Punch in the gut: Parasite tolerance of phytochemicals reflects host diet

Gut parasites of plant-eating insects are exposed to antimicrobial phytochemicals that can reduce infection. Trypanosomatid gut parasites infect insects of diverse nutritional ecologies as well as mammals and plants, raising the question of how host diet-associated phytochemicals shape parasite evolution and host specificity. To test the hypothesis that phytochemical tolerance of trypanosomatids reflects the chemical ecology of their hosts, we compared related parasites from honey bees and mosquitoes- hosts that differ in phytochemical consumption- and contrasted our results with previous studies on phylogenetically related, human-parasitic Leishmania. We identified one bacterial and ten plant-derived substances with known antileishmanial activity that also inhibited honey bee parasites associated with colony collapse. Bee parasites exhibited greater tolerance of chrysin- a flavonoid found in nectar, pollen, and plant resin-derived propolis. In contrast, mosquito parasites were more tolerant of cinnamic acid- a product of lignin decomposition present in woody debris-rich larval habitats. Parasites from both hosts tolerated many compounds that inhibit Leishmania, hinting at possible trade-offs between phytochemical tolerance and mammalian infection. Our results implicate the phytochemistry of host diets as a potential driver of insect-trypanosomatid associations, and identify compounds that could be incorporated into colony diets or floral landscapes to ameliorate infection in bees.

The neuroethology of avian brood parasitism

ABSTRACT Obligate brood-parasitic birds never build nests, incubate eggs or supply nestlings with food or protection. Instead, they leave their eggs in nests of other species and rely on host parents to raise their offspring, which allows the parasite to continue reproducing throughout the breeding season. Although this may be a clever fitness strategy, it is loaded with a set of dynamic challenges for brood parasites, including recognizing individuals from their own species while growing up constantly surrounded by unrelated individuals, remembering the location of potential host nests for successful reproduction and learning the song of their species while spending time being entirely surrounded by another species during a critical developmental period, a predicament that has been likened to being ‘raised by wolves’. Here, I will describe what we currently know about the neurobiology associated with the challenges of being a brood parasite and what is known about the proximate mechanisms of brood parasite evolution. The neuroethology of five behaviors (mostly social) in brood parasites is discussed, including: (1) parental care (or the lack thereof), (2) species recognition, (3) song learning, (4) spatial memory and (5) pair-bonding and mate choice. This Review highlights how studies of brood parasites can lend a unique perspective to enduring neuroethological questions and describes the ways in which studying brood-parasitic species enhances our understanding of ecologically relevant behaviors.

Elucidating relationships between P.falciparum prevalence and measures of genetic diversity with a combined genetic-epidemiological model of malaria

There is an abundance of malaria genetic data being collected from the field, yet using these data to understand the drivers of regional epidemiology remains a challenge. A key issue is the lack of models that relate parasite genetic diversity to epidemiological parameters. Classical models in population genetics characterize changes in genetic diversity in relation to demographic parameters, but fail to account for the unique features of the malaria life cycle. In contrast, epidemiological models, such as the Ross-Macdonald model, capture malaria transmission dynamics but do not consider genetics. Here, we have developed an integrated model encompassing both parasite evolution and regional epidemiology. We achieve this by combining the Ross-Macdonald model with an intra-host continuous-time Moran model, thus explicitly representing the evolution of individual parasite genomes in a traditional epidemiological framework. Implemented as a stochastic simulation, we use the model to explore relationships between measures of parasite genetic diversity and parasite prevalence, a widely-used metric of transmission intensity. First, we explore how varying parasite prevalence influences genetic diversity at equilibrium. We find that multiple genetic diversity statistics are correlated with prevalence, but the strength of the relationships depends on whether variation in prevalence is driven by host- or vector-related factors. Next, we assess the responsiveness of a variety of statistics to malaria control interventions, finding that those related to mixed infections respond quickly (∼months) whereas other statistics, such as nucleotide diversity, may take decades to respond. These findings provide insights into the opportunities and challenges associated with using genetic data to monitor malaria epidemiology.

