Size always matters, shape matters only for the big: potential optical effects of silica bodies in Selaginella.

Silica bodies are commonly found in Selaginella, but their function is unclear. Lens-like appearance and location in many species above giant chloroplasts of dorsal epidermal cells suggest optical functions. Silica body morphology in three Selaginella species was studied by microscopy. Optical effects were assessed by wave-optic simulations. Large convex, approximately hemispherical (papillose) and small approximately conical (concave-convex) silica bodies were found in different species. Both types lead to a concentrated spot of light high in the dorsal epidermal cell. Large convex bodies concentrate light 10-25 times in a shape-dependent manner by refraction, and small silica bodies concentrate light in a shape-insensitive, but wavelength-dependent, manner by diffraction (red light: approx. 2.3 times; blue light: approx. 1.5 times). Due to chloroplast movement, this concentrated light is above the chloroplast under high light, but within it under low light. Beyond the spot of concentration, light is dispersed into the chloroplast. Thin Selaginella leaves mean these effects may enhance light capture and minimize photodamage, but other effects such as inhibition of herbivory, mechanical support, and immune responses need to be considered. Silica bodies undoubtedly have optical effects, but their significance to the functioning of the plant requires direct studies of ecophysiological performance.

The complete plastid genome of Selaginella erythropus (Selaginellaceae), a species with distinctive giant chloroplasts.

The plastid genome of the deep-shade plant Selaginella erythropus, which has highly unusual chloroplasts, was characterized using Illumina pair-end sequencing. This plastome is 140,151 bp in length with a large single-copy region (LSC) of 56,133 bp, a small single-copy region (SSC) of 61,268 bp, and two direct repeats (DRs) of 11,375 bp. The overall GC content is 50.68%, while those of LSC, SSC, and DR are 48.96%, 50.3%, and 55.96%, respectively. The plastome contains 102 genes, including 76 protein-coding, 15 tRNA (12 tRNA species), and 8 rRNA genes (4 rRNA species). The phylogenetic analysis shows that S. erythropus is closely related to S. moellendorffii and S. doederleinii. This result is consistent with the previous phylogenetic relationship inferred from multiple plastid and nuclear loci. However, only S. erythropus has the two-zoned giant chloroplast, the bizonoplast. The plastome provides an excellent reference for understanding the unique chloroplast differentiation in Selaginellaceae.

Character displacement in the presence of multiple trait differences: Evolution of the storage effect in germination and growth.

Ecological character displacement is a prominent hypothesis for the maintenance of ecological differences between species that are critical to stable coexistence. Models of character displacement often ascribe interspecific competitive interactions to a single character, but multiple characters contribute to competition, and their effects on selection can be nonadditive. Focusing on one character, we ask if other characters that affect competition alter evolutionary outcomes for the focal character. We address this question using the variable environment seed bank model for two species with two traits. The focal trait is the temporal pattern of germination, which is evolutionary labile. The other trait is the temporal pattern of plant growth, which is assumed fixed. We ask whether evolutionary divergence of germination patterns between species depends on species differences in plant growth. Patterns of growth can affect selection on germination patterns in two ways. First, cues present at germination can provide information about future growth. Second, germination and growth jointly determine the biomass of plants, which determines demand for resources. Germination and growth contribute to the selection gradient in distinct components, one density-independent and the other density-dependent. Importantly, the relative strengths of the components are key. When the density-dependent component is stronger, displacement in germination patterns between species is larger. Stronger cues at germination strengthen the density-independent component by increasing the benefits of germinating in years of favorable growth. But cues also affect the density-dependent component by boosting a species' biomass, and hence its competitive effect, in good years. Consequently, cues weaken character displacement when growth patterns are similar for two competitors, but favor displacement when growth patterns are species-specific. Understanding how these selection components change between contexts can help understand the origin and maintenance of species differences in germination patterns in temporally fluctuating environments.

A general theory of coexistence and extinction for stochastic ecological communities.

