Eleanore D. Sternberg

Food plant derived disease tolerance and resistance in a natural butterfly-plant-parasite interactions.

Organisms can protect themselves against parasite‐induced fitness costs through resistance or tolerance. Resistance includes mechanisms that prevent infection or limit parasite growth while tolerance alleviates the fitness costs from parasitism without limiting infection. Although tolerance and resistance affect host–parasite coevolution in fundamentally different ways, tolerance has often been ignored in animal–parasite systems. Where it has been studied, tolerance has been assumed to be a genetic mechanism, unaffected by the host environment. Here we studied the effects of host ecology on tolerance and resistance to infection by rearing monarch butterflies on 12 different species of milkweed food plants and infecting them with a naturally occurring protozoan parasite. Our results show that monarch butterflies experience different levels of tolerance to parasitism depending on the species of milkweed that they feed on, with some species providing over twofold greater tolerance than other milkweed species. Resistance was also affected by milkweed species, but there was no relationship between milkweed‐conferred resistance and tolerance. Chemical analysis suggests that infected monarchs obtain highest fitness when reared on milkweeds with an intermediate concentration, diversity, and polarity of toxic secondary plant chemicals known as cardenolides. Our results demonstrate that environmental factors—such as interacting species in ecological food webs—are important drivers of disease tolerance.

Local adaptation to temperature and the implications for vector-borne diseases

Vector life-history traits and parasite development respond in strongly nonlinear ways to changes in temperature. These thermal sensitivities create the potential for climate change to have a marked impact on disease transmission. To date, most research considering impacts of climate change on vector-borne diseases assumes that all populations of a given parasite or vector species respond similarly to temperature, regardless of their source population. This may be an inappropriate assumption because spatial variation in selective pressures such as temperature can lead to local adaptation. We examine evidence for local adaptation in disease vectors and present conceptual models for understanding how local adaptation might modulate the effects of both short- and long-term changes in climate.

Lack of genetic differentiation between monarch butterflies with divergent migration destinations

Monarch butterflies are best known for their spectacular annual migration from eastern North America to Mexico. Monarchs also occur in the North American states west of the Rocky Mountains, from where they fly shorter distances to the California Coast. Whether eastern and western North American monarchs form one genetic population or are genetically differentiated remains hotly debated, and resolution of this debate is essential to understand monarch migration patterns and to protect this iconic insect species. We studied the genetic structure of North American migratory monarch populations, as well as nonmigratory populations in Hawaii and New Zealand. Our results show that eastern and western migratory monarchs form one admixed population and that monarchs from Hawaii and New Zealand have genetically diverged from North American butterflies. These findings suggest that eastern and western monarch butterflies maintain their divergent migrations despite genetic mixing. The finding that eastern and western monarchs form one genetic population also suggests that the conservation of overwintering sites in Mexico is crucial for the protection of monarchs in both eastern and western North America.

Eave tubes for malaria control in Africa: an introduction

In spite of massive progress in the control of African malaria since the turn of the century, there is a clear and recognized need for additional tools beyond long-lasting insecticide-treated bed nets (LLINs) and indoor residual spraying (IRS) of insecticides, to progress towards elimination. Moreover, widespread and intensifying insecticide resistance requires alternative control agents and delivery systems to enable development of effective insecticide resistance management strategies. This series of articles presents a novel concept for malaria vector control, the ‘eave tube’, which may fulfil these important criteria. From its conceptualization to laboratory and semi-field testing, to demonstration of potential for implementation, the stepwise development of this new vector control approach is described. These studies suggest eave tubes (which comprise a novel way of delivering insecticides plus screening to make the house more ‘mosquito proof’) could be a viable, cost-effective, and acceptable control tool for endophilic and endophagic anophelines, and possibly other (nuisance) mosquitoes. The approach could be applicable in a wide variety of housing in sub-Saharan Africa, and possibly beyond, for vectors that use the eave as their primary house entry point. The results presented in these articles were generated during an EU-FP7 funded project, the mosquito contamination device (MCD) project, which ran between 2012 and 2015. This was a collaborative project undertaken by vector biologists, product developers, modellers, materials scientists, and entrepreneurs from five different countries.

Patterns of Host-Parasite Adaptation in Three Populations of Monarch Butterflies Infected with a Naturally Occurring Protozoan Disease: Virulence, Resistance, and Tolerance

Many studies have used host-parasite systems to study local adaptation, but few of these studies have found unequivocal evidence for adaptation. One potential reason is that most studies have focused on limited measures of host and parasite fitness that are generally assumed to be under negative frequency-dependent selection. We have used reciprocal cross-infection experiments to test for local adaptation in Hawaiian, south Floridian, and eastern North American populations of monarch butterflies and their protozoan parasites. Sympatric host-parasite combinations did not result in greater host or parasite fitness, as would be expected under coevolutionary dynamics driven by negative frequency-dependent selection. Instead, we found that Hawaiian hosts were more resistant and carried more infective and virulent parasites, which is consistent with theoretical predictions for virulence evolution and coevolutionary arms race dynamics. We also found that Hawaiian hosts were more tolerant, particularly of Hawaiian parasites, indicating that increased resistance does not preclude increased tolerance within a population and that hosts may be more tolerant of local parasites. We did not find a similar pattern in the south Floridian or eastern populations, possibly because host-parasite adaptation occurs within the context of a greater ecological community.

