Abstract
The recent global decline in Western honeybee (Apis mellifera) populations is of great concern for pollination and honey production worldwide. Declining honeybee populations are frequently infected by the microsporidian pathogen Nosema ceranae. This species was originally described in the Asiatic honeybee (Apis cerana), and its identification in global A. mellifera hives could result from a recent host transfer. Recent genome studies have found that global populations of this parasite are polyploid and that humans may have fueled their global expansion. To better understand N. ceranae biology, we investigated its genetic diversity within part of their native range (Thailand) and among different hosts (A. mellifera, A. cerana) using both PCR and genome-based methods. We find that Thai N. ceranae populations share many SNPs with other global populations and appear to be clonal. However, in stark contrast with previous studies, we found that these populations also carry many SNPs not found elsewhere, indicating that these populations have evolved in their current geographic location for some time. Our genome analyses also indicate the potential presence of diploidy within Thai populations of N. ceranae.
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References
Nägeli KW (1857) Uber die neue Krankheit der Seidenraupe und verwandte Organismen. Bot Z 15:760–761
Corradi N (2015) Microsporidia: eukaryotic intracellular parasites shaped by gene loss and horizontal gene transfers. Annu Rev Microbiol 69:167–183. https://doi.org/10.1146/annurev-micro-091014-104136
Keeling PJ, Fast NM (2002) Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu Rev Microbiol 56:93–116. https://doi.org/10.1146/annurev.micro.56.012302.160854
Vávra J, Lukeš J (2013) Microsporidia and “the art of living together”. Adv Parasitol 82:253–319. https://doi.org/10.1016/B978-0-12-407706-5.00004-6
Williams BAP, Hirt RP, Lucocq JM, Embley TM (2002) A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865–869. https://doi.org/10.1038/nature00949
Vávra J, Larsson JIR (2014) Structure of microsporidia. In: Weiss LM, Becnel JJ (eds) Microsporidia: pathogens of opportunity, First. John Wiley & Sons, Inc., Chichester, pp 1–70
Corradi N, Slamovits CH (2011) The intriguing nature of microsporidian genomes. Brief Funct Genomics 10:115–124. https://doi.org/10.1093/bfgp/elq032
Franzen C (2004) Microsporidia: how can they invade other cells? Trends Parasitol 20:275–279. https://doi.org/10.1016/j.pt.2004.04.009
Xu Y, Weiss LM (2005) The microsporidian polar tube: a highly specialised invasion organelle. Int J Parasitol 35:941–953. https://doi.org/10.1016/j.ijpara.2005.04.003
Selman M, Pombert JF, Solter L, Farinelli L, Weiss LM, Keeling P, Corradi N (2011) Acquisition of an animal gene by microsporidian intracellular parasites. Curr Biol 21:R576-R577. https://doi.org/10.1016/j.cub.2011.06.017
Pombert J-F, Selman M, Burki F, Bardell FT, Farinelli L, Solter LF, Whitman DW, Weiss LM, Corradi N, Keeling PJ (2012) Gain and loss of multiple functionally related, horizontally transferred genes in the reduced genomes of two microsporidian parasites. Proc Natl Acad Sci 109:12638–12643. https://doi.org/10.1073/pnas.1205020109
James TY, Pelin A, Bonen L, Ahrendt S, Sain D, Corradi N, Stajich JE (2013) Shared signatures of parasitism and phylogenomics unite Cryptomycota and Microsporidia. Curr Biol 23:1548–1553. https://doi.org/10.1016/j.cub.2013.06.057
Quandt CA, Beaudet D, Corsaro D, Walochnik J, Michel R, Corradi N, James TY (2017) The genome of an intranuclear parasite, Paramicrosporidium saccamoebae, reveals alternative adaptations to obligate intracellular parasitism. Elife 6:1–19. https://doi.org/10.7554/eLife.29594