Determinants of haemosporidian single and co-infections risks in western paleartic birds

Co-infections with multiple pathogens are common in the wild and may act as a strong selective pressure on both host and parasite evolution. Yet, contrary to single infection, the factors that shape co-infection risk are largely under-investigated. Here, we explored the extent to which bird ecology and phylogeny impact single and co-infection probabilities by haemosporidian parasites using large datasets from museum collections and a Bayesian phylogenetic modelling framework. While both phylogeny and species attributes (e.g. size of the geographic range, life-history strategy, migration) were relevant predictors of co-infection risk, these factors were less pertinent in predicting the probability of being single infected. Our study suggests that co-infection risk is under a stronger deterministic control than single-infection risk. These results underscore the combined influence of host evolutionary history and species attributes in determining single and co-infection pattern providing new avenues regarding our ability to predict infection risk in the wild.

Hidden paths to endless forms most wonderful: parasite-blind diversification of host quality

Evolutionary diversification can occur in allopatry or sympatry, can be driven by selection or unselected, and can be phenotypically manifested immediately or remain latent until manifested in a newly encountered environment. Diversification of host–parasite interactions is frequently studied in the context of intrinsically selective coevolution, but the potential for host–parasite interaction phenotypes to diversify latently during parasite-blind host evolution is rarely considered. Here, we use a social bacterium experimentally adapted to several environments in the absence of phage to analyse allopatric diversification of host quality—the degree to which a host population supports a viral epidemic. Phage-blind evolution reduced host quality overall, with some bacteria becoming completely resistant to growth suppression by phage. Selective-environment differences generated only mild divergence in host quality. However, selective environments nonetheless played a major role in shaping evolution by determining the degree of stochastic diversification among replicate populations within treatments. Ancestral motility genotype was also found to strongly shape patterns of latent host-quality evolution and diversification. These outcomes show that (i) adaptive landscapes can differ in how they constrain stochastic diversification of a latent phenotype and (ii) major effects of selection on biological diversification can be missed by focusing on trait means. Collectively, our findings suggest that latent-phenotype evolution should inform host–parasite evolution theory and that diversification should be conceived broadly to include latent phenotypes.

Hidden paths to endless forms most wonderful: Parasite-blind diversification of host quality

Evolutionary diversification can occur in allopatry or sympatry, can be unselected or driven by selection, and can be phenotypically manifested immediately or remain phenotypically latent until later manifestation in a newly encountered environment. Diversification of host-parasite interactions is frequently studied in the context of intrinsically selective coevolution, but the potential for host-parasite interaction phenotypes to diversify latently during parasite-blind evolution is rarely considered. Here we use a social bacterium experimentally adapted to several environments in the absence of phage to analyse allopatric diversification of latent host quality - the degree to which a host population supports a viral epidemic. Phage-blind evolution reduced host quality overall, with some bacteria becoming completely resistant to growth suppression by phage. Selective-environment differences generated only mild divergence in host-quality. However, selective environments nonetheless played a major role in shaping evolution by determining the degree of stochastic diversification among replicate populations within treatments. Ancestral motility genotype was also found to strongly shape patterns of latent hostquality evolution and diversification. These outcomes show that adaptive landscapes can differ in how they constrain stochastic diversification of a latent phenotype and that major effects of selection on biological diversification can be missed by focusing on trait means. Collectively, our findings suggest that latent-phenotype evolution (LPE) should inform host-parasite evolution theory and that diversification should be conceived broadly to include latent phenotypes.

Social information use shapes the coevolution of sociality and virulence

Social contacts can facilitate the spread of both survival-related information and infectious disease, but little is known about how these processes combine to shape host and parasite evolution. Here, we use a theoretical model that captures both transmission processes to investigate how host sociality and parasite virulence (co)evolve. We show how selection for sociality (and in turn, virulence) depends on both the intrinsic costs and benefits of information and disease as well as their relative prevalence in the population. Specifically, greater sociality and lower virulence evolve when the risk of infection is either low or high and information is neither very common nor too rare. Lower sociality and higher virulence evolve when the prevalence patterns are reversed. When disease and information are both at moderate levels, the direction of selection depends on the relative costs and benefits of being infected or informed. We also show that sociality varies inversely with virulence, and that disease may be unable to constrain the evolution of sociality. Together, these findings provide new insights for our understanding of group living and how apparently opposing ecological processes can influence the evolution of sociality and virulence in a range of ways.