We analyze a general theory for coexistence and extinction of ecological communities that are influenced by stochastic temporal environmental fluctuations. The results apply to discrete time (stochastic difference equations), continuous time (stochastic differential equations), compact and non-compact state spaces and degenerate or non-degenerate noise. In addition, we can also include in the dynamics auxiliary variables that model environmental fluctuations, population structure, eco-environmental feedbacks or other internal or external factors. We are able to significantly generalize the recent discrete time results by Benaim and Schreiber (J Math Biol 79:393-431, 2019) to non-compact state spaces, and we provide stronger persistence and extinction results. The continuous time results by Hening and Nguyen (Ann Appl Probab 28(3):1893-1942, 2018a) are strengthened to include degenerate noise and auxiliary variables. Using the general theory, we work out several examples. In discrete time, we classify the dynamics when there are one or two species, and look at the Ricker model, Log-normally distributed offspring models, lottery models, discrete Lotka-Volterra models as well as models of perennial and annual organisms. For the continuous time setting we explore models with a resource variable, stochastic replicator models, and three dimensional Lotka-Volterra models.

Gigantic chloroplasts, including bizonoplasts, are common in shade-adapted species of the ancient vascular plant family Selaginellaceae.

PREMISE: Unique among vascular plants, some species of Selaginella have single giant chloroplasts in their epidermal or upper mesophyll cells (monoplastidy, M), varying in structure between species. Structural variants include several forms of bizonoplast with unique dimorphic ultrastructure. Better understanding of these structural variants, their prevalence, environmental correlates and phylogenetic association, has the potential to shed new light on chloroplast biology unavailable from any other plant group. METHODS: The chloroplast ultrastructure of 76 Selaginella species was studied with various microscopic techniques. Environmental data for selected species and subgeneric relationships were compared against chloroplast traits. RESULTS: We delineated five chloroplast categories: ME (monoplastidy in a dorsal epidermal cell), MM (monoplastidy in a mesophyll cell), OL (oligoplastidy), Mu (multiplastidy, present in the most basal species), and RC (reduced or vestigial chloroplasts). Of 44 ME species, 11 have bizonoplasts, cup-shaped (concave upper zone) or bilobed (basal hinge, a new discovery), with upper zones of parallel thylakoid membranes varying subtly between species. Monoplastidy, found in 49 species, is strongly shade associated. Bizonoplasts are only known in deep-shade species (<2.1% full sunlight) of subgenus Stachygynandrum but in both the Old and New Worlds. CONCLUSIONS: Multiplastidic chloroplasts are most likely basal, implying that monoplastidy and bizonoplasts are derived traits, with monoplastidy evolving at least twice, potentially as an adaptation to low light. Although there is insufficient information to understand the adaptive significance of the numerous structural variants, they are unmatched in the vascular plants, suggesting unusual evolutionary flexibility in this ancient plant genus.

Germination variation facilitates the evolution of seed dormancy when coupled with seedling competition.

Fluctuating environmental conditions have consequences for the evolution of life histories because they cause fitness variance. This variance can favor risk-spreading strategies, often known as bet-hedging strategies, in which growth or reproduction is spread over time or space, with some costs, but greater certainty of success. An important example is seed dormancy in annual plants, in which some fraction of seed remains dormant at any given germination opportunity with the potential of germinating later when environmental conditions may differ. Previous theory shows that environmental variation is critical for the evolution of dormancy. However, these studies have focused on temporal variation in reproduction, ignoring the strong observed effects of environmental variation on the germination fraction, a major contributor to fitness variance. We ask what effects germination fluctuations have on selection for dormancy by adding germination fluctuations to existing density-independent (d.i.) and density-dependent (d.d.) models of annual plant dynamics, extending previous analyses by including temporally fluctuating germination. Specifically, we ask how germination variance affects selection on the temporal average germination fraction, here used to define dormancy. When present alone, or when independently varying with other fitness components, germination fluctuations do not affect selection for dormancy in the d.i. model, despite generating fitness variance because this variance contribution is not reduced by higher dormancy. Germination fluctuations have strong effects in the d.d. model, favoring dormancy when present either alone or coupled with variation affecting plant growth. This is because germination variation causes seedling density to vary, which causes variable reproduction through variable intraspecific competition. Dormancy is advantaged under variable reproduction because it creates a more convex relationship between population growth and reproduction leading to benefits from nonlinear averaging. Predictive germination, a positive statistical association between germination and growth, weakens selection for dormancy under strong competition and strengthens it when competition is weak. Our results suggest that variable germination is a potential explanation for high levels of dormancy observed in nature, with implications for life-history theory for fluctuating environments.

