Microbial symbionts buffer hosts from the demographic costs of environmental stochasticity.

Species' persistence in increasingly variable climates will depend on resilience against the fitness costs of environmental stochasticity. Most organisms host microbiota that shield against stressors. Here, we test the hypothesis that, by limiting exposure to temporally variable stressors, microbial symbionts reduce hosts' demographic variance. We parameterized stochastic population models using data from a 14-year symbiont-removal experiment including seven grass species that host Epichloë fungal endophytes. Results provide novel evidence that symbiotic benefits arise not only through improved mean fitness, but also through dampened inter-annual variance. Hosts with "fast" life-history traits benefited most from symbiont-mediated demographic buffering. Under current climate conditions, contributions of demographic buffering were modest compared to benefits to mean fitness. However, simulations of increased stochasticity amplified benefits of demographic buffering and made it the more important pathway of host-symbiont mutualism. Microbial-mediated variance buffering is likely an important, yet cryptic, mechanism of resilience in an increasingly variable world.

Two-Sex Demography, Sexual Niche Differentiation, and the Geographic Range Limits of Texas Bluegrass (Poa arachnifera).

AbstractUnderstanding the mechanisms that generate biogeographic range limits is a long-standing goal of ecology. It is widely hypothesized that distributional limits reflect the environmental niche, but this hypothesis is complicated by the potential for intraspecific niche heterogeneity. In dioecious species, sexual niche differentiation may cause divergence between the sexes in their limits of environmental suitability. We studied range boundary formation in Texas bluegrass (Poa arachnifera), a perennial dioecious plant, testing the alternative hypotheses that range limits reflect the niche limits of females only versus the combined contributions of females and males, including their interdependence via mating. Common garden experiments across a longitudinal aridity gradient revealed female-biased flowering approaching eastern range limits, suggesting that mate limitation may constrain the species' distribution. However, a demographic model showed that declines in λ approaching range limits were driven almost entirely by female vital rates. The dominant role of females was attributable to seed viability being robust to sex ratio variation and to low sensitivity of λ to reproductive transitions. We suggest that female-dominant range limits may be common to long-lived species with polygamous mating systems and that female responses to environmental drivers may often be sufficient for predicting range shifts in response to environmental change.

Nectar resources affect bird-dispersed microbial metacommunities in suburban and rural gardens.

As cities expand, understanding how urbanization affects biodiversity is a key ecological goal. Yet, little is known about how host-associated microbial diversity responds to urbanization. We asked whether communities of microbial (bacterial and fungal) in floral nectar and sugar-water feeders and vectored by nectar-feeding birds-thus forming a metacommunity-differed in composition and diversity between suburban and rural gardens. Compared to rural birds, we found that suburban birds vectored different and more diverse bacterial communities. These differences were not detected in the nectar of common plant species, suggesting that nectar filters microbial taxa and results in metacommunity convergence. However, when considering all the nectar sources present, suburban beta diversity was elevated compared to rural beta diversity due to turnover of bacterial taxa across a plant species and sugar-water feeders. While fungal metacommunity composition and beta diversity in nectar were similar between suburban and rural sites, alpha diversity was elevated in suburban sites, which mirrored the trend of increased fungal alpha diversity on birds. These results emphasize the interdependence of host, vector, and microbial diversity and demonstrate that human decisions can shape nectar microbial diversity in contrasting ways for bacteria and fungi.

Mammalian herbivores restrict the altitudinal range limits of alpine plants.

Although rarely experimentally tested, biotic interactions have long been hypothesised to limit low-elevation range boundaries of species. We tested the effects of herbivory on three alpine-restricted plant species by transplanting plants below (novel), at the edge (limit), or in the centre (core) of their current elevational range and factorially fencing-out above- and belowground mammals. Herbivore damage was greater in range limit and novel habitats than in range cores. Exclosures increased plant biomass and reproduction more in novel habitats than in range cores, suggesting demographic costs of novel interactions with herbivores. We then used demographic models to project population growth rates, which increased 5-20% more under herbivore exclosure at range limit and novel sites than in core habitats. Our results identify mammalian herbivores as key drivers of the low-elevation range limits of alpine plants and indicate that upward encroachment of herbivores could trigger local extinctions by depressing plant population growth.

