Revenge of the host: cannibalism, ontogenetic niche shifts, and the evolution of life-history strategies in host-parasitoid systems

Question: How does cannibalism in the host alter the evolution of a parasitoid’s oviposition strategy? Can differences in cannibalism risk between parasitized and healthy hosts alter the stage-specific foraging of parasitoids? Can host-specific differences in cannibalistic behaviour explain why parasitoids vary in what host stages they attack? Mathematical methods: We examined the evolutionary dynamics of a stage-structured host–parasitoid model using two complementary approaches: (1) individual-based numerical simulations of evolutionary dynamics, and (2) the theory of adaptive dynamics focusing on evolutionarily stable strategies (ESSs). Assumptions: Cannibalism in the host is assumed to be stage structured, with larger stages consuming smaller stages. The consumption of parasitized hosts also results in killing of the parasitoid’s offspring. Vulnerability to cannibalism of parasitized versus healthy hosts was allowed to vary. The parasitoid’s preference for attacking early versus late host stages was the trait under selection and allowed to evolve. Results: When cannibalism rates increase relative to the parasitoid’s attack rates, the ESS of the parasitoid shifts from attacking only early host stages to attacking only late host stages. This shift occurs at lower cannibalism rates when parasitized hosts are more susceptible to cannibalism than healthy hosts. Under equilibrium conditions, a small boundary area exists between these two regions where attacking only early or only late host stages are alternative ESSs. The threshold and alternative stable ESSs are the result of cannibalism, which creates a positive feedback between the parasitoid’s oviposition rate and its own mortality. Intermediate strategies, where parasitoids evolve to attack both stages, occur only when host populations exhibit large population oscillations or when generalist parasitoids that attack both stages have a foraging advantag

Cannibalism and infectious disease: Friends or foes?

© 2017 by The University of Chicago. Cannibalism occurs in a majority of both carnivorous and noncarnivorous animal taxa from invertebrates to mammals. Similarly, infectious parasites are ubiquitous in nature. Thus, interactions between cannibalism and disease occur regularly. While some adaptive benefits of cannibalism are clear, the prevailing view is that the risk of parasite transmission due to cannibalism would increase disease spread and, thus, limit the evolutionary extent of cannibalism throughout the animal kingdom. In contrast, surprisingly little attention has been paid to the other half of the interaction between cannibalism and disease, that is, how cannibalism affects parasites. Here we examine the interaction between cannibalism and parasites and show howadvances across independent lines of research suggest that cannibalism can also reduce the prevalence of parasites and, thus, infection risk for cannibals. Cannibalism does this by both directly killing parasites in infected victims and by reducing the number of susceptible hosts, often enhanced by the stage-structured nature of cannibalism and infection. While the well-established view that disease should limit cannibalism has held sway, we present theory and examples from a synthesis of the literature showing how cannibalism may also limit disease and highlight key areas where conceptual and empirical work is needed to resolve this debate

Opportunities for behavioral rescue under rapid environmental change

Laboratory measurements of physiological and demographic tolerances are important in understanding the impact of climate change on species diversity; however, it has been recognized that forecasts based solely on these laboratory estimates overestimate risk by omitting the capacity for species to utilize microclimatic variation via behavioral adjustments in activity patterns or habitat choice. The complex, and often context‐dependent nature, of microclimate utilization has been an impediment to the advancement of general predictive models. Here, we overcome this impediment and estimate the potential impact of warming on the fitness of ectotherms using a benefit/cost trade‐off derived from the simple and broadly documented thermal performance curve and a generalized cost function. Our framework reveals that, for certain environments, the cost of behavioral thermoregulation can be reduced as warming occurs, enabling behavioral buffering (e.g., the capacity for behavior to ameliorate detrimental impacts) and “behavioral rescue” from extinction in extreme cases. By applying our framework to operative temperature and physiological data collected at an extremely fine spatial scale in an African lizard, we show that new behavioral opportunities may emerge. Finally, we explore large‐scale geographic differences in the impact of behavior on climate‐impact projections using a global dataset of 38 insect species. These multiple lines of inference indicate that understanding the existing relationship between thermal characteristics (e.g., spatial configuration, spatial heterogeneity, and modal temperature) is essential for improving estimates of extinction risk

Large expert-curated database for benchmarking document similarity detection in biomedical literature search