Effects of Predator Avoidance Behavior on the Coexistence of Competing Prey.

Predator avoidance behavior, in which prey limit foraging activities in the presence of predation threats, affects the dynamics of many ecological communities. Despite the growing theoretical appreciation of the role predation plays in coexistence, predator avoidance behavior has yet to be incorporated into the theory in a general way. We introduce adaptive avoidance behavior to a consumer-resource model with three trophic levels to ask whether the ability of prey-the middle trophic level-to avoid predators alters their ability to coexist. We determine the characteristics of cases in which predator avoidance behavior changes prey coexistence or the order of competitive dominance. The mechanism underlying such changes is the weakening of apparent competition relative to resource competition in determining niche overlap, even with resource intake costs. Avoidance behavior thus generally promotes coexistence if prey partition resources but not predators, whereas it undermines coexistence if prey partition predators but not resources. For any given case, the changes in the average fitness difference between two species resulting from avoidance behavior interact with changes in niche overlap to determine coexistence. These results connect the substantial body of theoretical work on avoidance behavior and population dynamics with the body of theory on competitive coexistence.

Contributions to nonstationary community theory.

The study of the role of environmental variation in community dynamics has traditionally assumed that the environment is a stationary stochastic process or a periodic deterministic process. However, the physical environment in nature is nonstationary. Moreover, anthropogenically driven climate change provides a new challenge emphasizing a persistent but frequently ignored problem: how to make predictions about the dynamics of communities when the nonstationarity of the physical environment is recognized. Recent work is providing a path to conclusions with none of the traditional assumptions of environmental stationarity or periodicity. Traditional assumptions about convergence of long-term averages of functions of environmental states can be replaced by assumptions about temporal sums, allowing convergence and persistence of population processes to be demonstrated in general nonstationary environments. These tools are further developed and illustrated here with some simple models of nonstationary community dynamics, including the Beverton-Holt model, the threshold exponential and the lottery model.

Lamelloplasts and minichloroplasts in Begoniaceae: iridescence and photosynthetic functioning.

Iridoplasts (modified plastids in adaxial epidermal cells) reported from Begonia were originally hypothesized to cause iridescence, which was broadly accepted for decades. However, several species of Begonia with iridoplasts are not iridescent causing confusion. Here chloroplast ultrastructure was observed in 40 taxa of Begoniaceae to explore the phenomenon of iridescence. However, 22 Begonias and Hillebrandia were found to have iridoplasts, but only nine display visually iridescent blue to blue-green leaves. Unexpectedly, a new type of plastid, a 'minichloroplast,' was found in the abaxial epidermal cells of all taxa, but was present in adaxial epidermal cells only if iridoplasts were absent. Comparative ultrastructural study of iridoplasts and a shading experiment of selected taxa show that a taxon with iridoplasts does not inevitably have visual iridescence, but iridescence is greatly affected by the spacing between thylakoid lamellae (stoma spacing). Thus, we propose instead the name 'lamelloplast' for plastids filled entirely with regular lamellae to avoid prejudging their function. To evaluate photosynthetic performance, chlorophyll fluorescence (F v /F m ) was measured separately from the chloroplasts in the adaxial epidermis and lower leaf tissues by using leaf dermal peels. Lamelloplasts and minichloroplasts have much lower photosynthetic efficiency than mesophyll chloroplasts. Nevertheless, photosynthetic proteins (psbA protein of PSII, RuBisCo and ATPase) were detected in both plastids as well as mesophyll chloroplasts in an immunogold labeling. Spectrometry revealed additional blue to blue-green peaks in visually iridescent leaves. Micro-spectrometry detected a blue peak from single blue spots in adaxial epidermal cells confirming that the color is derived from lamelloplasts. Presence of lamelloplasts or minichloroplasts is species specific and exclusive. High prevalence of lamelloplasts in Begoniaceae, including the basal clade Hillebrandia, highlights a unique evolutionary development. These new findings clarify the association between iridescence and lamelloplasts, and with implications for new directions in the study of plastid morphogenesis.