Malaria transmission potential could be reduced with current and future climate change

Several studies suggest the potential for climate change to increase malaria incidence in cooler, marginal transmission environments. However, the effect of increasing temperature in warmer regions where conditions currently support endemic transmission has received less attention. We investigate how increases in temperature from optimal conditions (27 °C to 30 °C and 33 °C) interact with realistic diurnal temperature ranges (DTR: ± 0 °C, 3 °C, and 4.5 °C) to affect the ability of key vector species from Africa and Asia (Anopheles gambiae and An. stephensi) to transmit the human malaria parasite, Plasmodium falciparum. The effects of increasing temperature and DTR on parasite prevalence, parasite intensity, and mosquito mortality decreased overall vectorial capacity for both mosquito species. Increases of 3 °C from 27 °C reduced vectorial capacity by 51–89% depending on species and DTR, with increases in DTR alone potentially halving transmission. At 33 °C, transmission potential was further reduced for An. stephensi and blocked completely in An. gambiae. These results suggest that small shifts in temperature could play a substantial role in malaria transmission dynamics, yet few empirical or modeling studies consider such effects. They further suggest that rather than increase risk, current and future warming could reduce transmission potential in existing high transmission settings.

Priorities for Broadening the Malaria Vector Control Tool Kit

Long-lasting insecticidal nets (LLINs) and indoor residual spraying (IRS) have contributed substantially to reductions in the burden of malaria in the past 15 years. Building on this foundation, the goal is now to drive malaria towards elimination. Vector control remains central to this goal, but there are limitations to what is achievable with the current tools. Here we highlight how a broader appreciation of adult mosquito behavior is yielding a number of supplementary approaches to bolster the vector-control tool kit. We emphasize tools that offer new modes of control and could realistically contribute to operational control in the next 5 years. Promoting complementary tools that are close to field-ready is a priority for achieving the global malaria-control targets.

A virulent parasite can provide protection against a lethal parasitoid.

Hosts often become infected with multiple parasite strains or species. Previous work has shown that the outcome of infections with multiple parasite strains or species often differs significantly from that of single infections, making them a potentially important factor in determining the prevalence and spread of disease. Here we show that infection with a virulent parasite increases host survival during later exposure to a lethal parasitoid. Specifically, when monarch butterfly larvae (Danaus plexippus) are inoculated with the virulent protozoan parasite Ophryocystis elektroscirrha and then attacked by the lethal parasitoid fly Lespesia archippivora, survival is higher than when the larvae are exposed to the parasitoid only. This is potentially a result of the protozoans requirement for host survival to obtain between-host transmission. Our findings suggest that a virulent parasite can play a protective role for its host and indicate that parasites can act as mutualists depending on the presence of other parasites. We emphasize the importance of considering infection in an ecological context, including the presence of competing parasites.

Trans-generational parasite protection associated with paternal diet.

Multiple generations of hosts are often exposed to the same pathogens, favouring the evolution of trans-generational defences. Because females have more opportunities to transfer protective molecules to offspring, many studies have focused on maternally derived protection. However, males of many species can transfer compounds along with sperm, including chemicals that could provide protection. Here, we assess maternally and paternally derived protection in a monarch butterfly-protozoan parasite system where parasite resistance is heavily influenced by secondary plant chemicals, known as cardenolides, present in the larval diet of milkweed plants. We reared monarch butterflies on medicinal and non-medicinal milkweed species and then measured resistance of their offspring to infection. We also measured cardenolide content in adult monarchs reared on the two species, and in the eggs that they produced. We found that offspring were more resistant to infection when their fathers were reared on medicinal milkweed, while maternal diet had less of an effect. We also found that eggs contained the highest levels of cardenolides when both parents were reared on the medicinal species. Moreover, females reared on non-medicinal milkweed produced eggs with significantly higher levels of cardenolides if they mated with males reared on the medicinal milkweed species. However, we found an equivocal relationship between the cardenolides present in eggs and parasite resistance in the offspring. Our results demonstrate that males reared on medicinal plants can transfer protection to their offspring, but the exact mechanism remains unresolved. This suggests that paternal protection from parasitism might be important, particularly when there are environmental sources of parasite resistance and when males transfer spermatophores during mating.

Insights from agriculture for the management of insecticide resistance in disease vectors

Key to contemporary management of diseases such as malaria, dengue, and filariasis is control of the insect vectors responsible for transmission. Insecticide‐based interventions have contributed to declines in disease burdens in many areas, but this progress could be threatened by the emergence of insecticide resistance in vector populations. Insecticide resistance is likewise a major concern in agriculture, where insect pests can cause substantial yield losses. Here, we explore overlaps between understanding and managing insecticide resistance in agriculture and in public health. We have used the Global Plan for Insecticide Resistance Management in malaria vectors, developed under the auspices of the World Health Organization Global Malaria Program, as a framework for this exploration because it serves as one of the few cohesive documents for managing a global insecticide resistance crisis. Generally, this comparison highlights some fundamental differences between insect control in agriculture and in public health. Moreover, we emphasize that the success of insecticide resistance management strategies is strongly dependent on the biological specifics of each system. We suggest that the biological, operational, and regulatory differences between agriculture and public health limit the wholesale transfer of knowledge and practices from one system to the other. Nonetheless, there are some valuable insights from agriculture that could assist in advancing the existing Global Plan for Insecticide Resistance Management framework.