Corradi N, Pombert J-F, Farinelli L, Didier ES, Keeling PJ (2010) The complete sequence of the smallest known nuclear genome from the microsporidian Encephalitozoon intestinalis. Nat Commun 1:1–7. https://doi.org/10.1038/ncomms1082
Dowd SE, Gerba CP, Pepper IL (1998) Confirmation of the human-pathogenic Microsporidia Enterocytozoon bieneusi, Encephalitozoon intestinalis, and Vittaforma corneae in water. Appl Environ Microbiol 64:3332–3335
Gupta SK, Hossain Z, Nanu MM, Mondal K (2016) Impact of microsporidian infection on growth and development of silkworm Bombyx mori L. (Lepidoptera: Bombycidae). Agric Nat Resour 50:388–395. https://doi.org/10.1016/j.anres.2016.02.005
Fries I, Feng F, da Silva A, Slemenda SB, Pieniazek NJ (1996) Nosema ceranae n. sp. (Microspora, Nosematidae), morphological and molecular characterization of a microsporidian parasite of the Asian honey bee Apis cerana (Hymenoptera, Apidae). Eur J Protistol 32:356–365. https://doi.org/10.1016/S0932-4739(96)80059-9
Dussaubat C, Brunet J-L, Higes M, Colbourne JK, Lopez J, Choi JH, Martín-Hernández R, Botías C, Cousin M, McDonnell C, Bonnet M, Belzunces LP, Moritz RFA, le Conte Y, Alaux C (2012) Gut pathology and responses to the microsporidium Nosema ceranae in the honey bee Apis mellifera. PLoS One 7:e37017. https://doi.org/10.1371/journal.pone.0037017
Higes M, Meana A, Bartolomé C, Botías C, Martín-Hernández R (2013) Nosema ceranae (Microsporidia), a controversial 21st century honey bee pathogen. Environ Microbiol Rep 5:17–29. https://doi.org/10.1111/1758-2229.12024
Higes M, Martín-Hernández R, Botías C, Bailón EG, González-Porto AV, Barrios L, del Nozal MJ, Bernal JL, Jiménez JJ, Palencia PG, Meana A (2008) How natural infection by Nosema ceranae causes honeybee colony collapse. Environ Microbiol 10:2659–2669. https://doi.org/10.1111/j.1462-2920.2008.01687.x
Suwannapong G, Benbow ME, Nieh JC (2011) Biology of Thai honeybees: natural history and threats. Nova Science Publishers, Inc., New York
Kearns CA, Inouye DW, Waser NM (1998) Endangered mutualisms: the conservation of plant-pollinator interactions. Annu Rev Ecol Syst 29:83–112. https://doi.org/10.1146/annurev.ecolsys.29.1.83
VanEngelsdorp D, Meixner MD (2010) A historical review of managed honey bee populations in Europe and the United States and the factors that may affect them. J Invertebr Pathol 103:S80–S95. https://doi.org/10.1016/j.jip.2009.06.011
VanEngelsdorp D, Evans JD, Saegerman C et al (2009) Colony collapse disorder: a descriptive study. PLoS One 4:e6481. https://doi.org/10.1371/journal.pone.0006481
Chen Y, Evans JD, Zhou L, Boncristiani H, Kimura K, Xiao T, Litkowski AM, Pettis JS (2009) Asymmetrical coexistence of Nosema ceranae and Nosema apis in honey bees. J Invertebr Pathol 101:204–209. https://doi.org/10.1016/j.jip.2009.05.012
Botías C, Martín-Hernández R, Barrios L, Meana A, Higes M (2013) Nosema spp. infection and its negative effects on honey bees (Apis mellifera iberiensis) at the colony level. Vet Res 44:25. https://doi.org/10.1186/1297-9716-44-25
Martín-Hernández R, Botías C, Bailón EG, Martínez-Salvador A, Prieto L, Meana A, Higes M (2012) Microsporidia infecting Apis mellifera: coexistence or competition. Is Nosema ceranae replacing Nosema apis? Environ Microbiol 14:2127–2138. https://doi.org/10.1111/j.1462-2920.2011.02645.x
Klee J, Besana AM, Genersch E, Gisder S, Nanetti A, Tam DQ, Chinh TX, Puerta F, Ruz JM, Kryger P, Message D, Hatjina F, Korpela S, Fries I, Paxton RJ (2007) Widespread dispersal of the microsporidian Nosema ceranae, an emergent pathogen of the western honey bee, Apis mellifera. J Invertebr Pathol 96:1–10. https://doi.org/10.1016/j.jip.2007.02.014
