Trade-offs and mixed infections in an obligate-killing insect pathogen

Abstract

Natural populations of pathogens are frequently composed of numerous interacting strains. Understanding what maintains this diversity remains a key focus of research in disease ecology. In addition, within-host pathogen dynamics can have a strong impact on both infection outcome and the evolution of pathogen virulence, and thus, understanding the impact of pathogen diversity is important for disease management. We compared eight genetically distinguishable variants from Spodoptera exempta nucleopolyhedrovirus (SpexNPV) isolated from the African armyworm, Spodoptera exempta. NPVs are obligate killers, and the vast majority of transmission stages are not released until after the host has died. The NPV variants differed significantly in their virulence and could be clustered into two groups based on their dose-response curves. They also differed in their speed of kill and productivity (transmission potential) for S. exempta. The mixed-genotype wild-type (WT) SpexNPV, from which each variant was isolated, was significantly more virulent than any individual variant and its mean mortality rate was within the fastest group of individual variants. However, the WT virus produced fewer new infectious stages than any single variant, which might reflect competition among the variants. A survival analysis, combining the mortality and speed of kill data, confirmed the superiority of the genetically mixed WT virus over any single variant. Spodoptera exempta larvae infected with WT SpexNPV were predicted to die 2·7 and 1·9 times faster than insects infected with isolates from either of the two clusters of genotypes. Theory suggests that there are likely to be trade-offs between pathogen fitness traits. Across all larvae, there was a negative linear relationship between virus yield and speed of kill, such that more rapid host death carried the cost of producing fewer transmission stages. We also found a near-significant relationship for the same trend at the intervariant level. However, there was no evidence for a significant relationship between the induced level of mortality and transmission potential (virus yield) or speed of kill.

Keywords: dose-response; entomopathogen; infection diversity; mortality rate; polymorphism; transmission potential; virulence.

Figure 1

Infection traits for each Spodoptera exempta NPV variant (A–H) and the parent wild type (WT). (a) Lethal dose (LD)50s ± standard errors (SEs). (b) Speed of kill (1/infection duration (±SEs), averaged over all virus doses to make it comparable with (a) and (c). Sample size ranged from 209 to 319 individuals per genotype. (c) Mean yield (±SE). Sample size ranged from 19 to 22 individuals per genotype. The black dots represent the wild‐type virus; the white (Group I) and grey (Group II) dots represent the two groups of viruses that can be distinguished in terms of their mortality rate (see text for details).

Figure 2

Kaplan–Meier survival curves for individual SpexNPV genotypes (A–H) in comparison with the wild‐type (WT) virus. Each curve shows the fitted values from the survival model standardized for a viral inoculation dose of 1000 OBs. Dotted lines = group I variants (A, C, E and F), and dotted lines = group II variants (B, D, G and H) and the solid line = WT virus.

Figure 3

Yield speed of kill trade‐offs for individual SpexNPV genotypes and the wild‐type virus at the (a) intragenotype level (genotype A , B , C , D , E , F , G , H and WT ) and (b) intergenotype level. In (b), mean speed of kill was estimated only using larvae for which virus yield data were also available.