Ecology and evolution of pathogens in natural populations of Lepidoptera

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.

Keywords: disease ecology; disease transmission; forest Lepidoptera; insect pathogens; migration; population regulation; tritrophic interactions; virulence.

Figure 1

Transmission of baculoviruses can be horizontal among individuals through environmental contamination, or vertical from parents to offspring on or in the eggs. Upon death of an infected larva, occlusion bodies are released and other larvae become infected if they ingest the occlusion bodies on contaminated foliage. Vertical transmission can occur if larvae consume occlusion bodies (small yellow dots) but pupate before death leading to sublethally infected adults (indicated by larger yellow dot). Adults sublethally infected as larvae might transmit virus to their offspring either on or in the eggs. This can lead to an active infection killing the offspring or potentially a covert infection that is passed on to offspring that will survive.

Figure 2

Change in numbers of tents (bars) for a western tent caterpillar population on Galiano Island, BC and the per cent families containing virus‐killed larvae (line) since 1990. The populations were too low in 2007 and 2008 to determine levels of infection.

Figure 3

The relationship between the rate of population change [R] from 1 year to the next in one population of western tent caterpillars monitored on Galiano Island, and the level of infection for each year measured by the per cent of families with at least one NPV‐infected larva between the years 1991 and 2014 (J. H. Myers and J. S. Cory unpublished data).

Figure 4

Top – the relationship between mean number of eggs per egg mass (fecundity) and numbers of tent caterpillar tents on Galiano Island. Bars are numbers of tents and circles are mean eggs per egg mass. Hatched bars indicate years of high viral infection. Bottom – the relationship between moth fecundity (mean number of eggs per egg mass) and the per cent families with viral infection for each year on Galiano Island.

Figure 5

Top – The annual sum of the number of territories recording larval infestations of S. exempta in East Africa from 1940 to 1984. Data summarized from Haggis (1986). Bottom – Number of years with recorded outbreaks of S. exempta in Tanzania summed on a monthly basis for 1930 to 1999 (from table 1 in Rose et al. (2000).

Figure 6

Gypsy moth populations monitored annually as the area defoliated in north‐eastern USA by the US Forest Service Northeastern Area (http://www.na.fs.fed.us/fhp/gm/cfm_files/dsp/dsp_defchart.cfm). Arrow indicates the year when mortality from fungus was first observed.

Figure 7

The neogregarine parasite of monarch butterflies reproduces in the larvae. Adults developing from infected larvae are contaminated by spores on their bodies, particularly their abdomens, following emergence from the pupa. The parasite is transferred vertically from adult females to their eggs or larval feeding sites at oviposition. At hatching, larvae ingest spores that reproduce through the larval stage (indicated by white dots above), and then form spores that contaminate adults at emergence. Adults arising from infected larvae can be smaller and have reduced longevity compared to healthy individuals. Horizontal transmission will occur if spores are ingested by larvae that are not offspring of the ovipositing female. Transmission from males to offspring is low.

Figure 8

Top. Monarch populations are estimated over time by the area of overwintering butterfly colonies (data from Vidal and Rendón‐Salinas 2014). Bottom. Total counts of butterflies made in driving censuses at Cape May NJ (circles – data from Davis 2012) and the proportion of individuals with high spore loads (squares) recorded for Eastern migratory populations by Altizer et al. (2000).