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

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.publishedVersio

Fungal Symbionts as Manipulators of Plant Reproductive Biology

Symbioses have shaped the evolution of life, most notably through the fixation of heritable symbionts into organelles. The inheritance of symbionts promotes mutualism and fixation by coupling partner fitness. However, conflicts arise if symbionts are transmitted through only one sex and can shift host resources toward the sex through which they propagate. Such reproductive manipulators have been documented in animals with separate sexes but not in other phyla or sexual systems. Here we investigated whether the investment in male relative to female reproduction differed between hermaphroditic host plants with versus without a maternally inherited fungal symbiont. Plants with the fungus produced more seeds and less pollen than plants lacking the fungus, resulting in an ∼40% shift in functional gender and a switch from male-biased to female-biased sex allocation. Given the ubiquity of endophytes in plants, reproductive manipulators of hermaphrodites may be widespread in nature

KING OF THE HILL? HOW BIOTIC INTERACTIONS AFFECT BIOGEOGRAPHICAL PATTERN AND SPECIES RESPONSES TO CLIMATE CHANGE

As climate has warmed, many species have moved up mountains as physiological limits to their distributions have ameliorated. These distribution shifts are creating novel communities, begging the question: What happens to species at the tops of mountains as potential antagonists encroach upwards? Theory predicts that upward migrations will cause range contractions for high-elevation species because of novel interactions with encroaching antagonists. My dissertation work is one of the most comprehensive tests of this question to date, using a combination of ecological niche modeling (ENM), experiments, and demographic and trait-based modeling approaches. I created novel ENMs that suggest context-dependency of biotic interactions, where predictions of biotic interactions change from positive to negative over environmental gradients, is common over elevation gradients. Additionally, ENMs suggested the current focus on plant-plant interactions in niche modeling targets the most important biotic interaction for many species. I then constructed space-for-time experiments that transplanted alpine species into novel low elevation plant and mammal communities expected to encroach upwards, as well as into their native high elevation communities. Plant competition was manipulated by vegetation removals and mammals were excluded in a separate factorial experiment using below- and aboveground fencing. In both experiments, low elevation plant and mammal communities suppressed growth of alpine species to a greater extent than those antagonists found in their home range. However, demographic models suggested that environmental factors (e.g. temperature) other than novel plant and mammal communities are more consequential for determining population fate. The experiments validated a novel trait-based model of competitive interactions that can be broadly applied to other systems and conservation needs. My dissertation work found that alpine plants are unlikely to remain “king of the hill” under climate change, in part due to the upward encroachment of novel competitors and intensification of herbivore pressure

Predicting Changes in Bee Assemblages Following State Transitions at North American Dryland Ecotones

Drylands worldwide are experiencing ecosystem state transitions: the expansion of some ecosystem types at the expense of others. Bees in drylands are particularly abundant and diverse, with potential for large compositional differences and seasonal turnover across ecotones. To better understand how future ecosystem state transitions may influence bees, we compared bee assemblages and their seasonality among sites at the Sevilleta National Wildlife Refuge (NM, USA) that represent three dryland ecosystem types (and two ecotones) of the southwestern U.S. (Plains grassland, Chihuahuan Desert grassland, and Chihuahuan Desert shrubland). Using passive traps, we caught bees during two-week intervals from March–October, 2002–2014. The resulting dataset included 302 bee species and 56 genera. Bee abundance, composition, and diversity differed among ecosystems, indicating that future state transitions could alter bee assemblage composition in our system. We found strong seasonal bee species turnover, suggesting that bee phenological shifts may accompany state transitions. Common species drove the observed trends, and both specialist and generalist bee species were indicators of ecosystem types or months; these species could be sentinels of community-wide responses to future shifts. Our work suggests that predicting the consequences of global change for bee assemblages requires accounting for both within-year and among-ecosystem variation

Herbivory damage but not plant disease under experimental warming is dependent on weather for three subalpine grass species