Lagged and dormant season climate better predict plant vital rates than climate during the growing season.

Understanding the effects of climate on the vital rates (e.g., survival, development, reproduction) and dynamics of natural populations is a long-standing quest in ecology, with ever-increasing relevance in the face of climate change. However, linking climate drivers to demographic processes requires identifying the appropriate time windows during which climate influences vital rates. Researchers often do not have access to the long-term data required to test a large number of windows, and are thus forced to make a priori choices. In this study, we first synthesize the literature to assess current a priori choices employed in studies performed on 104 plant species that link climate drivers with demographic responses. Second, we use a sliding-window approach to investigate which combination of climate drivers and temporal window have the best predictive ability for vital rates of four perennial plant species that each have over a decade of demographic data (Helianthella quinquenervis, Frasera speciosa, Cylindriopuntia imbricata, and Cryptantha flava). Our literature review shows that most studies consider time windows in only the year preceding the measurement of the vital rate(s) of interest, and focus on annual or growing season temporal scales. In contrast, our sliding-window analysis shows that in only four out of 13 vital rates the selected climate drivers have time windows that align with, or are similar to, the growing season. For many vital rates, the best window lagged more than 1 year and up to 4 years before the measurement of the vital rate. Our results demonstrate that for the vital rates of these four species, climate drivers that are lagged or outside of the growing season are the norm. Our study suggests that considering climatic predictors that fall outside of the most recent growing season will improve our understanding of how climate affects population dynamics.

Demography-Dispersal Trait Correlations Modify the Eco-Evolutionary Dynamics of Range Expansion.

Spreading populations are subject to evolutionary processes acting on dispersal and reproduction that can increase invasion speed and variability. It is typically assumed that dispersal and demography traits evolve independently, but abundant evidence points to correlations between them that may be positive or negative and genetic, maternal, or environmental. We sought to understand how demography-dispersal correlations modify the eco-evolutionary dynamics of range expansion. We first explored this question with the beetle Callosobruchus maculatus, a laboratory model in which evolutionary acceleration of invasion has been demonstrated. We then built a simulation model to explore the role of trait correlations in this system and more generally. We found that positive correlations amplify the positive influence of evolution on speed and variability while negative correlations (such as we found empirically) constrain that influence. Strong negative genetic correlations can even cause evolution to decelerate invasion. Genetic and nongenetic (maternal and environmental) correlations had similar effects on some measures of invasion but different effects on others. Model results enabled us to retrospectively explain invasion dynamics and trait evolution in C. maculatus and may similarly aid the interpretation of other field and laboratory studies. Nonindependence of demography and dispersal is an important consideration for understanding and predicting outcomes of range expansion.

Simulated folivory increases vertical transmission of fungal endophytes that deter herbivores and alter tolerance to herbivory in Poa autumnalis.

BACKGROUND AND AIMS: The processes that maintain variation in the prevalence of symbioses within host populations are not well understood. While the fitness benefits of symbiosis have clearly been shown to drive changes in symbiont prevalence, the rate of transmission has been less well studied. Many grasses host symbiotic fungi (Epichloë spp.), which can be transmitted vertically to seeds or horizontally via spores. These symbionts may protect plants against herbivores by producing alkaloids or by increasing tolerance to damage. Therefore, herbivory may be a key ecological factor that alters symbiont prevalence within host populations by affecting either symbiont benefits to host fitness or the symbiont transmission rate. Here, we addressed the following questions: Does symbiont presence modulate plant tolerance to herbivory? Does folivory increase symbiont vertical transmission to seeds or hyphal density in seedlings? Do plants with symbiont horizontal transmission have lower rates of vertical transmission than plants lacking horizontal transmission? METHODS: We studied the grass Poa autumnalis and its symbiotic fungi in the genus Epichloë. We measured plant fitness (survival, growth, reproduction) and symbiont transmission to seeds following simulated folivory in a 3-year common garden experiment and surveyed natural populations that varied in mode of symbiont transmission. KEY RESULTS: Poa autumnalis hosted two Epichloë taxa, an undescribed vertically transmitted Epichloë sp. PauTG-1 and E. typhina subsp. poae with both vertical and horizontal transmission. Simulated folivory reduced plant survival, but endophyte presence increased tolerance to damage and boosted fitness. Folivory increased vertical transmission and hyphal density within seedlings, suggesting induced protection for progeny of damaged plants. Across natural populations, the prevalence of vertical transmission did not correlate with symbiont prevalence or differ with mode of transmission. CONCLUSIONS: Herbivory not only mediated the reproductive fitness benefits of symbiosis, but also promoted symbiosis prevalence by increasing vertical transmission of the fungus to the next generation. Our results reveal a new mechanism by which herbivores could influence the prevalence of microbial symbionts in host populations.