Chen YP, Huang ZY (2010) Nosema ceranae, a newly identified pathogen of Apis mellifera in the USA and Asia. Apidologie 41:364–374. https://doi.org/10.1051/apido/2010021
Huang W-F, Jiang J-H, Chen Y-W, Wang C-H (2007) A Nosema ceranae isolate from the honeybee Apis mellifera. Apidologie 38:30–37. https://doi.org/10.1051/apido:2006054
Higes M, Martín R, Meana A (2006) Nosema ceranae, a new microsporidian parasite in honeybees in Europe. J Invertebr Pathol 92:93–95. https://doi.org/10.1016/j.jip.2006.02.005
Botías C, Anderson DL, Meana A, Garrido-Bailón E, Martín-Hernández R, Higes M (2012) Further evidence of an oriental origin for Nosema ceranae (Microsporidia: Nosematidae). J Invertebr Pathol 110:108–113. https://doi.org/10.1016/j.jip.2012.02.014
Gómez-Moracho T, Bartolomé C, Bello X, Martín-Hernández R, Higes M, Maside X (2015) Recent worldwide expansion of Nosema ceranae (Microsporidia) in Apis mellifera populations inferred from multilocus patterns of genetic variation. Infect Genet Evol 31:87–94. https://doi.org/10.1016/j.meegid.2015.01.002
Martín-Hernández R, Meana A, Prieto L et al (2007) Outcome of colonization of Apis mellifera by Nosema ceranae. Appl Environ Microbiol 73:6331–6338. https://doi.org/10.1128/AEM.00270-07
Williams GR, Shafer ABA, Rogers REL, Shutler D, Stewart DT (2008) First detection of Nosema ceranae, a microsporidian parasite of European honey bees (Apis mellifera), in Canada and Central USA. J Invertebr Pathol 97:189–192. https://doi.org/10.1016/j.jip.2007.08.005
Suwannapong G, Yemor T, Boonpakdee C, Benbow ME (2011) Nosema ceranae, a new parasite in Thai honeybees. J Invertebr Pathol 106:236–241. https://doi.org/10.1016/j.jip.2010.10.003
Sagastume S, del Águila C, Martín-Hernández R, Higes M, Henriques-Gil N (2011) Polymorphism and recombination for rDNA in the putatively asexual microsporidian Nosema ceranae, a pathogen of honeybees. Environ Microbiol 13:84–95. https://doi.org/10.1111/j.1462-2920.2010.02311.x
Sagastume S, Martín-Hernández R, Higes M, Henriques-Gil N (2014) Ribosomal gene polymorphism in small genomes: analysis of different 16S rRNA sequences expressed in the honeybee parasite Nosema ceranae (Microsporidia). J Eukaryot Microbiol 61:42–50. https://doi.org/10.1111/jeu.12084
Sagastume S, Martín-Hernández R, Higes M, Henriques-Gil N (2016) Genotype diversity in the honey bee parasite Nosema ceranae: multi-strain isolates, cryptic sex or both? BMC Evol Biol 16:216. https://doi.org/10.1186/s12862-016-0797-7
Roudel M, Aufauvre J, Corbara B et al (2013) New insights on the genetic diversity of the honeybee parasite Nosema ceranae based on multilocus sequence analysis. Parasitology 140:1346–1356. https://doi.org/10.1017/S0031182013001133
Huang W-F, Bocquet M, Lee K-C, Sung IH, Jiang JH, Chen YW, Wang CH (2008) The comparison of rDNA spacer regions of Nosema ceranae isolates from different hosts and locations. J Invertebr Pathol 97:9–13. https://doi.org/10.1016/j.jip.2007.07.001
Medici SK, Sarlo EG, Porrini MP, Braunstein M, Eguaras MJ (2012) Genetic variation and widespread dispersal of Nosema ceranae in Apis mellifera apiaries from Argentina. Parasitol Res 110:859–864. https://doi.org/10.1007/s00436-011-2566-2
Cornman RS, Chen YP, Schatz MC, Street C, Zhao Y, Desany B, Egholm M, Hutchison S, Pettis JS, Lipkin WI, Evans JD (2009) Genomic analyses of the microsporidian Nosema ceranae, an emergent pathogen of honey bees. PLoS Pathog 5:e1000466. https://doi.org/10.1371/journal.ppat.1000466
