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      Understanding the Evolutionary Ecology of host–pathogen Interactions Provides Insights into the Outcomes of Insect Pest Biocontrol

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          Abstract

          The use of viral pathogens to control the population size of pest insects has produced both successful and unsuccessful outcomes. Here, we investigate whether those biocontrol successes and failures can be explained by key ecological and evolutionary processes between hosts and pathogens. Specifically, we examine how heterogeneity in pathogen transmission, ecological and evolutionary tradeoffs, and pathogen diversity affect insect population density and thus successful control. We first review the existing literature and then use numerical simulations of mathematical models to further explore these processes. Our results show that the control of insect densities using viruses depends strongly on the heterogeneity of virus transmission among insects. Overall, increased heterogeneity of transmission reduces the effect of viruses on insect densities and increases the long-term stability of insect populations. Lower equilibrium insect densities occur when transmission is heritable and when there is a tradeoff between mean transmission and insect fecundity compared to when the heterogeneity of transmission arises from non-genetic sources. Thus, the heterogeneity of transmission is a key parameter that regulates the long-term population dynamics of insects and their pathogens. We also show that both heterogeneity of transmission and life-history tradeoffs modulate characteristics of population dynamics such as the frequency and intensity of “boom–bust" population cycles. Furthermore, we show that because of life-history tradeoffs affecting the transmission rate, the use of multiple pathogen strains is more effective than the use of a single strain to control insect densities only when the pathogen strains differ considerably in their transmission characteristics. By quantifying the effects of ecology and evolution on population densities, we are able to offer recommendations to assess the long-term effects of classical biocontrol.

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          How should pathogen transmission be modelled?

          Host-pathogen models are essential for designing strategies for managing disease threats to humans, wild animals and domestic animals. The behaviour of these models is greatly affected by the way in which transmission between infected and susceptible hosts is modelled. Since host-pathogen models were first developed at the beginning of the 20th century, the 'mass action' assumption has almost always been used for transmission. Recently, however, it has been suggested that mass action has often been modelled wrongly. Alternative models of transmission are beginning to appear, as are empirical tests of transmission dynamics.
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            Insect pathogens as biological control agents: Back to the future.