Document recommendation systems for locating relevant literature have mostly relied on methods developed a decade ago. This is largely due to the lack of a large offline gold-standard benchmark of relevant documents that cover a variety of research fields such that newly developed literature search techniques can be compared, improved and translated into practice. To overcome this bottleneck, we have established the RElevant LIterature SearcH consortium consisting of more than 1500 scientists from 84 countries, who have collectively annotated the relevance of over 180 000 PubMed-listed articles with regard to their respective seed (input) article/s. The majority of annotations were contributed by highly experienced, original authors of the seed articles. The collected data cover 76% of all unique PubMed Medical Subject Headings descriptors. No systematic biases were observed across different experience levels, research fields or time spent on annotations. More importantly, annotations of the same document pairs contributed by different scientists were highly concordant. We further show that the three representative baseline methods used to generate recommended articles for evaluation (Okapi Best Matching 25, Term Frequency-Inverse Document Frequency and PubMed Related Articles) had similar overall performances. Additionally, we found that these methods each tend to produce distinct collections of recommended articles, suggesting that a hybrid method may be required to completely capture all relevant articles. The established database server located at https://relishdb.ict.griffith.edu.au is freely available for the downloading of annotation data and the blind testing of new methods. We expect that this benchmark will be useful for stimulating the development of new powerful techniques for title and title/abstract-based search engines for relevant articles in biomedical research.Peer reviewe

Integrated analysis of environmental and genetic influences on cord blood DNA methylation in new-borns

Epigenetic processes, including DNA methylation (DNAm), are among the mechanisms allowing integration of genetic and environmental factors to shape cellular function. While many studies have investigated either environmental or genetic contributions to DNAm, few have assessed their integrated effects. Here we examine the relative contributions of prenatal environmental factors and genotype on DNA methylation in neonatal blood at variably methylated regions (VMRs) in 4 independent cohorts (overall n = 2365). We use Akaike’s information criterion to test which factors best explain variability of methylation in the cohort-specific VMRs: several prenatal environmental factors (E), genotypes in cis (G), or their additive (G + E) or interaction (GxE) effects. Genetic and environmental factors in combination best explain DNAm at the majority of VMRs. The CpGs best explained by either G, G + E or GxE are functionally distinct. The enrichment of genetic variants from GxE models in GWAS for complex disorders supports their importance for disease risk

Data from: Non-linear effects of phenological shifts link inter-annual variation to species interactions

1. The vast majority of species interactions are seasonally structured and depend on species’ relative phenologies. However, differences in the phenologies of species naturally vary across years and are altered by ongoing climate change around the world. 2. By combining experiments that shifted the relative hatching of two competing tadpole species across a productivity gradient with simulations of inter-annual variation in arrival times I tested how phenological variation across years can alter the strength and outcome of interspecific competition. 3. Shifting the relative timing of hatching (phenology) of a species fundamentally altered interspecific competition, and the effect of shifting the timing on competition was highly non-linear for most demographic rates. Furthemore, this relationship varied with productivity of the system. As a consequence, (i) shifts in relative timing of phenologies had small or large effects depending on the average natural timing of interactions, and (ii) changes in the inter-annual variation in onset of interaction alone can alter species interactions in simulations even when mean phenologies (timing) remain unchanged across years. 4. Traditionally, studies on phenologies focus on directional shifts in the mean of phenologies, but our results suggest that we also need to consider inter-annual variation in phenologies of interacting species to predict dynamics of natural communities and how they will be modified by climate change

Data from: Legacy effects of developmental stages determine the functional role of predators

Predators are instrumental in structuring natural communities and ecosystem processes. The strong effects of predators are often attributed to their high trophic position in the food web. However, most predators have to grow and move up the food chain before reaching their final trophic position and during this developmental process, their traits, interactions, and abundances change. Here we show that this process of “moving up” the food chain during development strongly determines the ecological role of a predator. By experimentally manipulating the succession of developmental stages of a predatory salamander in seasonal aquatic ecosystem, we found that effects of this apex predator on the ecosystem typically declined with age and size. Furthermore, younger, smaller predator stages had long-lasting effects on community structure and ecosystem function that determined effects of subsequent older, larger stages. Consequently, legacy effects of early stages largely shaped the impact of the predator on the ecosystem, which could not simply be inferred from its final trophic position. Our results highlight that accounting for all life stages when managing natural populations is crucial to preserve functioning of natural ecosystems, especially given that early life stages of species are often particularly vulnerable to natural and anthropogenic disturbances