Pelin A, Selman M, Aris-Brosou S, Farinelli L, Corradi N (2015) Genome analyses suggest the presence of polyploidy and recent human-driven expansions in eight global populations of the honeybee pathogen Nosema ceranae. Environ Microbiol 17:4443–4458. https://doi.org/10.1111/1462-2920.12883
Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874. https://doi.org/10.1093/molbev/msw054
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New York
Paradis E (2010) pegas: an R package for population genetics with an integrated-modular approach. Bioinformatics 26:419–420. https://doi.org/10.1093/bioinformatics/btp696
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Kofler R, Orozco-terWengel P, De Maio N et al (2011) PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS One 6:e15925. https://doi.org/10.1371/journal.pone.0015925
Li H, Durbin R (2009) Fast and accurate short read alignment with burrows-wheeler transform. Bioinformatics 25:1754–1760. https://doi.org/10.1093/bioinformatics/btp324
Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, Marth G, Abecasis G, Durbin R, 1000 Genome Project Data Processing Subgroup (2009) The sequence alignment/map format and SAMtools. Bioinformatics 25:2078–2079. https://doi.org/10.1093/bioinformatics/btp352
Kofler R, Pandey RV, Schlötterer C (2011) PoPoolation2: identifying differentiation between populations using sequencing of pooled DNA samples (Pool-Seq). Bioinformatics 27:3435–3436. https://doi.org/10.1093/bioinformatics/btr589
seqtk: Toolkit for processing sequences in FASTA/Q formats. https://github.com/lh3/seqtk. Accessed 20 Aug 2005
Wickam H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Garrison E, Marth G (2012) Haplotype-based variant detection from short-read sequencing. Science 342:357–360
Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574. https://doi.org/10.1093/bioinformatics/btg180
Darriba D, Taboada GL, Doallo R, Posada D (2012) jModelTest 2: more models, new heuristics and high-performance computing. Nat Methods 9:772. https://doi.org/10.1038/nmeth.2109.jModelTest
Danecek P, Auton A, Abecasis G, Albers CA, Banks E, DePristo MA, Handsaker RE, Lunter G, Marth GT, Sherry ST, McVean G, Durbin R, 1000 Genomes Project Analysis Group (2011) The variant call format and VCFtools. Bioinformatics 27:2156–2158. https://doi.org/10.1093/bioinformatics/btr330
Conesa A, Götz S, García-Gómez JM et al (2005) Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21:3674–3676. https://doi.org/10.1093/bioinformatics/bti610
Watterson GA (1975) On the number of segregating sites in genetical models without recombination. Theor Popul Biol 7:256–276. https://doi.org/10.1016/0040-5809(75)90020-9
Feder AF, Petrov DA, Bergland AO (2012) LDx: estimation of linkage disequilibrium from high-throughput pooled resequencing data. PLoS One 7:e48588. https://doi.org/10.1371/journal.pone.0048588
Nurk S, Bankevich A, Antipov D, Gurevich AA, Korobeynikov A, Lapidus A, Prjibelski AD, Pyshkin A, Sirotkin A, Sirotkin Y, Stepanauskas R, Clingenpeel SR, Woyke T, Mclean JS, Lasken R, Tesler G, Alekseyev MA, Pevzner PA (2013) Assembling single-cell genomes and mini-metagenomes from chimeric MDA products. J Comput Biol 20:714–737. https://doi.org/10.1089/cmb.2013.0084
Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410. https://doi.org/10.1016/S0022-2836(05)80360-2
Bao E, Jiang T, Girke T (2014) AlignGraph: algorithm for secondary de novo genome assembly guided by closely related references. Bioinformatics 30:i319–i328. https://doi.org/10.1093/bioinformatics/btu291
