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The First Steps Toward a Global Pandemic: Reconstructing The The first steps toward a global pandemic: Reconstructing the demographic history of parasite host switches in its native range Ma´eva Techer1, John Roberts2, Reed Cartwright3, and Alexander Mikheyev1 1Okinawa Institute of Science and Technology Graduate University 2Commonwealth Scientific and Industrial Research Organisation 3Arizona State University August 25, 2021 Abstract Host switching allows parasites to expand their niches. However, successful switching may require suites of adaptations and also 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 their demographic parameters in real-time. 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 the history of independent switches 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 63 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 multiple previously undiscovered mitochondrial lineages on the novel host, along with the genetic equivalent of tens of individuals that were involved in the initial host switch. Despite being greatly reduced, some gene flow remains between mites adapted to different hosts. Our findings suggest that while reproductive isolation may facilitate the fixation of traits beneficial for exploitation of the new host, ongoing genetic exchange may allow genetic amelioration of inbreeding effects. Hosted file Draft_MolEcol_July2021.docx available at https://authorea.com/users/351631/articles/535233- the-first-steps-toward-a-global-pandemic-reconstructing-the-demographic-history-of- parasite-host-switches-in-its-native-range Hosted file mec-228320.pdf available at https://authorea.com/users/351631/articles/535233-the-first- steps-toward-a-global-pandemic-reconstructing-the-demographic-history-of-parasite-host- switches-in-its-native-range Hosted file Figure1_HQ.pdf available at https://authorea.com/users/351631/articles/535233-the-first- steps-toward-a-global-pandemic-reconstructing-the-demographic-history-of-parasite-host- switches-in-its-native-range Posted on Authorea 25 Aug 2021 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.162990851.12719028/v1 | This a preprint and has not been peer reviewed. Data may be preliminary. 1 Genomic mtDNA Host V. destructor ancestry lineage species A B PC2 Viet Nam V1 Nepal 2 China C1 China C3 0.2 China C4 Viet Nam V1 A. cerana Japan J1 China C1 0.0 PC1 * Japan J1 * Korean K1 Korean K1 −0.2 A. mellifera Nepal 2 Korean K1 −0.4 China C3 China C4 −0.1 0.0 0.1 0.2 0.3 0% 50% 100% V. jacobsoni C D Laos 1 Papua Laos 1 North Thailand 4 PC2 New Guinea 1 0.00 Bengaluru 1 Bengalaru 1 Malaysia 2 PC1 A. cerana Java 1 Malaysia 2 Lombok 2 −0.25 Java 1 PNG 1 −0.50 PNG 1 −0.75 A. mellifera * North Thailand 4 Lombok 2 −0.3 −0.2 −0.1 0.0 0.1 Java 1 A. nigrocincta 0% 50% 100% Past (generations) A B Past (generations) 1000 156 haploid mites 138 haploid mites 887 [866-906] Founding [146-165] [126-151] event 183 [179-183] 200 710 [693-726] Founding Bottleneck event end 170 [165-175] 500 100 0.0003 0.0161 Migration Migration rate rate 0.0001 0.0295 Sampling date 17,166 29,659 17,376 5,220 Sampling date haploid mites haploid mites haploid mites haploid mites [16,598-17,731] [28,722-30,666] [16,589-18,144] [4,787-5,683] Original host Novel host Original host Novel host A. cerana A. mellifera A. cerana A. mellifera XXX Mean estimate value [XXX-XXX] 95% confidence interval Posted on Authorea 25 Aug 2021 | The copyright holder is the author/funder. All rights reserved. No reuse without permission. | https://doi.org/10.22541/au.162990851.12719028/v1 | This a preprint and has not been peer reviewed. Data may be preliminary. 2.
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