The first steps toward a global pandemic: Reconstructing the demographic history of parasite host switches in its native range

Abstract

Host switching allows parasites to expand their niches. However, successful switching may require suites of adaptations and may decrease performance on the old host. As a result, reductions in gene flow accompany many host switches, driving speciation. Because host switches tend to be rapid, it is difficult to study them in real time and their demographic parameters remain poorly understood. As a result, fundamental factors that control subsequent parasite evolution, such as the size of the switching population or the extent of immigration from the original host, remain largely unknown. To shed light on the host switching process, we explored how host switches occur in independent host shifts by two ectoparasitic honey bee mites (Varroa destructor and V. jacobsoni). Both switched to the western honey bee (Apis mellifera) after it was brought into contact with their ancestral host (Apis cerana), ~70 and ~12 years ago, respectively. Varroa destructor subsequently caused worldwide collapses of honey bee populations. Using whole-genome sequencing on 44 mites collected in their native ranges from both the ancestral and novel hosts, we were able to reconstruct the known temporal dynamics of the switch. We further found that hundreds of haploid genomes were involved in the initial host switch, and, despite being greatly reduced, some gene flow remains between mites adapted to different hosts remains. Our findings suggest that while reproductive isolation may facilitate fixation of traits beneficial for exploitation of the new host, ongoing genetic exchange may allow genetic amelioration of inbreeding effects.

Reproduction of ectoparasitic mites in a coevolved system: Varroa spp.—Eastern honey bees, Apis cerana

“…In brood cells hosting more than one foundress, male and female offspring of two or more mother mites can mate, thereby allowing for recombination (Beaurepaire et al., 2017) and contributing to the high genetic diversity of these populations (Dietemann et al., 2019; Z Lin, S Wang, P Neumann, G Chen, P Page, L Li, F Hu, H Zheng & V Dietemann, unpublished data). Multiple infestations can lead to hybridization between sympatric mite taxa, which are identified with increasing frequency and can affect the population structure and virulence of this parasite (e.g., Dietemann et al., 2019; Techer et al., 2020; Z Lin, S Wang, P Neumann, G Chen, P Page, L Li, F Hu, H Zheng & V Dietemann, unpublished data; H Zheng, S Wang, Y Wu, S Zou, V Dietemann, P Neumann, Y Chen, H Li‐Byarlay, C Pirk, J Evans, F Hu & Y Feng, unpublished data).…”

Evolutionarily diverse origins of honey bee deformed wing viruses

“…Our study illustrates the dynamic interaction between virus, vector and host. Although the original host switch of V. destrucor took place in the mid-20th century, (co-)evolutionary dynamics continue in this system with the acquisition of novel viruses and novel vectors (14, 15). Our findings raise interesting questions about how viruses interact with both varroa and host gene expression, and how viruses evolve to increase their fitness on novel hosts (see for example (21)).…”

“…However, that changed in the 19th century when beekeepers took western honey bees to Asia where they came in contact with eastern honey bees and Varroa mites, which are obligate parasites of honey bee brood. By the mid-20th century, Varroa destructor switched to its novel honey bee host ( A. mellifera ), followed by Varroa jacobsoni in the early 21st century (11, 14, 15). V. destructor then spread worldwide, transmitting a wide variety of bee viruses and causing global population collapses of western honey bees (12).…”

Varroa mites escape the evolutionary trap of haplodiploidy

“…DNA extraction, library preparation, and sequencing Genomic DNA was extracted from each single mite following the protocol described previously (22). In brief, after surface sterilization using absolute ethanol, each mite was crushed in a 1.5 mL microcentrifuge tube dipped in liquid nitrogen.…”

“…In addition, Varroa is believed to be haplodiploid, which further reduces the effective population size (20,21). Despite the above, the mite shows high adaptability: it efficiently switches between host species (22)(23)(24), and can rapidly evolve resistance to pesticides via various mechanisms (25). While a high level of adaptability explains the mite's successful global spread, the mechanisms underlying this adaptability remain puzzling in the light of regular genetic bottlenecks, routine inbreeding, and male haploidy.…”