AEDT: A new concept for ecological dynamics in the ever-changing world.

The important concept of equilibrium has always been controversial in ecology, but a new, more general concept, an asymptotic environmentally determined trajectory (AEDT), overcomes many concerns with equilibrium by realistically incorporating long-term climate change while retaining much of the predictive power of a stable equilibrium. A population or ecological community is predicted to approach its AEDT, which is a function of time reflecting environmental history and biology. The AEDT invokes familiar questions and predictions but in a more realistic context in which consideration of past environments and a future changing profoundly due to human influence becomes possible. Strong applications are also predicted in population genetics, evolution, earth sciences, and economics.

Leaf structure affects a plant's appearance: combined multiple-mechanisms intensify remarkable foliar variegation.

The presence of foliar variegation challenges perceptions of leaf form and functioning. But variegation is often incorrectly identified and misinterpreted. The striking variegation found in juvenile Blastus cochinchinensis (Melastomataceae) provides an instructive case study of mechanisms and their ecophysiological implications. Variegated (white and green areas, vw and vg) and non-variegated leaves (normal green leaves, ng) of seedlings of Blastus were compared structurally with microtechniques, and characterized for chlorophyll content and fluorescence. More limited study of Sonerila heterostemon (Melastomataceae) and Kaempferia pulchra (Zingiberaceae) tested the generality of the findings. Variegation in Blastus combines five mechanisms: epidermal, air space, upper mesophyll, chloroplast and crystal, the latter two being new mechanisms. All mesophyll cells (vw, vg, ng) have functional chloroplasts with dense thylakoids. The vw areas are distinguished by flatter adaxial epidermal cells and central trichomes containing crystals, the presence of air spaces between the adaxial epidermis and a colorless spongy-like upper mesophyll containing smaller and fewer chloroplasts. The vw area is further distinguished by having the largest spongy-tissue chloroplasts and fewer stomata. Both leaf types have similar total chlorophyll content and similar  F v/F m (maximum quantum yield of PSII), but vg has significantly higher F v/F m than ng. Variegation in Sonerila and Kaempferia is also caused by combined mechanisms, including the crystal type in Kaempferia. This finding of combined mechanisms in three different species suggests that combined mechanisms may occur more commonly in nature than current understanding. The combined mechanisms in Blastus variegated leaves represent intricate structural modifications that may compensate for and minimize photosynthetic loss, and reflect changing plant needs.

How optimally foraging predators promote prey coexistence in a variable environment.

Optimal foraging is one of the major predictive theories of predator foraging behavior. However, how an optimally foraging predator affects the coexistence of competing prey is not well understood either in a constant or variable environment, especially for multiple prey species. We study the impact of optimal foraging on prey coexistence using an annual plant model, with and without annual variation in seed germination. Seed predators are modeled using Charnov's model of adaptive diet choice. Our results reveal that multiple prey species can coexist because of this type of predator, and that their effect is not greatly modified by environmental variation. However, in diverse communities, the requirements for coexistence by optimal foraging alone are very restrictive. Optimally foraging predators can have a strong equalizing effect on their prey by creating a competition-predation trade-off. Thus, their main role in promoting diversity may be to reduce species-average fitness differences, making it easier for other mechanisms, such as the storage effect, to allow multiple species to coexist. Like previous models, our model showed that when germination rates vary, the storage effect from competition promotes coexistence. Our results also show that optimally foraging predators can generate a negative storage effect from predation, undermining coexistence, but that this effect will be minor whenever predators commonly differentiate their prey.