Density dependence in demography and dispersal generates fluctuating invasion speeds.

Density dependence plays an important role in population regulation and is known to generate temporal fluctuations in population density. However, the ways in which density dependence affects spatial population processes, such as species invasions, are less understood. Although classical ecological theory suggests that invasions should advance at a constant speed, empirical work is illuminating the highly variable nature of biological invasions, which often exhibit nonconstant spreading speeds, even in simple, controlled settings. Here, we explore endogenous density dependence as a mechanism for inducing variability in biological invasions with a set of population models that incorporate density dependence in demographic and dispersal parameters. We show that density dependence in demography at low population densities-i.e., an Allee effect-combined with spatiotemporal variability in population density behind the invasion front can produce fluctuations in spreading speed. The density fluctuations behind the front can arise from either overcompensatory population growth or density-dependent dispersal, both of which are common in nature. Our results show that simple rules can generate complex spread dynamics and highlight a source of variability in biological invasions that may aid in ecological forecasting.

Sex-specific early survival drives adult sex ratio bias in snowy plovers and impacts mating system and population growth.

Adult sex ratio (ASR) is a central concept in population biology and a key factor in sexual selection, but why do most demographic models ignore sex biases? Vital rates often vary between the sexes and across life history, but their relative contributions to ASR variation remain poorly understood-an essential step to evaluate sex ratio theories in the wild and inform conservation. Here, we combine structured two-sex population models with individual-based mark-recapture data from an intensively monitored polygamous population of snowy plovers. We show that a strongly male-biased ASR (0.63) is primarily driven by sex-specific survival of juveniles rather than adults or dependent offspring. This finding provides empirical support for theories of unbiased sex allocation when sex differences in survival arise after the period of parental investment. Importantly, a conventional model ignoring sex biases significantly overestimated population viability. We suggest that sex-specific population models are essential to understand the population dynamics of sexual organisms: reproduction and population growth are most sensitive to perturbations in survival of the limiting sex. Overall, our study suggests that sex-biased early survival may contribute toward mating system evolution and population persistence, with implications for both sexual selection theory and biodiversity conservation.

Testing the roles of vertical transmission and drought stress in the prevalence of heritable fungal endophytes in annual grass populations.

Beneficial inherited symbionts are expected to reach high prevalence in host populations, yet many are observed at intermediate prevalence. Theory predicts that a balance of fitness benefits and efficiency of vertical transmission may interact to stabilize intermediate prevalence. We established populations of grass hosts (Lolium multiflorum) that varied in prevalence of a heritable fungal endophyte (Epichloё occultans), allowing us to infer long-term equilibria by tracking change in prevalence over one generation. We manipulated an environmental stressor (elevated precipitation), which we hypothesized would reduce the fitness benefits of symbiosis, and altered the efficiency of vertical transmission by replacing endophyte-positive seeds with endophyte-free seeds. Endophytes and elevated precipitation both increased host fitness, but symbiont effects were not stronger in the drier treatment, suggesting that benefits of symbiosis were unrelated to drought tolerance. Reduced transmission suppressed the inferred equilibrium prevalence from 42.6% to 11.7%. However, elevated precipitation did not modify prevalence, consistent with the result that it did not modify fitness benefits. Our results demonstrate that failed transmission can influence the prevalence of heritable microbes and that intermediate prevalence can be a stable equilibrium due to forces that allow symbionts to increase (fitness benefits) but prevent them from reaching fixation (failed transmission).

