Test of the invasive pathogen hypothesis of bumble bee decline in North America

Abstract

Emergent fungal diseases are critical factors in global biodiversity declines. The fungal pathogen Nosema bombi was recently found to be widespread in declining species of North American bumble bees (Bombus), with circumstantial evidence suggesting an exotic introduction from Europe. This interpretation has been hampered by a lack of knowledge of global genetic variation, geographic origin, and changing prevalence patterns of N. bombi in declining North American populations. Thus, the temporal and spatial emergence of N. bombi and its potential role in bumble bee decline remain speculative. We analyze Nosema prevalence and genetic variation in the United States and Europe from 1980, before an alleged introduction in the early 1990s, to 2011, extracting Nosema DNA from Bombus natural history collection specimens from across this time period. Nosema bombi prevalence increased significantly from low detectable frequency in the 1980s to significantly higher frequency in the mid- to late-1990s, corresponding to a period of reported massive infectious outbreak of N. bombi in commercial bumble bee rearing stocks in North America. Despite the increased frequency, we find no conclusive evidence of an exotic N. bombi origin based on genetic analysis of global Nosema populations; the widespread Nosema strain found currently in declining United States bumble bees was present in the United States before commercial colony trade. Notably, the US N. bombi is not detectably different from that found predominantly throughout Western Europe, with both regions characterized by low genetic diversity compared with high levels of diversity found in Asia, where commercial bee breeding activities are low or nonexistent.