaf area. We found that most functional traits indeed change through time, that the direction of many changes are consistent between species but the magnitude of change is species specific, and most time-related variation occurred earlier in development. These results emphasize the importance of considering sampling timing and differences between young and old plants when measuring functional traits. Our results suggest that ontogenetic intraspecific variation can be substantial, especially early in life. It may be problematic to use traits measured from mature plants to interpret the importance of processes that occur at earlier life stages or vice versa; using seedling traits to understand adult plant responses may also be inappropriate.

     

Disentangling niche and neutral influences on community assembly: assessing the performance of community phylogenetic structure tests

Patterns of phylogenetic relatedness within communities have been widely used to infer the importance of different ecological and evolutionary processes during community assembly, but little is known about the relative ability of community phylogenetics methods and null models to detect the signature of processes such as dispersal, competition and filtering under different models of trait evolution. Using a metacommunity simulation incorporating quantitative models of trait evolution and community assembly, I assessed the performance of different tests that have been used to measure community phylogenetic structure. All tests were sensitive to the relative phylogenetic signal in species metacommunity abundances and traits; methods that were most sensitive to the effects of niche-based processes on community structure were also more likely to find non-random patterns of community phylogenetic structure under dispersal assembly. When used with a null model that maintained species occurrence frequency in random communities, several metrics could detect niche-based assembly when there was strong phylogenetic signal in species traits, when multiple traits were involved in community assembly, and in the presence of environmental heterogeneity. Interpretations of the causes of community phylogenetic structure should be modified to account for the influence of dispersal.     

Intraspecific trait variation and colonization sequence alter community assembly and disease epidemics

When individuals from multiple populations colonize a new habitat patch, intraspecific trait variation can make the arrival order of colonists an important factor for subsequent population and community dynamics. In particular, intraspecific priority effects (IPEs) allow early arrivers to limit the growth or establishment of later arrivers, even when competitively inferior on a per‐capita basis. Through their effects on genes and traits, IPEs can alter short‐term growth and long‐term evolutionary change in single species metapopulations. Given their importance for intraspecific interactions, IPEs in a dominant species have the potential to affect the composition of entire communities. We conducted an experiment to determine whether and how arrival order and IPEs in the zooplankter Daphnia pulex affected its interactions with both competitors (the cladoceran Simocephalus vetulus) and parasites (the virulent fungus Metschnikowia bicuspidata). We found strong evidence for IPEs in Daphnia, as early arrivers inhibited late arrivers even when competitively inferior. These IPEs in Daphnia altered both the establishment success of interspecific competitors and the size of disease epidemics: early colonization by fast‐growing D. pulex led to large Daphnia populations and low competitor establishment, but large disease epidemics. Early colonization by slow‐growing D. pulex, on the other hand, resulted in small Daphnia populations with high competitor establishment, but smaller disease epidemics. Overall, our results demonstrate the importance of intraspecific variation and arrival order for community dynamics, and highlight IPEs as a general mechanism driving variation in natural communities.