Priyanga Amarasekare

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 Framework for Elucidating the Temperature Dependence of Fitness

Climate warming is predicted to cause large-scale extinctions, particularly of ectothermic species. A striking difference between tropical and temperate ectotherms is that tropical species experience a mean habitat temperature that is closer to the temperature at which fitness is maximized (Topt) and an upper temperature limit for survival (Tmax) that is closer to Topt than do temperate species. Thus, even a small increase in environmental temperature could put tropical ectotherms at high risk of extinction, whereas temperate ectotherms have a wider temperature cushion. Although this pattern is widely observed, the mechanisms that produce it are not well understood. Here we develop a mathematical framework to partition the temperature response of fitness into its components (fecundity, mortality, and development) and test model predictions with data for insects. We find that fitness declines at high temperatures because the temperature responses of fecundity and mortality act in opposite ways: fecundity decreases with temperature when temperatures exceed the optimal range, whereas mortality continues to increase. The proximity of Topt to Tmax depends on how the temperature response of development mediates the interaction between fecundity and mortality. When development is highly temperature sensitive, mortality exceeds reproduction only after fecundity has started to decline with temperature, which causes fitness to decline rapidly to zero when temperatures exceed Topt. The model correctly predicts empirically observed fitness-temperature relationships in insects from different latitudes. It also suggests explanations for the widely reported phenological shifts in many ectotherms and the latitudinal differences in fitness responses.

Selection on stability across ecological scales

Much of the focus in evolutionary biology has been on the adaptive differentiation among organisms. It is equally important to understand the processes that result in similarities of structure among systems. Here, we discuss examples of similarities occurring at different ecological scales, from predator-prey relations (attack rates and handling times) through communities (food-web structures) to ecosystem properties. Selection among systemic configurations or patterns that differ in their intrinsic stability should lead generally to increased representation of relatively stable structures. Such nonadaptive, but selective processes that shape ecological communities offer an enticing mechanism for generating widely observed similarities, and have sparked new interest in stability properties. This nonadaptive systemic selection operates not in opposition to, but in parallel with, adaptive evolution.

Competition for benefits can promote the persistence of mutualistic interactions.

Mutualistic interactions are characterized by positive density-dependence that should cause interacting species to go extinct when rare. However, data show mutualistic interactions to be common and persistent. Previous theory predicts persistence provided that mutualistic species are regulated by factors external to the mutualistic interaction (e.g., limiting background resources). Empirical data suggest that competition for the benefits provided by mutualistic partners could be a source of negative density-dependence that allows for population regulation, but there is little, if any, theoretical exploration of this mechanism. Here we develop mathematical models to investigate whether competition for benefits alone can allow the persistence of obligate mutualistic interactions. We consider the role of trade-offs in persistence, specifically, trade-offs between benefits acquired versus given and between competition for access to partners (competitive ability) and benefit acquisition. We find that competition for benefits alone is sufficient to promote the persistence of pairwise interactions and the assembly of a three-species community module from an initially pairwise interaction. We find that a trade-off between benefits acquired versus given reduces opportunities for cheating (because a species that acquires significantly more benefits than it gives drives its partner extinct), while a trade-off between competitive ability and benefit acquisition facilitates persistence when it is weak, but constrains persistence when it is strong. When both trade-offs operate simultaneously, persistence requires that each species acquire sufficient benefits to avoid being cheated by its partners, but not so much that it loses its competitive ability. The key finding is that competition for benefits provides a biologically-realistic mechanism for the long-term persistence of mutualistic interactions and the assembly of complex community modules from initially pairwise interactions.

The biological control of disease vectors.

Vector-borne diseases are common in nature and can have a large impact on humans, livestock and crops. Biological control of vectors using natural enemies or competitors can reduce vector density and hence disease transmission. However, the indirect interactions inherent in host-vector disease systems make it difficult to use traditional pest control theory to guide biological control of disease vectors. This necessitates a conceptual framework that explicitly considers a range of indirect interactions between the host-vector disease system and the vectors biological control agent. Here we conduct a comparative analysis of the efficacy of different types of biological control agents in controlling vector-borne diseases. We report three key findings. First, highly efficient predators and parasitoids of the vector prove to be effective biological control agents, but highly virulent pathogens of the vector also require a high transmission rate to be effective. Second, biocontrol agents can successfully reduce long-term host disease incidence even though they may fail to reduce long-term vector densities. Third, inundating a host-vector disease system with a natural enemy of the vector has little or no effect on reducing disease incidence, but inundating the system with a competitor of the vector has a large effect on reducing disease incidence. The comparative framework yields predictions that are useful in developing biological control strategies for vector-borne diseases. We discuss how these predictions can inform ongoing biological control efforts for host-vector disease systems.

Effects of warming on predator-prey interactions - a resource-based approach and a theoretical synthesis

We theoretically explore consequences of warming for predator-prey dynamics, broadening previous approaches in three ways: we include beyond-optimal temperatures, predators may have a type III functional response, and prey carrying capacity depends on explicitly modelled resources. Several robust patterns arise. The relationship between prey carrying capacity and temperature can range from near-independence to monotonically declining/increasing to hump-shaped. Predators persist in a U-shaped region in resource supply (=enrichment)-temperature space. Type II responses yield stable persistence in a U-shaped band inside this region, giving way to limit cycles with enrichment at all temperatures. In contrast, type III responses convey stability at intermediate temperatures and confine cycles to low and high temperatures. Warming-induced state shifts can be predicted from system trajectories crossing stability and persistence boundaries in enrichment-temperature space. Results of earlier studies with more restricted assumptions map onto this graph as special cases. Our approach thus provides a unifying framework for understanding warming effects on trophic dynamics.

