Individual vital rates, such as mortality and birth rates, are key determinants of lifetime reproductive success, and variability in these rates shapes population dynamics. Previous studies have found that this vital rate heterogeneity can influence demographic properties including population growth rates. However, the explicit effects of the amount of variation within and the covariance between vital rates that can also vary throughout the lifespan on population growth remains unknown. Here, we explore the analytical consequences of nongenetic heterogeneity on long-term population growth rates and rates of evolution by modifying traditional age-structured population projection matrices to incorporate variation among individual vital rates. The model allows vital rates to be permanent throughout life ("fixed condition”) or to change over the lifespan ("dynamic condition”). We reduce the complexity associated with adding individual heterogeneity to age-structured models through a novel application of matrix collapsing ("phenotypic collapsing"), showing how to collapse in a manner that preserves the asymptotic and transient dynamics of the original matrix. The main conclusion is that nongenetic individual heterogeneity can strongly impact the long-term growth rate and rates of evolution. The magnitude and sign of this impact depends heavily on how the heterogeneity covaries across the lifespan of an organism. Our results emphasize that nongenetic variation cannot simply be viewed as random noise, but rather that it has consistent, predictable effects on fitness and evolvability.

Parasitoids are small insects, (e.g., small wasps or flies) that reproduce by laying eggs on or within host arthropods. Parasitoids make up a large proportion of the world’s biodiversity and are popular agents of biological control. Idiobiont parasitoids paralyze their hosts upon attack and thus are expected to only target hosts large enough to support offspring development. Host resources generally impact host attributes and life histories including size, development, and life span. Some argue slow host development in response to resource quality increases parasitoid efficacy (i.e., a parasitoid’s ability to successfully reproduce on or within a host) due to longer host exposure to parasitoids. However, this hypothesis is not always supported and does not consider variation in other host traits in response to resources that may be important for parasitoids (e.g., variation in host size is known to impact parasitoid efficacy). In this study, we test whether trait variation within host developmental stages in response to host resources is more important for parasitoid efficacy and life histories than trait variation across host developmental stages. We exposed seed beetle hosts raised on a food quality gradient to mated female parasitoids and measured the number of hosts parasitized and parasitoid life history traits at the scale of host stage- and age-structure. Our results suggest host food quality does not cascade to impact idiobiont parasitoid life histories despite large food quality effects on host life history. Instead, variation in host life histories across host developmental stages better predicts parasitoid efficacy and life histories, suggesting finding a host in a specific instar is more important for idiobiont parasitoids than finding hosts on or within higher quality resources.

Many populations have intraspecific diversity in phenotype and ecological strategy, but the mechanisms maintaining such diversity are not fully understood. Multiple behaviors can be maintained either as a conditional strategy, where fitness depends on an individual’s phenotype, or as a mixed strategy where alternative behaviors have similar fitness independent of phenotype. Using high-resolution depth and time sampling, we characterize two distinct diel vertical migration behaviors in a population of freshwater zooplankton (Daphnia pulicaria). Individuals in this population differ in their color phenotype and migratory behavior with red morphs upregulating hemoglobin and undergoing a deep migration, and pale morphs not producing hemoglobin and undergoing a shallow migration. We experimentally manipulated the behavior of each phenotype in the field, and measured population growth in their natural migration behavior as well as population growth in their alternative behaviors. Experimental populations of pale and red morphs under their natural migrations had roughly equal fitness, despite vast differences in environmental conditions. When forced to switch behaviors, pale morphs suffered reduced fitness, whereas red morphs had similar fitness compared to their natural migration. Our results suggest that while behavioral diversity may be promoted by the opportunity for alternative behaviors of equal fitness, the distinct physiological conditions required for survival in alternative behaviors limit the capacity for individual behavioral switching and likely maintain behavioral diversity as a conditional strategy.

Asymmetric interactions among conspecifics can have diverse effects on population dynamics including stabilization, generation of cycles and induction of chaotic fluctuations. A difficult challenge, however, is establishing the link between the impact of asymmetric interactions on life history and the consequences for population dynamics. The smaller tea tortrix, Adoxophyes honmai, is a good example. Larval instars differ dramatically in size and have a tendency for cannibalism, which suggests the potential for strong asymmetric interactions among instars. Yet whether these asymmetries have any role in generating the distinct single-generation cycles observed in the field and laboratory is unclear. Here we report on the development of a new experimental approach to characterize the impact of asymmetric interactions on life history that can be directly embedded into stage-structured population models. The experiments use donor-replacement protocols in which focal individuals are challenged to complete their life-cycles in competitive environments where the instar and density of the competitors is held constant. The experimentally-derived interaction surface contains all the information about stage-specific interactions and provides a straightforward framework for evaluating alternative ways of abstracting the interactions into traditional models of asymmetric competition. Working with the smaller tea tortrix, we found strong evidence of asymmetric interactions and identified critical ‘tipping points’ in the competitive environment that strongly affected survival but not development. We incorporated the experimentally-derived interaction surface into a stage-structured population model and found that despite the strong impact that asymmetric interactions have on tea tortrix life history, they do not scale-up to impact the predicted asymptotic population dynamics. Comparing these dynamics with two abstracted models of stage-structured interactions revealed that while the quantitative details of the emergent dynamics depends on the shape of the interaction surface, the qualitative features — such as the emergence of single-generation cycles and rapid synchronization of development among individuals — are pleasingly robust.

