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      Ecology and evolution of pathogens in natural populations of Lepidoptera

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          Abstract

          Pathogens are ubiquitous in insect populations and yet few studies examine their dynamics and impacts on host populations. We discuss four lepidopteran systems and explore their contributions to disease ecology and evolution. More specifically, we elucidate the role of pathogens in insect population dynamics. For three species, western tent caterpillars, African armyworm and introduced populations of gypsy moth, infection by nucleopolyhedrovirus ( NPV) clearly regulates host populations or reduces their outbreaks. Transmission of NPV is largely horizontal although low levels of vertical transmission occur, and high levels of covert infection in some cases suggest that the virus can persist in a nonsymptomatic form. The prevalence of a mostly vertically transmitted protozoan parasite, Ophryocystis elektroscirrha , in monarch butterflies is intimately related to their migratory behaviour that culls highly infected individuals. Virulence and transmission are positively related among genotypes of this parasite. These systems clearly demonstrate that the interactions between insects and pathogens are highly context dependent. Not only is the outcome a consequence of changes in density and genetic diversity: environmental factors, particularly diet, can have strong impacts on virulence, transmission and host resistance or tolerance. What maintains the high level of host and pathogen diversity in these systems, however, remains a question.

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          Unravelling the annual cycle in a migratory animal: breeding-season habitat loss drives population declines of monarch butterflies.

          Threats to migratory animals can occur at multiple periods of the annual cycle that are separated by thousands of kilometres and span international borders. Populations of the iconic monarch butterfly (Danaus plexippus) of eastern North America have declined over the last 21 years. Three hypotheses have been posed to explain the decline: habitat loss on the overwintering grounds in Mexico, habitat loss on the breeding grounds in the United States and Canada, and extreme weather events. Our objectives were to assess population viability, determine which life stage, season and geographical region are contributing the most to population dynamics and test the three hypotheses that explain the observed population decline. We developed a spatially structured, stochastic and density-dependent periodic projection matrix model that integrates patterns of migratory connectivity and demographic vital rates across the annual cycle. We used perturbation analysis to determine the sensitivity of population abundance to changes in vital rate among life stages, seasons and geographical regions. Next, we compared the singular effects of each threat to the full model where all factors operate concurrently. Finally, we generated predictions to assess the risk of host plant loss as a result of genetically modified crops on current and future monarch butterfly population size and extinction probability. Our year-round population model predicted population declines of 14% and a quasi-extinction probability ( 5% within a century. Monarch abundance was more than four times more sensitive to perturbations of vital rates on the breeding grounds than on the wintering grounds. Simulations that considered only forest loss or climate change in Mexico predicted higher population sizes compared to milkweed declines on the breeding grounds. Our model predictions also suggest that mitigating the negative effects of genetically modified crops results in higher population size and lower extinction risk. Recent population declines stem from reduction in milkweed host plants in the United States that arise from increasing adoption of genetically modified crops and land-use change, not from climate change or degradation of forest habitats in Mexico. Therefore, reducing the negative effects of host plant loss on the breeding grounds is the top conservation priority to slow or halt future population declines of monarch butterflies in North America.
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            Plant-mediated effects in insect-pathogen interactions.

            Interactions between insect herbivores and their pathogens can be modulated by host plants. Inter- and intraspecific differences in plant chemistry and structure can alter the susceptibility of insects to infection and the production and environmental persistence of pathogens. Whether plants can manipulate insect pathogens to act as "bodyguards" and increase their own fitness remains to be shown. Reduced insect performance owing to poor plant quality can enhance the susceptibility of an insect to disease while these same phytochemicals can also reduce the effectiveness of entomopathogens in killing the host. As we discuss here, plants have an important role in the evolution of insect-pathogen relationships and a tritrophic perspective should thus be incorporated into the study of insects and their pathogens.
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              Monarch butterfly migration and parasite transmission in eastern North America

              Seasonal migration occurs in many animal systems and is likely to influence interactions between animals and their parasites. Here, we focus on monarch butterflies (Danaus plexippus) and a protozoan parasite (Ophryocystis elektroscirrha) to investigate how host migration affects infectious disease processes. Previous work showed that parasite prevalence was lower among migratory than nonmigratory monarch populations; two explanations for this pattern are that (1) migration allows animals to periodically escape contaminated habitats (i.e., migratory escape), and (2) long‐distance migration weeds out infected animals (i.e., migratory culling). We combined field‐sampling and analysis of citizen science data to examine spatiotemporal trends of parasite prevalence and evaluate evidence for these two mechanisms. Analysis of within‐breeding‐season variation in eastern North America showed that parasite prevalence increased from early to late in the breeding season, consistent with the hypothesis of migratory escape. Prevalence was also positively related to monarch breeding activity, as indexed by larval density. Among adult monarchs captured at different points along the east coast fall migratory flyway, parasite prevalence declined as monarchs progressed southward, consistent with the hypothesis of migratory culling. Parasite prevalence was also lower among monarchs sampled at two overwintering sites in Mexico than among monarchs sampled during the summer breeding period. Collectively, these results indicate that seasonal migration can affect parasite transmission in wild animal populations, with implications for predicting disease risks for species with threatened migrations.
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                Author and article information

                Journal
                Evol Appl
                Evol Appl
                10.1111/(ISSN)1752-4571
                EVA
                Evolutionary Applications
                John Wiley and Sons Inc. (Hoboken )
                1752-4571
                23 November 2015
                January 2016
                : 9
                : 1 , Women's contribution to basic and applied evolutionary biology ( doiID: 10.1111/eva.2016.9.issue-1 )
                : 231-247
                Affiliations
                [ 1 ] Department of ZoologyUniversity of British Columbia Vancouver BCCanada
                [ 2 ] Department of Biological SciencesSimon Fraser University Burnaby BCCanada
                Author notes
                [*] [* ] Correspondence

                Judith H. Myers, Department of Zoology, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada.

                Tel.: +1‐604‐2243438;

                fax: +1‐604‐8222416;

                e‐mails: myers@ 123456zoology.ubc.ca , jsc21@ 123456sfu.ca

                Article
                EVA12328
                10.1111/eva.12328
                4780379
                27087850
                eea4aa49-3453-4057-a189-afeaff5f4395
                © 2015 The Authors. Evolutionary Applications published by John Wiley & Sons Ltd

                This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

                History
                : 06 March 2015
                : 19 August 2015
                Page count
                Pages: 17
                Funding
                Funded by: Natural Sciences and Engineering Research Council of Canada
                Funded by: Natural Environment Research Council
                Funded by: United Kingdom Department for International Development (DFID)
                Categories
                Review and Syntheses
                Review and Syntheses
                Custom metadata
                2.0
                eva12328
                January 2016
                Converter:WILEY_ML3GV2_TO_NLMPMC version:4.8.4 mode:remove_FC converted:07.03.2016

                Evolutionary Biology
                disease ecology,disease transmission,forest lepidoptera,insect pathogens,migration,population regulation,tritrophic interactions,virulence

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