Data from: Ghosts of habitats past: environmental carry-over effects drive population dynamics in novel habitat

The phenotype of adults can be strongly influenced by the environmental conditions experienced during development. Consequently, variation in habitat quality across space and through time also leads to differences in the phenotypes of adults. This could create carry-over effects where differences in the natal habitat quality of colonizers influence population dynamics in new habitats. We tested this hypothesis experimentally by simulating dispersal of Tribolium castaneum from low or high quality natal habitat into new patches of low or high quality habitat. Differences in natal habitat quality of colonizers altered population growth trajectories and led to carrying capacities that differed by up to 85% within a habitat type, indicating that patch dynamics are determined by the interaction of past and current habitat quality. Interestingly, even after multiple generations, natal habitat of colonizers determined differences in adult traits that were related to density-dependent population regulation. These changes in adult phenotype could at least partially explain why carry-over effects continued to alter population dynamics for multiple generations until the end of the experiment. These results highlight the importance of variable habitat quality and carry-over effects for population dynamics

Data from: Within-host priority effects systematically alter pathogen coexistence

Coinfection of host populations alters pathogen prevalence, host mortality, and pathogen evolution. Because pathogens compete for limiting resources, whether multiple pathogens can coexist in a host population can depend on their within-host interactions which, in turn, can depend on the order in which pathogens infect hosts (within-host priority effects). However, the consequences of within-host priority effects for pathogen coexistence have not been tested. Using laboratory studies with a coinfected zooplankton system, we found that pathogens had increased fitness in coinfected hosts when they were the second pathogen to infect a host, compared to when they were the first pathogen to infect a host. With these results, we parameterized a pathogen coexistence model with priority effects, finding that pathogen coexistence (1) decreased when priority effects increased the fitness of the first pathogen to arrive in coinfected hosts, and (2) increased when priority effects increased the fitness of the second pathogen to arrive in coinfected hosts. We also identified the natural conditions under which we expect within-host priority effects to foster coexistence in our system. These outcomes were the result of positive or negative frequency dependence created by feedback loops between pathogen prevalence and infection order in coinfected hosts. This suggests that priority effects can systematically alter conditions for pathogen coexistence in host populations, thereby changing pathogen community structure and potentially altering host mortality and pathogen evolution via emergent processes

Data from: Drivers of individual niche variation in coexisting species

1. Although neglected by classic niche theory, individual variation is now recognized as a prevalent phenomenon in nature with evolutionary and ecological relevance. Recent theory suggests that differences in individual variation across competitors can affect species coexistence and community patterns. However, the degree of individual variation is flexible across wild populations and we still know little about the ecological drivers of this variation across populations of single species and, especially, across coexisting species. 2. Here we aimed to (i) elucidate the major drivers of individual niche variation in natural communities and (ii) to determine how consistent this variation is across coexisting species and communities. 3. We analyzed natural patterns of individual-level niche variation in four species of coexisting generalist frogs across a wide range of tropical communities. Specifically, we used gut contents and stable isotopes (δ13C and δ15N) from frog species and their prey to quantify individual niche specialization. Then we combined data on local community structure, availability of prey, phylogenetic relationships, and predator-prey size models to test how this variation is related to four ecological factors which are predicted to be key drivers of individual specialization: intraspecific competition, interspecific competition, ecological opportunity (i.e., diversity of resources), and predation. 4. We found that the degree of individual trophic specialization varied by up to nine-fold across populations within the same species. This sizable variation in trophic specialization across populations was at least partially explained by gradients of density of competitors (both conspecifics and heterospecifics) and intraguild predation. However, the specific relationships between individual specialization and these ecological gradients were strongly species-specific. As consequences, the identity of the species with more individual variation changed among sites and there was typically no spatial correlation in the degree of individual specialization across co-existing species. 5. Our results show that individual niche specialization within and across species can be strongly context-dependent and that hierarchies of individual variation among coexisting species are not necessarily consistent across communities. Recent theory suggests that this pattern could lead to concurrent changes in competitive interactions across sites and thereby could play a key role in species coexistence at the landscape level. Our results suggest that individual variation across and within coexisting species has the potential to affect not only species coexistence at local communities, but also regional diversity patterns