Both theory and prior studies predict that climate warming should increase attack rates by herbivores and pathogens on plants. However, past work has often assumed that variation in abiotic conditions other than temperature (e.g. precipitation) do not alter warming responses of plant damage by natural enemies. Studies over short time periods span low variation in weather, and studies over long time-scales often neglect to account for fine-scale weather conditions. Here, we used a 20+ year warming experiment to investigate if warming affects on herbivory and pathogen disease are dependent on variation in ambient weather observed over 3 years. We studied three common grass species in a subalpine meadow in the Colorado Rocky Mountains, USA. We visually estimated herbivory and disease every 2 weeks during the growing season and evaluated weather conditions during the previous 2- or 4-week time interval (2-week average air temperature, 2- and 4-week cumulative precipitation) as predictors of the probability and amount of damage. Herbivore attack was 13% more likely and damage amount was 29% greater in warmed plots than controls across the focal species but warming treatment had little affect on plant disease. Herbivory presence and damage increased the most with experimental warming when preceded by wetter, rather than drier, fine-scale weather, but preceding ambient temperature did not strongly interact with elevated warming to influence herbivory. Disease presence and amount increased, on average, with warmer weather and more precipitation regardless of warming. Synthesis. The effect of warming over reference climate on herbivore damage is dependent on and amplified by fine-scale weather variation, suggesting more boom-and-bust damage dynamics with increasing climate variability. However, the mean effect of regional climate change is likely reduced monsoon rainfall, for which we predict a reduction in insect herbivore damage. Plant disease was generally unresponsive to warming, which may be a consequence of our coarse disease estimates that did not track specific pathogen species or guilds. The results point towards temperature as an important but not sufficient determinant and regulator of species interactions, where precipitation and other constraints may determine the affect of warming.publishedVersio

Bioavailability of Macro and Micronutrients Across Global Topsoils: Main Drivers and Global Change Impacts

Understanding the chemical composition of our planet\u27s crust was one of the biggest questions of the 20th century. More than 100 years later, we are still far from understanding the global patterns in the bioavailability and spatial coupling of elements in topsoils worldwide, despite their importance for the productivity and functioning of terrestrial ecosystems. Here, we measured the bioavailability and coupling of thirteen macro- and micronutrients and phytotoxic elements in topsoils (3–8 cm) from a range of terrestrial ecosystems across all continents (∼10,000 observations) and in response to global change manipulations (∼5,000 observations). For this, we incubated between 1 and 4 pairs of anionic and cationic exchange membranes per site for a mean period of 53 days. The most bioavailable elements (Ca, Mg, and K) were also amongst the most abundant in the crust. Patterns of bioavailability were biome-dependent and controlled by soil properties such as pH, organic matter content and texture, plant cover, and climate. However, global change simulations resulted in important alterations in the bioavailability of elements. Elements were highly coupled, and coupling was predictable by the atomic properties of elements, particularly mass, mass to charge ratio, and second ionization energy. Deviations from the predictable coupling-atomic mass relationship were attributed to global change and agriculture. Our work illustrates the tight links between the bioavailability and coupling of topsoil elements and environmental context, human activities, and atomic properties of elements, thus deeply enhancing our integrated understanding of the biogeochemical connections that underlie the productivity and functioning of terrestrial ecosystems in a changing world

Plant-symbiotic fungi as chemical engineers: multi-genome analysis of the Clavicipitaceae reveals dynamics of alkaloid Loci

The fungal family Clavicipitaceae includes plant symbionts and parasites that produce several psychoactive and bioprotective alkaloids. The family includes grass symbionts in the epichloae clade (Epichloë and Neotyphodium species), which are extraordinarily diverse both in their host interactions and in their alkaloid profiles. Epichloae produce alkaloids of four distinct classes, all of which deter insects, and some—including the infamous ergot alkaloids—have potent effects on mammals. The exceptional chemotypic diversity of the epichloae may relate to their broad range of host interactions, whereby some are pathogenic and contagious, others are mutualistic and vertically transmitted (seed-borne), and still others vary in pathogenic or mutualistic behavior. We profiled the alkaloids and sequenced the genomes of 10 epichloae, three ergot fungi (Claviceps species), a morning-glory symbiont (Periglandula ipomoeae), and a bamboo pathogen (Aciculosporium take), and compared the gene clusters for four classes of alkaloids. Results indicated a strong tendency for alkaloid loci to have conserved cores that specify the skeleton structures and peripheral genes that determine chemical variations that are known to affect their pharmacological specificities. Generally, gene locations in cluster peripheries positioned them near to transposon-derived, AT-rich repeat blocks, which were probably involved in gene losses, duplications, and neofunctionalizations. The alkaloid loci in the epichloae had unusual structures riddled with large, complex, and dynamic repeat blocks. This feature was not reflective of overall differences in repeat contents in the genomes, nor was it characteristic of most other specialized metabolism loci. The organization and dynamics of alkaloid loci and abundant repeat blocks in the epichloae suggested that these fungi are under selection for alkaloid diversification. We suggest that such selection is related to the variable life histories of the epichloae, their protective roles as symbionts, and their associations with the highly speciose and ecologically diverse cool-season grasses

Covariation of Soil Bacterial Composition with Plant Rarity ▿ †

Rare and common plants are predicted to host different rhizospheric microbes. To evaluate this prediction, we used terminal restriction fragment length polymorphism (T-RFLP) analysis to compare rhizospheric bacteria from eight native grass species whose local abundances in their natural ecosystem spanned a 15-fold range. We observed that locally rare versus common plants are associated with divergent bacterial communities