Native insect herbivory overwhelms context dependence to limit complex invasion dynamics of exotic weeds.

Understanding the role of consumers in density-dependent plant population dynamics is a long-standing goal in ecology. However, the generality of herbivory effects across heterogeneous landscapes is poorly understood due to the pervasive influence of context-dependence. We tested effects of native insect herbivory on the population dynamics of an exotic thistle, Cirsium vulgare, in a field experiment replicated across eight sites in eastern Nebraska. Using hierarchical Bayesian analysis and density-dependent population models, we found potential for explosive low-density population growth (λ > 5) and complex density fluctuations under herbivore exclusion. However, herbivore access drove population decline (λ < 1), suppressing complex fluctuations. While plant-herbivore interaction outcomes are famously context-dependent, we demonstrated that herbivores suppress potentially invasive populations throughout our study region, and this qualitative outcome is insensitive to environmental context. Our novel use of Bayesian demographic modelling shows that native insect herbivores consistently prevent hard-to-predict fluctuations of weeds in environments otherwise susceptible to invasion.

Can't live with them, can't live without them? Balancing mating and competition in two-sex populations.

Two-sex populations are usually studied through frequency-dependent models that describe how sex ratio affects mating, recruitment and population growth. However, in two-sex populations, mating and recruitment should also be affected by density and by its interactions with the sex ratio. Density may have positive effects on mating (Allee effects) but negative effects on other demographic processes. In this study, we quantified how positive and negative inter-sexual interactions balance in two-sex populations. Using a dioecious grass (Poa arachnifera), we established experimental field populations that varied in density and sex ratio. We then quantified mating success (seed fertilization) and non-mating demographic performance, and integrated these responses to project population-level recruitment. Female mating success was positively density-dependent, especially at female-biased sex ratios. Other demographic processes were negatively density-dependent and, in some cases, frequency-dependent. Integrating our experimental results showed that mate-finding Allee effects dominated other types of density-dependence, giving rise to recruitment that increased with increasing density and peaked at intermediate sex ratios, reflecting tension between seed initiation (greater with more females) and seed viability (greater with more males). Our results reveal, for the first time, the balance of positive and negative inter-sexual interactions in sex-structured populations. Models that account for both density- and sex ratio dependence, particularly in mating, may be necessary for understanding and predicting two-sex population dynamics.

Genetic mixture of multiple source populations accelerates invasive range expansion.

A wealth of population genetic studies have documented that many successful biological invasions stem from multiple introductions from genetically distinct source populations. Yet, mechanistic understanding of whether and how genetic mixture promotes invasiveness has lagged behind documentation that such mixture commonly occurs. We conducted a laboratory experiment to test the influence of genetic mixture on the velocity of invasive range expansion. The mechanistic basis for effects of genetic mixture could include evolutionary responses (mixed invasions may harbour greater genetic diversity and thus elevated evolutionary potential) and/or fitness advantages of between-population mating (heterosis). If driven by evolution, positive effects of source population mixture should increase through time, as selection sculpts genetic variation. If driven by heterosis, effects of mixture should peak following first reproductive contact and then dissipate. Using a laboratory model system (beetles spreading through artificial landscapes), we quantified the velocity of range expansion for invasions initiated with one, two, four or six genetic sources over six generations. Our experiment was designed to test predictions corresponding to the evolutionary and heterosis mechanisms, asking whether any effects of genetic mixture occurred in early or later generations of range expansion. We also quantified demography and dispersal for each experimental treatment, since any effects of mixture should be manifest in one or both of these traits. Over six generations, invasions with any amount of genetic mixture (two, four and six sources) spread farther than single-source invasions. Our data suggest that heterosis provided a 'catapult effect', leaving a lasting signature on range expansion even though the benefits of outcrossing were transient. Individual-level trait data indicated that genetic mixture had positive effects on local demography (reduced extinction risk and enhanced population growth) during the initial stages of invasion but no consistent effects on dispersal ability. Our work is the first to demonstrate that genetic mixture can alter the course of spatial expansion, the stage of invasion typically associated with the greatest ecological and economic impacts. We suggest that similar effects of genetic mixture may be a common feature of biological invasions in nature, but that these effects can easily go undetected.

