Context-dependent effects of a cryptic virus on butterfly population dynamics.

Viruses have the potential to impact host populations, but our picture of host-virus relationships is largely colored by virulent pathogens that lead to easily detectable epizootic events. Modern molecular methods have demonstrated that viruses are ubiquitous in animal populations, and the influence of these "cryptic" viruses is largely unexplored. Insects provide an ideal system to examine population-level impacts of novel, "cryptic" viruses-short generation times allow for meaningful population-level field studies over a relatively short timeframe, and their abundance and small size facilitate experimental manipulation across each life stage. Many insect species are capable of high population growth rates, potentially buffering them from pathogen-driven declines in the face of high pathogen prevalence. We explored the impacts of a recently detected non-occluded densovirus (Junonia coenia DV, JcDV) on the demography of a nymphalid butterfly, Euphydryas phaeton (Baltimore checkerspot). E. phaeton populations are known to have the capacity for rapid growth and to exhibit large, often unexplained population fluctuations. We used a field mesocosm experiment to measure the vital rates of E. phaeton under a range of levels of viral exposure over 2 years (2021 and 2022) and used these vital rates to parameterize a demographic model of population growth in each year. We found that JcDV reduced E. phaeton post-diapause larval survival, skewed sex ratios toward a male bias, and reduced fecundity in surviving females. JcDV reduced estimated population growth rates in both years, but only led to population decline in 2022. This increased impact was associated with a substantial regional drought, suggesting that the potential for this non-occluded virus to cause population decline is influenced by climatic factors. The findings of our controlled study parallel trends observed in a wild population of E. phaeton, supporting the hypothesis that JcDV can drive population decline. This study demonstrates that cryptic viruses likely influence butterfly population dynamics, especially when their effects are compounded with additional environmental stressors.