Scale-Dependent Community Theory for Streams and Other Linear Habitats.

The maintenance of species diversity occurs at the regional scale but depends on interacting processes at the full range of lower scales. Although there is a long history of study of regional diversity as an emergent property, analyses of fully multiscale dynamics are rare. Here, we use scale transition theory for a quantitative analysis of multiscale diversity maintenance with continuous scales of dispersal and environmental variation in space and time. We develop our analysis with a model of a linear habitat, applicable to streams or coastlines, to provide a theoretical foundation for the long-standing interest in environmental variation and dispersal, including downstream drift. We find that the strength of regional coexistence is strongest when local densities and local environmental conditions are strongly correlated. Increasing dispersal and shortening environmental correlations weaken the strength of coexistence regionally and shift the dominant coexistence mechanism from fitness-density covariance to the spatial storage effect, while increasing local diversity. Analysis of the physical and biological determinants of these mechanisms improves understanding of traditional concepts of environmental filters, mass effects, and species sorting. Our results highlight the limitations of the binary distinction between local communities and a species pool and emphasize species coexistence as a problem of multiple scales in space and time.

The Effects of Dynamical Rates on Species Coexistence in a Variable Environment: The Paradox of the Plankton Revisited.

Hutchinson's famous hypothesis for the "paradox of the plankton" has been widely accepted, but critical aspects have remained unchallenged. Hutchinson argued that environmental fluctuations would promote coexistence when the timescale for environmental change is comparable to the timescale for competitive exclusion. Using a consumer-resource model, we do find that timescales of processes are important. However, it is not the time to exclusion that must be compared with the time for environmental change but the time for resource depletion. Fast resource depletion, when resource consumption is favored for different species at different times, strongly promotes coexistence. The time for exclusion is independent of the rate of resource depletion. Therefore, the widely believed predictions of Hutchinson are misleading. Fast resource depletion, as determined by environmental conditions, ensures strong coupling of environmental processes and competition, which leads to enhancement over time of intraspecific competition relative to interspecific competition as environmental shifts favor different species at different times. This critical coupling is measured by the covariance between environment and competition. Changes in this quantity as densities change determine the stability of coexistence and provide the key to rigorous analysis, both theoretically and empirically, of coexistence in a variable environment. These ideas apply broadly to diversity maintenance in variable environments whether the issue is species diversity or genetic diversity and competition or apparent competition.

The effect of soil-borne pathogens depends on the abundance of host tree species.

The overarching issue for understanding biodiversity maintenance is how fitness advantages accrue to a species as it becomes rare, as this is the defining feature of stable coexistence mechanisms. Without these fitness advantages, average fitness differences between species will lead to exclusion. However, empirical evidence is lacking, especially for forests, due to the difficulty of manipulating density on a large-enough scale. Here we took advantage of naturally occurring contrasts in abundance between sites of a subtropical tree species, Ormosia glaberrima, to demonstrate how low-density fitness advantages accrue by the Janzen-Connell mechanism. The results showed that soil pathogens suppressed seedling recruitment of O. glaberrima when it is abundant but had little effect on the seedlings when it is at low density due to the lack of pathogens. The difference in seedling survival between abundant and low-density sites demonstrates strong dependence of pathogenic effect on the abundance of host species.

Distance-responsive predation is not necessary for the Janzen-Connell hypothesis.