Background: Malaria-infected mosquitoes have been reported to be more likely to take a blood meal when parasites are infectious than when non-infectious. This change in feeding behavior increases the likelihood of malaria transmission, and has been considered an example of parasite manipulation of host behavior. However, immune challenge with heat-killed Escherichia coli induces the same behavior, suggesting that altered feeding behavior may be driven by adaptive responses of hosts to cope with an immune response, rather than by parasite-specific factors. Here we tested the alternative hypothesis that down-regulated feeding behavior prior to infectiousness is a mosquito adaptation that increases fitness during infection. Methods: We measured the impact of immune challenge and blood feeding on the fitness of individual mosquitoes. After an initial blood meal, Anopheles stephensi Liston mosquitoes were experimentally challenged with heat-killed E. coli at a dose known to mimic the same temporal changes in mosquito feeding behavior as active malaria infection. We then tracked daily egg production and survivorship of females maintained on blood-feeding regimes that either mimicked down-regulated feeding behaviors observed during early malaria infection, or were fed on a four-day feeding cycle typically associated with uninfected mosquitoes. Results: Restricting access to blood meals enhanced mosquito survival but lowered lifetime reproduction. Immune- challenge did not impact either fitness component. Combining fecundity and survival to estimate the population- scale intrinsic rate of increase (r), we found that, contrary to the mosquito adaptation hypothesis, mosquito fitness decreased if blood feeding was delayed following an immune challenge. Conclusions: Our data provide no support for the idea that malaria-induced suppression of blood feeding is an adaptation by mosquitoes to reduce the impact of immune challenge. Alternatively, the behavioral alterations may be neither host nor parasite adaptations, but rather a consequence of constraints imposed on feeding by activation of the mosquito immune response, i.e. non-adaptive illness-induced anorexia. Future work incorporating field conditions and different immune challenges could further clarify the effect of altered feeding on mosquito and parasite fitness.

A major determinant of the rate at which drug-resistant malaria parasites spread through a population is the ecology of resistant and sensitive parasites sharing the same host. Drug treatment can significantly alter this ecology by removing the drug-sensitive parasites, leading to competitive release of resistant parasites. Here, we test the hypothesis that the spread of resistance can be slowed by reducing drug treatment and hence restricting competitive release. Using the rodent malaria model Plasmodium chabaudi, we found that low-dose chemotherapy did reduce competitive release. A higher drug dose regimen exerted stronger positive selection on resistant parasites for no detectable clinical gain. We estimated instantaneous selection coefficients throughout the course of replicate infections to analyze the temporal pattern of the strength and direction of within-host selection. The strength of selection on resistance varied through the course of infections, even in untreated infections, but increased immediately following drug treatment, particularly in the high-dose groups. Resistance remained under positive selection for much longer than expected from the half life of the drug. Although there are many differences between mice and people, our data do raise the question whether the aggressive treatment regimens aimed at complete parasite clearance are the best resistance-management strategies for humans.

Insect species often undergo regular outbreaks in population density, but identifying the causal mechanism for such outbreaks in any particular species has proven difficult. Here we show that outbreak cycles in the tea tortrix Adoxophyes honmai can be explained by temperature-driven changes in system stability. Wavelet analysis of a 51yr time series spanning over 200 outbreaks reveals a threshold in outbreak amplitude each spring when temperature exceeds 15°C, and a secession of outbreaks each fall as temperature decreases. This is in close agreement with our independently parameterized mathematical model that predicts the system crosses a Hopf bifurcation from stability to sustained cycles as temperature increases. These results suggest that temperature can alter system stability and provide an explanation for generation cycles in multivoltine insects.

Malaria infections normally consist of more than one clonally-replicating lineage. Within-host interactions between sensitive and resistant parasites can have profound effects on the evolution of drug resistance. Here, using the Plasmodium chabaudi mouse malaria model, we ask whether the costs and benefits of resistance are affected by the number of co-infecting strains competing with a resistant clone. We found strong competitive suppression of resistant parasites in untreated infections and marked competitive release following treatment. The magnitude of competitive suppression depended on competitor identity. However, there was no overall effect of the diversity of susceptible parasites on the extent of competitive suppression or release. If these findings generalize, then transmission intensity will impact on resistance evolution because of its effect on the frequency of mixed infections, not because of its effect on the distribution of clones per host. This would greatly simplify the computational problems of adequately capturing within-host ecology in models of drug resistance evolution in malaria.