Short Communication
Exploring sub-lethal effects of exposure to a nucleopolyhedrovirus in the speckled wood (Pararge aegeria) butterfly

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Abstract

This study investigated the sub-lethal effects of larval exposure to baculovirus on host life history and wing morphological traits using a model system, the speckled wood butterfly Pararge aegeria (L.) and the virus Autographa californica nucleopolyhedrovirus. Males and females showed similar responses to the viral infection. Infection significantly reduced larval growth rate, whilst an increase in development time allowed the critical mass for pupation to be attained. There was no direct effect of viral infection on the wing morphological traits examined. There was, however, an indirect effect of resisting infection; larvae that took longer to develop had reduced resource investment in adult flight muscle mass.

Graphical abstract

Development time of speckled wood (Pararge aegeria) butterfly larvae increased in a concentration-dependent manner when inoculated in laboratory bioassays with Autographa californica nucleopolyhedrovirus. There was no apparent negative impact of sub-lethal infection with baculovirus on wing morphology measurements but larval development was prolonged.

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Highlights

Pararge aegeria were semi-permissive to infection with AcMNPV in the laboratory. ► Sublethal viral infection significantly increased larval development time. ► Reduced thorax mass in adults corresponded with longer larval development time. ► No significant effect of virus on other life history or wing morphology traits.

Introduction

The cost to an insect host of surviving a sub-lethal pathogen infection may be measured through changes in different fitness traits (Zuk and Stoehr, 2002). This has implications for designing effective biological control strategies and for understanding the role of pathogens in regulating natural populations of insects (Hesketh et al., 2010, Roy et al., 2009). Therefore, increasing attention is being focused on the contribution of immune defence to adult fitness in insect systems (Schmid-Hempel, 2005). We have investigated the consequences of overcoming a viral infection on life history and wing morphological traits in the speckled wood butterfly Pararge aegeria (L.). This species has been used extensively as a model system for studies of insect ecology and life history evolution (e.g. Van Dyck and Wiklund, 2002). Although sub-lethal effects of baculovirus infection on life history traits in Lepidoptera have been well recorded (e.g. Goulson and Cory, 1995, Sood et al., 2010, Sporleder et al., 2007), effects on wing development and morphology are less well considered; changes related to baculovirus infection have been crudely quantified through measurements of wing deformities (e.g. Milks, 1997, Vail and Hall, 1969). Any potential change to wing formation that could affect flight and/or dispersal ability will be particularly important to recognise in species such as P. aegeria that have experienced shifts in distribution and dispersal in response to climate change and habitat fragmentation over the last few decades (e.g. Hill et al., 1999, Gibbs and Van Dyck, 2010).

We specifically selected flight morphology traits commonly used in butterfly studies and known to be correlated to flight performance in P. aegeria (Berwaerts et al., 1998, Hill et al., 1999). We hypothesised that a concentration-dependent response against infection in the larval stage with Autographa californica multiple capsid nucleopolyhedrovirus (AcMNPV) would reduce investment in morphological traits associated with flight. To test this hypothesis, we examined changes in P. aegeria larval, pupal and adult development traits as well as sex differences in response to sub-lethal infection with baculovirus.

Section snippets

Bioassay

A stock of AcMNPV was obtained as described in Gibbs et al. (2010a) and the concentration of occlusion bodies was estimated by counting three times in an improved Neubauer haemocytometer at magnification 400× (<10% error in counts). Larvae starved overnight were inoculated individually in Petri dishes (5 cm diameter) containing a piece of damp filter paper and 5 × 1 cm pieces of Poa trivialis (L.) leaf with 1 μl of viral inoculum (concentration of virus between 1 × 103 and 1 × 109 occlusion bodies ml−1)

Results and discussion

Pararge aegeria was susceptible to infection with AcMNPV at the two highest viral concentrations (see Bishop et al., 1995 for comparative susceptibility of other Lepidoptera to AcMNPV). Mean viral mortality was greater at 1 × 109 OB’s ml−1 (46.3%) compared to 1 × 108 OB’s ml−1 (21.8%) and larvae died significantly more quickly at the higher concentration (days to death post-inoculation; F1,34 = 4.53, p = 0.041). There was no viral mortality in control insects.

Generally, adult females had significantly

Acknowledgments

HH & RSH are supported by the Natural Environment Research Council (NERC) and the Centre for Ecology & Hydrology (CEH) Environmental Change Integrating Fund. ET was supported by CEH and York University on a placement studentship at CEH. MG was supported by funding to HVD (FRFC research Grant 2.4595.07 of the Fund of Scientific Research FRS-FNRS and FSR06 grant of the Université catholique de Louvain, UCL) and a mobility grant to MG within the framework of this FRFC research project. This is

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