            The development and use of entomopathogens as classical, conservation and augmentative biological control agents have included a number of successes and some setbacks in the past 1years. In this forum paper we present current information on development, use and future directions of insect-specific viruses, bacteria, fungi and nematodes as components of integrated pest management strategies for control of arthropod pests of crops, forests, urban habitats, and insects of medical and veterinary importance. Insect pathogenic viruses are a fruitful source of microbial control agents (MCAs), particularly for the control of lepidopteran pests. Most research is focused on the baculoviruses, important pathogens of some globally important pests for which control has become difficult due to either pesticide resistance or pressure to reduce pesticide residues. Baculoviruses are accepted as safe, readily mass produced, highly pathogenic and easily formulated and applied control agents. New baculovirus products are appearing in many countries and gaining an increased market share. However, the absence of a practical in vitro mass production system, generally higher production costs, limited post application persistence, slow rate of kill and high host specificity currently contribute to restricted use in pest control. Overcoming these limitations are key research areas for which progress could open up use of insect viruses to much larger markets. A small number of entomopathogenic bacteria have been commercially developed for control of insect pests. These include several Bacillus thuringiensis sub-species, Lysinibacillus (Bacillus) sphaericus, Paenibacillus spp. and Serratia entomophila. B. thuringiensis sub-species kurstaki is the most widely used for control of pest insects of crops and forests, and B. thuringiensis sub-species israelensis and L. sphaericus are the primary pathogens used for control of medically important pests including dipteran vectors. These pathogens combine the advantages of chemical pesticides and MCAs: they are fast acting, easy to produce at a relatively low cost, easy to formulate, have a long shelf life and allow delivery using conventional application equipment and systemics (i.e. in transgenic plants). Unlike broad spectrum chemical pesticides, B. thuringiensis toxins are selective and negative environmental impact is very limited. Of the several commercially produced MCAs, B. thuringiensis (Bt) has more than 50% of market share. Extensive research, particularly on the molecular mode of action of Bt toxins, has been conducted over the past two decades. The Bt genes used in insect-resistant transgenic crops belong to the Cry and vegetative insecticidal protein families of toxins. Bt has been highly efficacious in pest management of corn and cotton, drastically reducing the amount of broad spectrum chemical insecticides used while being safe for consumers and non-target organisms. Despite successes, the adoption of Bt crops has not been without controversy. Although there is a lack of scientific evidence regarding their detrimental effects, this controversy has created the widespread perception in some quarters that Bt crops are dangerous for the environment. In addition to discovery of more efficacious isolates and toxins, an increase in the use of Bt products and transgenes will rely on innovations in formulation, better delivery systems and ultimately, wider public acceptance of transgenic plants expressing insect-specific Bt toxins. Fungi are ubiquitous natural entomopathogens that often cause epizootics in host insects and possess many desirable traits that favor their development as MCAs. Presently, commercialized microbial pesticides based on entomopathogenic fungi largely occupy niche markets. A variety of molecular tools and technologies have recently allowed reclassification of numerous species based on phylogeny, as well as matching anamorphs (asexual forms) and teleomorphs (sexual forms) of several entomopathogenic taxa in the Phylum Ascomycota. Although these fungi have been traditionally regarded exclusively as pathogens of arthropods, recent studies have demonstrated that they occupy a great diversity of ecological niches. Entomopathogenic fungi are now known to be plant endophytes, plant disease antagonists, rhizosphere colonizers, and plant growth promoters. These newly understood attributes provide possibilities to use fungi in multiple roles. In addition to arthropod pest control, some fungal species could simultaneously suppress plant pathogens and plant parasitic nematodes as well as promote plant growth. A greater understanding of fungal ecology is needed to define their roles in nature and evaluate their limitations in biological control. More efficient mass production, formulation and delivery systems must be devised to supply an ever increasing market. More testing under field conditions is required to identify effects of biotic and abiotic factors on efficacy and persistence. Lastly, greater attention must be paid to their use within integrated pest management programs; in particular, strategies that incorporate fungi in combination with arthropod predators and parasitoids need to be defined to ensure compatibility and maximize efficacy. Entomopathogenic nematodes (EPNs) in the genera Steinernema and Heterorhabditis are potent MCAs. Substantial progress in research and application of EPNs has been made in the past decade. The number of target pests shown to be susceptible to EPNs has continued to increase. Advancements in this regard primarily have been made in soil habitats where EPNs are shielded from environmental extremes, but progress has also been made in use of nematodes in above-ground habitats owing to the development of improved protective formulations. Progress has also resulted from advancements in nematode production technology using both in vivo and in vitro systems; novel application methods such as distribution of infected host cadavers; and nematode strain improvement via enhancement and stabilization of beneficial traits. Innovative research has also yielded insights into the fundamentals of EPN biology including major advances in genomics, nematode-bacterial symbiont interactions, ecological relationships, and foraging behavior. Additional research is needed to leverage these basic findings toward direct improvements in microbial control.
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              Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster.

              The extent to which an organism is selected to invest in defences against pathogens and parasites depends on the advantages that ensue should infection occur, but also on the costs of maintaining defences in the absence of infection. The presence of heritable variation in resistance suggests that costs exist, but we know very little about the nature or magnitude of these costs in natural populations of animals. A powerful technique for identifying trade-offs between fitness components is the study of correlated responses to artificial selection. We have selected Drosophila melanogaster for improved resistance against an endoparasitoid, Asobara tabida. Endoparasitoids are insects whose larvae develop internally within the body of other insects, eventually killing them, although their hosts can sometimes survive attack by mounting a cellular immune response. We found that reduced larval competitive ability in unparasitized D. melanogaster is a correlated response to artificial selection for improved resistance against A. tabida. The strength of selection for competitive ability and parasitoid resistance is likely to vary temporally and spatially, which may explain the observed heritable variation in resistance.
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                Author and article information

                Journal
                Viruses
                Viruses
                viruses
                Viruses
                MDPI
                1999-4915
                25 January 2020
                February 2020
                : 12
                : 2
                : 141
                Affiliations
                [1 ]School of Aquatic and Fishery Sciences, The University of Washington, 1122 NE Boat St, Box 355020, Seattle, WA 98195, USA
                [2 ]Department of Biology, University of San Diego, 5998 Alcala Park, San Diego, CA 92110, USA
                Author notes
                [* ]Correspondence: dpaezmc@ 123456gmail.com (D.J.P.); arietta.flemingdavies@ 123456gmail.com (A.E.F.-D.)
                [†]

                These authors contributed equally to this work.

                Author information
                https://orcid.org/0000-0003-1609-7014
                Article
                viruses-12-00141
                10.3390/v12020141
                7077243
                31991772
                f8490dc1-7792-4c05-a4d0-69deddde41d7
                © 2020 by the authors.

                Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license ( http://creativecommons.org/licenses/by/4.0/).

                History
                : 10 December 2019
                : 17 January 2020
                Categories
                Article

                Microbiology & Virology
                transmission,heterogeneity,tradeoffs,fecundity,genetic variation,insect pathogens,population dynamics

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