Single-nucleotide polymorphism markers in mitochondrial genomes for identifying Varroa destructor-resistant and -susceptible strains of Apis mellifera (Hymenoptera: Apidae)

References

• Andrews S. 2010. FastQC: A quality control tool for high throughput sequence data. http://www.bioinformatics.babraham.ac.uk/projects/fastqc.
   Google Scholar
• Bolger AM, Lohse M, Usadel B. 2014. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 30:2114–2120.
   PubMed Web of Science ®Google Scholar
• Boore JL. 1999. Animal mitochondrial genomes. Nucleic Acids Res. 27:1767–1780.
   PubMed Web of Science ®Google Scholar
• Büchler R, Berg S, Le Conte Y. 2010. Breeding for resistance to Varroa destructor in Europe. Apidologie. 41:393–408.
   Web of Science ®Google Scholar
• Burland TG. 2000. DNASTAR’s laser gene sequence analysis software. In: Misener S, Krawets SA, editors. Bioinformatics Methods and Protocols. Totowa: Humana Press; p. 71–91.
   Google Scholar
• Cameron SL. 2014a. Insect mitochondrial genomics: implications for evolution and phylogeny. Annu Rev Entomol. 59:95–117.
   PubMed Web of Science ®Google Scholar
• Cameron SL. 2014b. How to sequence and annotate insect mitochondrial gemones for systematic and comparative geneomics research. Syst Entomol. 39:400–411.
   Web of Science ®Google Scholar
• Chen YP, Siede R. 2007. Honey bee viruses. Adv Virus Res. 70:33–80.
   PubMed Web of Science ®Google Scholar
• Chaturvedi S, Lucas LK, Nice CC, Fordyce JA, Forister ML, Gompert Z. 2018. The predictability of genomic changes underlying a recent host shift in Melissa blue butterflies. Mol Ecol. 27:2651–2666.
   PubMed Web of Science ®Google Scholar
• Clermont A, Pasquali M, Eickermann M, Kraus F, Hoffmann L, Beyer M. Virus status, varroa levels and survival of 20 managed honey bee colonies monitored in Luxembourg between summer 2011 and spring 2013. J Apic Sci. 59:59–73.
   Web of Science ®Google Scholar
• Crozier RH, Crozier YC. 1993. The mitochondrial genome of the honeybee Apis mellifera: complete sequence and genome organization. Genetics. 133:97–117.
   PubMed Web of Science ®Google Scholar
• Dowton M, Cameron SL, Dowavic JI, Austin AD, Whiting MF. 2009. Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Mol Biol Evol. 26:1607–1617.
   PubMed Web of Science ®Google Scholar
• Dussex N, Chuah A, Waters JM. 2016. Genome-wide SNPs reveal fine-scale differentiation among wingless alpine stonefly populations and introgression between winged and wingless forms. Evolution. 70:38–47.
   PubMed Web of Science ®Google Scholar
• Eimanifar A, Kimball RT, Braun EL, Ellis JD. 2016. The complete mitochondrial genome of the Cape honey bee, Apis mellifera capensis Esch. (Insecta: hymenoptera: apidae). Mitochondrial DNA Part B. 1:817–819.
   PubMed Web of Science ®Google Scholar
• Eimanifar A, Kimball RT, Braun EL, Fuchs S, Grünewald B, Ellis JD. 2017. The complete mitochondrial genome and phylogenetic placement of Apis nigrocincta Smith (Insecta: Hymenoptera: Apidae), an Asian, cavity-nesting honey bee. Mitochondrial DNA Part B. 2:249–250.
   PubMed Web of Science ®Google Scholar
• Eimanifar A, Kimball RT, Braun EL, Fuchs S, Grünewald B, Ellis JD. 2017. The complete mitochondrial genome of Apis mellifera meda (Insecta: Hymenoptera: Apidae). Mitochondrial DNA Part B. 2:268–269.
   PubMed Web of Science ®Google Scholar
• Eimanifar A, Kimball RT, Braun EL, Moustafa DM, Haddad N, Fuchs S, Grünewald B, Ellis JD. 2017. The complete mitochondrial genome of the Egyptian honey bee, Apis mellifera lamarckii (Insecta: Hymenoptera: Apidae). Mitochondrial DNA Part B. 2:270–272.
   PubMed Web of Science ®Google Scholar
• Feijao PC, Neiva LS, Azeredo-Espin A. M L d, Lessinger AC. 2006. AMiGA: the arthropodan mitochondrial genomes accessible database. Bioinformatics. 22:902–903.
