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The extent to which honey bee-virus relationships change after<jats:italic>Varroa<\/jats:italic>invasion is poorly understood for most viruses, in part because there are few places in the world with several geographically close but completely isolated honey bee populations that either have, or have not, been exposed long-term to<jats:italic>Varroa<\/jats:italic>, allowing for separate ecological, epidemiological, and adaptive relationships to develop between honey bees and their viruses, in relation to the mite\u2019s presence or absence. The Azores is one such place, as it contains islands with and without the mite. Here, we combined qPCR with meta-amplicon deep sequencing to uncover the relationship between<jats:italic>Varroa<\/jats:italic>presence, and the prevalence, load, diversity, and phylogeographic structure of eight honey bee viruses screened across the archipelago. Four viruses were not detected on any island (ABPV-Acute bee paralysis virus, KBV-Kashmir bee virus, IAPV-Israeli acute bee paralysis virus, BeeMLV-Bee macula-like virus); one (SBV-Sacbrood virus) was detected only on mite-infested islands; one (CBPV-Chronic bee paralysis virus) occurred on some islands, and two (BQCV-Black queen cell virus, LSV-Lake Sinai virus,) were present on every single island. This multi-virus screening builds upon a parallel survey of Deformed wing virus (DWV) strains that uncovered a remarkably heterogeneous viral landscape featuring<jats:italic>Varroa<\/jats:italic>-infested islands dominated by DWV-A and -B,<jats:italic>Varroa<\/jats:italic>-free islands na\u00efve to DWV, and a refuge of the rare DWV-C dominating the easternmost<jats:italic>Varroa<\/jats:italic>-free islands. While all four detected viruses investigated here were affected by<jats:italic>Varroa<\/jats:italic>for one or two parameters (usually prevalence and\/or the Richness component of ASV diversity), the strongest effect was observed for the multi-strain LSV.<jats:italic>Varroa<\/jats:italic>unambiguously led to elevated prevalence, load, and diversity (Richness and Shannon Index) of LSV, with these results largely shaped by LSV-2, a major LSV strain. Unprecedented insights into the mite-virus relationship were further gained from implementing a phylogeographic approach. In addition to enabling the identification of a novel LSV strain that dominated the unique viral landscape of the easternmost islands, this approach, in combination with the recovered diversity patterns, strongly suggests that<jats:italic>Varroa<\/jats:italic>is driving the evolutionary change of LSV in the Azores. This study greatly advances the current understanding of the effect of<jats:italic>Varroa<\/jats:italic>on the epidemiology and adaptive evolution of these less-studied viruses, whose relationship with<jats:italic>Varroa<\/jats:italic>has thus far been poorly defined.<\/jats:p>","DOI":"10.1371\/journal.ppat.1012337","type":"journal-article","created":{"date-parts":[[2024,7,3]],"date-time":"2024-07-03T17:22:41Z","timestamp":1720027361000},"page":"e1012337","update-policy":"https:\/\/doi.org\/10.1371\/journal.ppat.corrections_policy","source":"Crossref","is-referenced-by-count":9,"title":["Varroa destructor shapes the unique viral landscapes of the honey bee populations of the Azores archipelago"],"prefix":"10.1371","volume":"20","author":[{"given":"Ana R.","family":"Lopes","sequence":"first","affiliation":[]},{"given":"Matthew","family":"Low","sequence":"additional","affiliation":[]},{"given":"Raquel","family":"Mart\u00edn-Hern\u00e1ndez","sequence":"additional","affiliation":[]},{"ORCID":"https:\/\/orcid.org\/0000-0002-0335-0386","authenticated-orcid":true,"given":"Joachim R.","family":"de Miranda","sequence":"additional","affiliation":[]},{"given":"M. Alice","family":"Pinto","sequence":"additional","affiliation":[]}],"member":"340","published-online":{"date-parts":[[2024,7,3]]},"reference":[{"issue":"1608","key":"ppat.1012337.ref001","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1098\/rspb.2006.3721","article-title":"Importance of pollinators in changing landscapes for world crops","volume":"274","author":"A-M Klein","year":"2007","journal-title":"Proc R Soc B Biol Sci"},{"issue":"3","key":"ppat.1012337.ref002","doi-asserted-by":"crossref","first-page":"810","DOI":"10.1016\/j.ecolecon.2008.06.014","article-title":"Economic valuation of the vulnerability of world agriculture confronted with pollinator decline","volume":"68","author":"N Gallai","year":"2009","journal-title":"Ecol Econ"},{"issue":"9","key":"ppat.1012337.ref003","doi-asserted-by":"crossref","first-page":"2034","DOI":"10.1111\/ele.14069","article-title":"Animal pollination increases stability of crop yield across spatial scales","volume":"25","author":"J 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of deformed wing virus","volume":"12","author":"JMK Roberts","year":"2020","journal-title":"Viruses"},{"issue":"2","key":"ppat.1012337.ref049","doi-asserted-by":"crossref","first-page":"289","DOI":"10.1099\/jgv.0.001206","article-title":"Occurrence of deformed wing virus variants in the stingless bee melipona subnitida and honey bee Apis mellifera populations in Brazil","volume":"100","author":"FS de Souza","year":"2019","journal-title":"J Gen Virol"},{"issue":"2","key":"ppat.1012337.ref050","doi-asserted-by":"crossref","first-page":"280","DOI":"10.1016\/j.virusres.2007.12.011","article-title":"Detection of Chronic bee paralysis virus (CBPV) genome and its replicative RNA form in various hosts and possible ways of spread","volume":"133","author":"O Celle","year":"2008","journal-title":"Virus Res"},{"issue":"6","key":"ppat.1012337.ref051","doi-asserted-by":"crossref","first-page":"969","DOI":"10.3390\/v13060969","article-title":"Ten years of Deformed wing virus (DWV) in Hawaiian honey 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Lett"},{"issue":"7","key":"ppat.1012337.ref057","doi-asserted-by":"crossref","first-page":"320","DOI":"10.3390\/vetsci9070320","article-title":"Colonisation patterns of Nosema ceranae in the Azores archipelago","volume":"9","author":"AR Lopes","year":"2022","journal-title":"Vet Sci"},{"issue":"8","key":"ppat.1012337.ref058","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1371\/journal.pone.0043562","article-title":"Pathogen webs in collapsing honey bee colonies","volume":"7","author":"RS Cornman","year":"2012","journal-title":"PLoS One"},{"issue":"1","key":"ppat.1012337.ref059","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1756-0500-7-649","article-title":"Holistic screening of collapsing honey bee colonies in Spain: a case study","volume":"7","author":"A Cepero","year":"2014","journal-title":"BMC research notes"},{"issue":"8","key":"ppat.1012337.ref060","doi-asserted-by":"crossref","first-page":"e0182814","DOI":"10.1371\/journal.pone.0182814","article-title":"Honey bee (Apis mellifera) colony health and pathogen composition in migratory beekeeping operations involved in California almond pollination","volume":"12","author":"W Glenny","year":"2017","journal-title":"PLoS One"},{"key":"ppat.1012337.ref061","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pone.0237544","article-title":"Longitudinal monitoring of honey bee colonies reveals dynamic nature of virus abundance and indicates a negative impact of Lake Sinai virus 2 on colony health","volume":"15","author":"C Faurot-Daniels","year":"2020","journal-title":"PLoS One"},{"issue":"5","key":"ppat.1012337.ref062","doi-asserted-by":"crossref","first-page":"1217","DOI":"10.3390\/v15051217","article-title":"Viral co-Infections and antiviral immunity in honey bees","volume":"15","author":"T 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