Variation in the Prevalence and Transmission of Heritable Symbionts Across Host Populations in Heterogeneous Environments.

Heritable microbes are abundant in nature and influential to their hosts and the communities in which they reside. However, drivers of variability in the prevalence of heritable symbionts and their rates of transmission are poorly resolved, particularly across host populations experiencing variable biotic and abiotic environments. To fill these gaps, we surveyed 25 populations of two native grasses (Elymus virginicus and Elymus canadensis) across the southern Great Plains (USA). Both grass species host heritable endophytic fungi (genus Epichloё) and can hybridize where their ranges overlap. From a subset of hosts, we characterized endophyte genotype using genetic loci that link to bioactive alkaloid production. First, we found mean vertical transmission rates and population-level prevalence were positively correlated, specifically for E. virginicus. However, both endophyte prevalence and transmission varied substantially across populations and did not strongly correlate with abiotic variables, with one exception: endophyte prevalence decreased as drought stress decreased for E. virginicus hosts. Second, we evaluated the potential influence of biotic factors and found that, after accounting for climate, endophyte genotype explained significant variation in symbiont inheritance. We also contrasted populations where host species co-occurred in sympatry vs. allopatry. Sympatry could potentially increase interspecific hybridization, but this variable did not associate with patterns of symbiont prevalence or transmission success. Our results reveal substantial variability in symbiont prevalence and transmission across host populations and identify symbiont genotype, and to a lesser extent, the abiotic environment as sources of this variation.

The Role of Host Demographic Storage in the Ecological Dynamics of Heritable Symbionts.

Heritable symbioses are widespread and ecologically important. Many host organisms have complex life cycles that include diverse opportunities for symbionts to affect their host and be lost during development. Yet, existing theory takes a simplified view of host demography. Here, we generalize symbiosis theory to understand how demographic "storage" in the form of dormant or prereproductive life stages can modify symbiosis dynamics. Using grass-endophyte symbioses as context, we developed models to contrast the role of the seed bank (a storage stage) against the reproductive stage in symbiont persistence and prevalence. We find that the seed bank is as important as or more important than the reproductive stage in driving symbiont dynamics, as long as passage through the seed bank is obligate. Flexible entry to the seed bank substantially weakens its influence on symbiont persistence but can modify prevalence in counterintuitive ways. Our models identify a role for legacy effects, where hosts that lose symbionts retain their demographic influence. The retention of benefits via legacy effects can reduce symbiont prevalence and even cause prevalence to decline with increasing benefits to hosts because symbiont-free hosts carry those benefits. Our results resolve connections between individual-level host-symbiont interactions and population-level patterns, providing guidance for empirical studies.

Niche differentiation in the dynamics of host-symbiont interactions: symbiont prevalence as a coexistence problem.

Heritable symbioses can have important ecological effects and have triggered important evolutionary innovations. Current predictions for long-term symbiont prevalence are based on their fitness benefits and vertical transmission rates but ignore nonlinear competitive feedbacks among symbiotic and symbiont-free hosts. We hypothesized that such feedbacks function as stabilizing mechanisms, promoting coexistence of host types and maintaining intermediate symbiont frequency at the population scale. Using a model grass/endophyte symbiosis, we manipulated competition within and between endophyte-symbiotic (E+) and endophyte-free (E-) hosts and fit competition models to experimental data. We show for the first time that symbiont-structured competition can generate stable coexistence of E+ and E- hosts, even under perfect vertical transmission. Niche differentiation was the key to coexistence, causing hosts of each type to limit themselves more strongly than each other. These results establish roles for nonlinear competitive dynamics and niche differentiation in the ecology and evolution of heritable symbionts.

Sex and stochasticity affect range expansion of experimental invasions.