The intrinsic growth rate as a predictor of population viability under climate warming

1. Lately, there has been interest in using the intrinsic growth rate (rm) to predict the effects of climate warming on ectotherm population viability. However, because rm is calculated using the Euler-Lotka equation, its reliability in predicting population persistence depends on whether ectotherm populations can achieve a stable age/stage distribution in thermally variable environments. Here, we investigate this issue using a mathematical framework that incorporates mechanistic descriptions of temperature effects on vital rates into a stage-structured population model that realistically captures the temperature-induced variability in developmental delays that characterize ectotherm life cycles. 2. We find that populations experiencing seasonal temperature variation converge to a stage distribution whose intra-annual pattern remains invariant across years. As a result, the mean annual per capita growth rate also remains constant between years. The key insight is the mechanism that allows populations converge to a stationary stage distribution. Temperature effects on the biochemical processes (e.g. enzyme kinetics, hormonal regulation) that underlie life-history traits (reproduction, development and mortality) exhibit well-defined thermodynamical properties (e.g. changes in entropy and enthalpy) that lead to predictable outcomes (e.g. reduction in reaction rates or hormonal action at temperature extremes). As a result, life-history traits exhibit a systematic and predictable response to seasonal temperature variation. This in turn leads to temporally predictable temperature responses of the stage distribution and the per capita growth rate. 3. When climate warming causes an increase in the mean annual temperature and/or the amplitude of seasonal fluctuations, the population model predicts the mean annual per capita growth rate to decline to zero within 100 years when warming is slow relative to the developmental period of the organism (0.03-0.05°C per year) and to become negative, causing population extinction, well before 100 years when warming is fast (e.g. 0.1°C per year). The Euler-Lotka equation predicts a slower decrease in rm when warming is slow and a longer persistence time when warming is fast, with the deviation between the two metrics increasing with increasing developmental period. These results suggest that predictions of ectotherm population viability based on rm may be valid only for species with short developmental delays, and even then, only over short time-scales and under slow warming regimes.

A Metric for Quantifying the Oscillatory Tendency of Consumer-Resource Interactions

The oscillatory tendency of consumer-resource interactions is a key determinant of food-web persistence. Here, we develop a metric for quantifying oscillatory tendency that scales the positive feedback effects of saturating functional responses with the negative feedback effects of self-limitation. We use this metric to predict the oscillatory tendency of a pairwise interaction, tritrophic chain, and tritrophic web. This framework yields two key predictions. First, the oscillatory tendency of any food web increases with the number of trophic links with long handling times regardless of the magnitude of attack rates. Attack rates influence oscillatory tendency only when handling times are short. Second, the realized oscillatory tendency of a trophic link depends on how the product of the attack rate and handling time scales with the strength of self-limitation. Importantly, our metric allows calculations of the critical self-limitation strength at which a consumer-resource interaction moves from stable to oscillatory dynamics. Our data analysis reveals that the majority (77%) of interactions involve low attack rates and handling times, requiring only a modest level of self-limitation to suppress oscillations. Only 23% of the interactions exhibit a strong oscillatory tendency, consistent with previous findings, based on time-series data, that 30% of consumer-resource interactions in nature exhibit oscillations.

Toward a Mechanistic Understanding of Thermal Niche Partitioning

We develop a theoretical framework to elucidate the mechanistic basis of thermal niche partitioning in ectotherms. Using a food web module of two consumers competing for a biotic resource, we investigate how temperature effects on species’ attack and mortality rates scale up to population-level outcomes of coexistence and exclusion. We find that differences between species in their competitive effects ultimately arise from asymmetries generated by the nonlinear nature of the temperature response of mortality: cold-adapted species and thermal specialists limit themselves more strongly than they limit their warm-adapted and generalist competitors. These asymmetries become greater as seasonal temperature fluctuations increase, generating latitudinal variation in coexistence patterns and priority effects. Characterizing species’ thermal niches in terms of mechanistic descriptions of trait responses to temperature allows us to make testable predictions about the population-level outcomes of competition based solely on three fundamental—and easily measurable—quantities: attack rate optima, response breadths, and temperature sensitivity of mortality. We validate our framework by testing its predictions with data from an insect host-parasitoid community. Simply by quantifying the three basic quantities, we predict that priority effects cannot occur in this system, which is borne out by population-level experiments showing that the outcome of competition does not depend on initial conditions. More broadly, our framework can predict the conditions under which exotic invasive species can exclude or coexist with native biota as well as the effects of climate warming on competitive communities across latitudinal gradients.

Modeling oncolytic virotherapy: Is complete tumor-tropism too much of a good thing?

The specific targeting of tumor cells by replication-competent oncolytic viruses is considered indispensable for realizing the potential of oncolytic virotherapy. Yet off-target infections by oncolytic viruses may increase virus production, further reducing tumor load. This ability may be critical when tumor-cell scarcity or the onset of an adaptive immune response constrain viral anti-tumoral efficacy. Here we develop a mathematical framework for assessing whether oncolytic viruses with reduced tumor-specificity can more effectively eliminate tumors while keeping losses to normal cell populations low. We find viruses that infect some normal cells can potentially balance the competing goals of tumor elimination and minimizing the effects on normal cell populations. Particularly when infected tissues can be regenerated, moderating rather than completely eliminating the ability of oncolytic viruses to infect and lyse normal cells could improve cancer treatment, with potentially fewer side-effects than conventional treatments such as chemotherapy.