Delcher AL, Phillippy A, Carlton J, Salzberg SL (2002) Fast algorithms for large-scale genome alignment and comparison. Nucleic Acids Res 30:2478–2483. https://doi.org/10.1093/nar/30.11.2478
Shigano T, Hatakeyama Y, Nishimoto N et al (2015) Variety and diversity of microsporidia isolated from the common cutworm Spodoptera litura in Chichijima, Ogasawara Islands. J Insect Biotechnol Sericol 84:69–73
Dong S, Shen Z, Xu L, Zhu F (2010) Sequence and phylogenetic analysis of SSU rRNA gene of five microsporidia. Curr Microbiol 60:30–37. https://doi.org/10.1007/s00284-009-9495-7
Whipps CM, Kent ML (2006) Polymerase chain reaction detection of Pseudoloma neurophilia, a common microsporidian of zebrafish (Danio rerio) reared in research laboratories. J Am Assoc Lab Anim Sci 45:36–39
Zhang W, Ren G, Zhao W, Yang Z, Shen Y, Sun Y, Liu A, Cao J (2017) Genotyping of Enterocytozoon bieneusi and subtyping of Blastocystis in cancer patients: relationship to diarrhea and assessment of zoonotic transmission. Front Microbiol 8:1835. https://doi.org/10.3389/fmicb.2017.01835
Ironside JE (2013) Diversity and recombination of dispersed ribosomal DNA and protein coding genes in microsporidia. PLoS One 8:e55878. https://doi.org/10.1371/journal.pone.0055878
Desjardins CA, Sanscrainte ND, Goldberg JM, Heiman D, Young S, Zeng Q, Madhani HD, Becnel JJ, Cuomo CA (2015) Contrasting host–pathogen interactions and genome evolution in two generalist and specialist microsporidian pathogens of mosquitoes. Nat Commun 6:7121. https://doi.org/10.1038/ncomms8121
Cuomo CA, Desjardins CA, Bakowski MA, Goldberg J, Ma AT, Becnel JJ, Didier ES, Fan L, Heiman DI, Levin JZ, Young S, Zeng Q, Troemel ER (2012) Microsporidian genome analysis reveals evolutionary strategies for obligate intracellular growth. Genome Res 22:2478–2488. https://doi.org/10.1101/gr.142802.112
Ndikumana S, Pelin A, Williot A, Sanders JL, Kent M, Corradi N (2017) Genome analysis of Pseudoloma neurophilia : a microsporidian parasite of zebrafish (Danio rerio). J Eukaryot Microbiol 64:18–30. https://doi.org/10.1111/jeu.12331
Selman M, Sak B, Kváč M, Farinelli L, Weiss LM, Corradi N (2013) Extremely reduced levels of heterozygosity in the vertebrate pathogen Encephalitozoon cuniculi. Eukaryot Cell 12:496–502. https://doi.org/10.1128/EC.00307-12
Pelin A, Moteshareie H, Sak B, Selman M, Naor A, Eyahpaise MÈ, Farinelli L, Golshani A, Kvac M, Corradi N (2016) The genome of an Encephalitozoon cuniculi type III strain reveals insights into the genetic diversity and mode of reproduction of a ubiquitous vertebrate pathogen. Heredity 116:458–465. https://doi.org/10.1038/hdy.2016.4
Pombert J-F, Xu J, Smith DR, Heiman D, Young S, Cuomo CA, Weiss LM, Keeling PJ (2013) Complete genome sequences from three genetically distinct strains reveal high Intraspecies genetic diversity in the microsporidian Encephalitozoon cuniculi. Eukaryot Cell 12:503–511. https://doi.org/10.1128/EC.00312-12
Diogo D, Bouchier C, D’Enfert C, Bougnoux M-E (2009) Loss of heterozygosity in commensal isolates of the asexual diploid yeast Candida albicans. Fungal Genet Biol 46:159–168. https://doi.org/10.1016/j.fgb.2008.11.005
Lamour KH, Mudge J, Gobena D, Hurtado-Gonzales OP, Schmutz J, Kuo A, Miller NA, Rice BJ, Raffaele S, Cano LM, Bharti AK, Donahoo RS, Finley S, Huitema E, Hulvey J, Platt D, Salamov A, Savidor A, Sharma R, Stam R, Storey D, Thines M, Win J, Haas BJ, Dinwiddie DL, Jenkins J, Knight JR, Affourtit JP, Han CS, Chertkov O, Lindquist EA, Detter C, Grigoriev IV, Kamoun S, Kingsmore SF (2012) Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. Mol Plant-Microbe Interact 25:1350–1360. https://doi.org/10.1094/MPMI-02-12-0028-R