Understanding and predicting range expansion are key objectives in many basic and applied contexts. Among dioecious organisms, there is strong evidence for sex differences in dispersal, which could alter the sex ratio at the expansion's leading edge. However, demographic stochasticity could also affect leading-edge sex ratios, perhaps overwhelming sex-biased dispersal. We used insects in laboratory mesocosms to test the effects of sex-biased dispersal on range expansion, and a simulation model to explore interactive effects of sex-biased dispersal and demographic stochasticity. Sex-biased dispersal created spatial clines in the sex ratio, which influenced offspring production at the front and altered invasion velocity. Increasing female dispersal relative to males accelerated spread, despite the prediction that demographic stochasticity would weaken a signal of sex-biased dispersal. Our results provide the first experimental evidence for an influence of sex-biased dispersal on invasion velocity, highlighting the value of accounting for sex structure in studies of range expansion.

Evolutionary demography of iteroparous plants: incorporating non-lethal costs of reproduction into integral projection models.

Understanding the selective forces that shape reproductive strategies is a central goal of evolutionary ecology. Selection on the timing of reproduction is well studied in semelparous organisms because the cost of reproduction (death) can be easily incorporated into demographic models. Iteroparous organisms also exhibit delayed reproduction and experience reproductive costs, although these are not necessarily lethal. How non-lethal costs shape iteroparous life histories remains unresolved. We analysed long-term demographic data for the iteroparous orchid Orchis purpurea from two habitat types (light and shade). In both the habitats, flowering plants had lower growth rates and this cost was greater for smaller plants. We detected an additional growth cost of fruit production in the light habitat. We incorporated these non-lethal costs into integral projection models to identify the flowering size that maximizes fitness. In both habitats, observed flowering sizes were well predicted by the models. We also estimated optimal parameters for size-dependent flowering effort, but found a strong mismatch with the observed flower production. Our study highlights the role of context-dependent non-lethal reproductive costs as selective forces in the evolution of iteroparous life histories, and provides a novel and broadly applicable approach to studying the evolutionary demography of iteroparous organisms.

Avoiding unintentional eviction from integral projection models.

Integral projection models (IPMs) are increasingly being applied to study size-structured populations. Here we call attention to a potential problem in their construction that can have important consequences for model results. IPMs are implemented using an approximating matrix and bounded size range. Individuals near the size limits can be unknowingly "evicted" from the model because their predicted future size is outside the range. We provide simple measures for the magnitude of eviction and the sensitivity of the population growth rate (lambda) to eviction, allowing modelers to assess the severity of the problem in their IPM. For IPMs of three plant species, we found that eviction occurred in all cases and caused underestimation of the population growth rate (lambda) relative to eviction-free models; it is likely that other models are similarly affected. Models with frequent eviction should be modified because eviction is only possible when size transitions are badly mis-specified. We offer several solutions to eviction problems, but we emphasize that the modeler must choose the most appropriate solution based on an understanding of why eviction occurs in the first place. We recommend testing IPMs for eviction problems and resolving them, so that population dynamics are modeled more accurately.

There are many ways to be a mutualist: endophytic fungus reduces plant survival but increases population growth.

One of the challenges to quantifying the costs and benefits of symbiosis is that symbionts can influence different components of host fitness. To improve understanding of the ecology of inherited symbionts, we developed general theory for a perennial host-hereditary symbiont interaction, in which symbionts can have independent and potentially opposing effects on host regeneration and survival. The model showed that negative effects on one component of fitness may be outweighed by positive effects on another, leading to a net positive impact of symbiosis on population growth. Model predictions depended on the availability of suitable patches, which influenced the relative contributions of survival vs. regeneration to host fitness. We then used experimental symbiont removal to quantify effects of a hereditary, fungal endophyte on a grass host. Endophyte presence strongly reduced host survival but increased regeneration. Application of the model revealed that negative effects on plant survival were overwhelmed by beneficial effects on regeneration, resulting in stable endophyte persistence at 100% frequency, consistent with field observations. Our work demonstrates the utility of a demographic perspective for predicting the dynamics of symbioses and supports the hypothesis that symbionts function as mutualists when host and symbiont fitness are coupled through vertical transmission.