The Janzen-Connell hypothesis states that tree diversity in tropical forests is maintained by specialist predators that are distance- or density-responsive (i.e. predators that reduce seed or seedling survival near adults of their hosts). Many empirical studies have investigated whether predators are distance-responsive; however, few studies have examined whether distance-responsiveness matters for how predators maintain tree diversity. Using a site-occupancy model, we show analytically that distance-responsive predators are actually less able to maintain diversity than specialist predators that are not distance-responsive. Generally, specialist predators maintain diversity because they become rare when their host's densities are low, reducing predation risk. However, if predators are distance-responsive, and most seeds cannot disperse away from these predators, then seed predation rates will remain high, even if predator density is low across the landscape. Consequently, a reduction in a host's population density may not lead to a significant reduction in seed and seedling predation. We show that habitat partitioning can cause recruitment to be highest near conspecific adults, even in the presence of distance-responsive predators, without any change in the effect that the predators have on coexistence (a result contrary to predictions of the Janzen-Connell hypothesis). Rather, specialist predators and habitat partitioning have additive effects on species coexistence in our model, i.e., neither mechanism alters the effect of the other one.

The relative importance of relative nonlinearity and the storage effect in the lottery model.

Although it is likely that many coexistence mechanisms contribute to maintenance of species diversity, most approaches to understanding species coexistence proceed as if only one mechanism would be present. In studies of species coexistence in a temporally fluctuating environment, the storage effect, believed to be the most important coexistence mechanism, has been the focus. Although a different coexistence mechanism--relative nonlinearity--is also predicted to arise frequently with environmental variation, its effect has been overshadowed by the storage effect. The relatively nonlinear growth rates on which the mechanism depends arise simply from differences in life history traits. Many kinds of temporal variation can then interact with these nonlinearity differences to create the relative nonlinearity coexistence mechanism. Much is unknown about when this mechanism is important and its total neglect is not justified. Here, we use the lottery model to provide a much needed quantitative assessment of the relative and combined effects of relative nonlinearity and the storage effect. Our analysis takes advantage of recently developed techniques for quantifying coexistence mechanisms when multiple mechanisms operate in concert. We find that relative nonlinearity is able to contribute substantially to species coexistence in the lottery model when two conditions are satisfied: (1) species must differ greatly in their adult death rates, (2) sensitivity of recruitment to environmental variation must be greater for species with larger adult death rates. In addition, relative nonlinearity has a critical role in compensating for a weakened storage effect when there is high correlation between species in their responses to the varying environment. In some circumstances relative nonlinearity is stronger than the storage effect or is even the sole mechanism of coexistence.

A variation on chloroplast development: the bizonoplast and photosynthetic efficiency in the deep-shade plant Selaginella erythropus.

UNLABELLED: • PREMISE OF THE STUDY: Chloroplast development and structure are highly conserved in vascular plants, but the bizonoplast of Selaginella is a notable exception. In the shade plant S. erythropus, each dorsal epidermal cell contains one bizonoplast, while other cells have normal chloroplasts. Our quest was to (1) determine the origin of bizonoplasts, (2) explore developmental plasticity, and (3) correlate developmental changes with photosynthetic activity to provide insights unavailable in other green plants with more constrained development.• METHODS: Bizonoplast development was studied in juvenile prostrate and older erect shoots of S. erythropus. Plastid plasticity was studied in plants cultivated under different light conditions. Chlorophyll fluorescence was measured and correlated with photosynthetic activity.• KEY RESULTS: The bizonoplast originates from a proplastid, forming a distinctive upper zone rapidly after exposure to low light. In the prostrate shoots, the proplastid develops through early stages only. When the shoot becomes erect, the proplastid soon develops into a mature bizonoplast. Erect shoots have significantly higher photosynthetic efficiency than prostrate shoots. No bizonoplasts were found in the plants growing in high light, where 2-4 spheroidal chloroplasts formed, or with light from below.• CONCLUSIONS: The upper zone develops above a normal-looking chloroplast structure to produce a bizonoplast. Bizonoplast developmental plasticity suggests that regular lamellar structure and monoplastidy are adaptations to deep shade environments. Such novel variation in S. erythropus is in stark contrast to known plastid development in other vascular plants, possibly reflecting retention of developmental flexibility in the basal clade, Lycophyta, to which it belongs.