Nebavi F, Ayala FJ, Renaud F, Bertout S, Eholie S, Moussa K, Mallie M, de Meeus T (2006) Clonal population structure and genetic diversity of Candida albicans in AIDS patients from Abidjan (Côte d’Ivoire). Proc Natl Acad Sci 103:3663–3668. https://doi.org/10.1073/pnas.0511328103
Rogers MB, Downing T, Smith BA, Imamura H, Sanders M, Svobodova M, Volf P, Berriman M, Cotton JA, Smith DF (2014) Genomic confirmation of hybridisation and recent inbreeding in a vector-isolated Leishmania population. PLoS Genet 10:e1004092. https://doi.org/10.1371/journal.pgen.1004092
Gatehouse HS, Malone LA (1998) The ribosomal RNA gene region of Nosema apis (Microspora): DNA sequence for small and large subunit rRNA genes and evidence of a large tandem repeat unit size. J Invertebr Pathol 71:97–105. https://doi.org/10.1006/jipa.1997.4737
Rosenberg SM (2011) Stress-induced loss of heterozygosity in Candida: a possible missing link in the ability to evolve. MBio 2:e00200–e00211. https://doi.org/10.1128/mBio.00200-11
Acknowledgements
We are grateful to Eric Chen, Nathan Liang, and Stephanie Mathieu for the assistance in the laboratory. NC’s work is supported by the Discovery program from the Natural Sciences and Engineering Research Council of Canada (NSERC-Discovery) and an Early Researcher Award from the Ontario Ministry of Research and Innovation (ER13-09-190).
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Fig. S1
Discontinuous sequence alignment of a region of the SSU gene. Includes the novel Nosema sequence detected in Thai honeybee populations (top row), N. ceranae (middle row), and N. apis (bottom row). Asterisks (*) indicate sites without polymorphisms and SNPs are highlighted in white. (PNG 1927 kb)
Fig. S2
SNP allele frequency distributions for the Thailand populations of N. ceranae. Frequencies are based on read counts of bi-allelic SNPs within each genome. (PNG 245 kb)
Fig. S3
SNP density of scaffolds containing evidence for loss of heterozygosity (LOH) in the genome of N. ceranae populations from Thailand. SNPs were plotted in a 1 kb window and the regions exhibiting LOH are indicated. LOH present in scaffolds JPQZ01000016.1 and JPQZ01000026.1 are specific to Thailand populations. (PNG 1153 kb)
Fig. S4
Distribution of average Watterson’s θ values for coding regions within N. ceranae populations from Thailand. The top 1% of genes are indicated in the boxed region and the average exome-wide θ is indicated by the dotted line. (PNG 72 kb)
Fig. S5
Linkage disequilibrium (r2) plotted along the three largest scaffolds of Thailand populations of N. ceranae. (PNG 1574 kb)
Fig. S6
Linkage disequilibrium decay plotted as mean r2 as a function of distance between SNPs on the three largest scaffolds of N. ceranae. Gray area surrounding the curve indicates standard deviation from the mean at each distance. (PNG 447 kb)
Table S1
Sample and sequencing coverage information for populations of N. ceranae sent for Illumina sequencing. (DOCX 13 kb)
Table S2
Predicted functions for genes within regions exhibiting loss of heterozygosity (LOH). (DOCX 17 kb)
Table S3
The top 50 coding regions with the highest Watterson’s θ values for each population of N. ceranae from Thailand and their predicted gene functions. (DOCX 20 kb)
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Peters, M.J., Suwannapong, G., Pelin, A. et al. Genetic and Genome Analyses Reveal Genetically Distinct Populations of the Bee Pathogen Nosema ceranae from Thailand. Microb Ecol 77, 877–889 (2019). https://doi.org/10.1007/s00248-018-1268-z
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DOI: https://doi.org/10.1007/s00248-018-1268-z