   PubMed Web of Science ®Google Scholar
• Francis RM, Nielsen SL, Kryger P. 2013. Varroa-virus interaction in collapsing honey bee colonies. PLoS One. 8:e57540.
   PubMed Web of Science ®Google Scholar
• Fuller ZL, Niño EL, Patch HM, Bedoya-Reina OC, Baumgarten T, Muli E, Mumoki F, Ratan A, McGraw J, Frazier M, et al. 2015. Genome-wide analysis of signatures of selection in populations of African honey bees (Apis mellifera) using new web-based tools. BMC Genomics. 16:518.
   PubMed Web of Science ®Google Scholar
• Gibson JD, Hunt GJ. 2016. The complete mitochondrial genome of the invasive Africanized honey bee, Apis mellifera scutellata (Insecta: Hymenoptera: Apidae). Mitochondrial DNA Part A. 27:561–562.
   PubMed Web of Science ®Google Scholar
• Guzmán-Novoa E, Eccles L, Calvete Y, Mcgowan J, Kelly PG, Correa-Benítez A. 2010. Varroa destructor is the main culprit for the death and reduced populations of overwintered honey bee (Apis mellifera) colonies in Ontario, Canada. Apidologie. 41:443–450.
   Web of Science ®Google Scholar
• Haddad NJ. 2016. Mitochondrial genome of the Levant Region honeybee, Apis mellifera syriaca (Hymenoptera: Apidae). Mitochondrial DNA Part A. 27:4067–4068.
   PubMed Web of Science ®Google Scholar
• Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PDN. 2006. DNA barcodes distinguish species of tropical Lepidoptera. Proc Natl Acad Sci USA. 103:968–971.
   PubMed Web of Science ®Google Scholar
• Harrison RG. 1989. Animal mitochondrial DNA as a genetic marker in population and evolutionary biology. Trends Ecol. Evol. (Amst.) 4:6–11.
   PubMed Web of Science ®Google Scholar
• Holloway B, Sylvester HA, Bourgeois L, Rinderer TE. 2012. Association of single nucleotide polymorphisms to resistance to chalkbrood in Apis mellifera. J Apic Res. 51:154–163.
   Web of Science ®Google Scholar
• Hu P, Lu ZX, Haddad N, Noureddine A, Loucif-Ayad W, Wang YZ, Zhao RB, Zhang AL, Guan X, Zhang HX, et al. 2016. Complete mitochondrial genome of the Algerian honeybee, Apis mellifera intermissa (Hymenoptera: Apidae). Mitochondrial DNA Part A. 27:1791–1792.
   PubMed Web of Science ®Google Scholar
• Katoh K, Misawa K, Kuma K, Miyata T. 2002. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 30:3059–3066.
   PubMed Web of Science ®Google Scholar
• Kim MJ, Hong EJ, Kim I. 2016. Complete mitochondrial genome of Camponotus atrox (Hymenoptera: Formicidae): a new tRNA arrangement in Hymenoptera. Genome. 59:59–74.
   PubMed Web of Science ®Google Scholar
• Kim MJ, Im HH, Lee KY, Han YS, Kim I. 2014. Complete mitochondrial genome of the whiter-spotted flower chafer, Protaetia brevitarsis (Coleoptera: Scarabaeidae). Mitochondrial DNA. 25:177–178.
   PubMed Web of Science ®Google Scholar
• Kim MJ, Jeong JS, Kim JS, Jeong SY, Kim I. 2017. Complete mitochondrial genome of the lappet moth, Kunugia undans (Lepidoptera: Lasiocampidae): genomic comparisons among macroheteroceran superfamilies. Genet Mol Biol. 40:717–723.
   PubMed Web of Science ®Google Scholar
• Kim HK, Lee MY, Lee ML, Choi YS, Byeon KH. 2015. Hygienic behavior test of six inbred lines in Apis mellifera through freeze-killed brood method. J Apic. 30:187–190.
   Google Scholar
• Li H, Durbin R. 2009. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics. 25:1754–1760.
   PubMed Web of Science ®Google Scholar
• Li Y, Hu Y, Bolund L, Wang J. 2010. State of the art de novo assembly of human genomes from massively parallel sequencing data. Hum Genomics. 4:271–277.
   PubMedGoogle Scholar
• Li D, Guo Y, Shao H, Tellier LC, Wang J, Xiang Z, Xia Q. 2010. Genetic diversity, molecular phylogeny and selection evidence of the silkworm mitochondria implicated by complete resequencing of 41 genomes. BMC Evol Biol. 10:81.
   PubMed Web of Science ®Google Scholar
• Li C, Waldbieser G, Bosworth B, Beck BH, Thongda W, Peatman E. 2014. SNP discovery in wild and domesticated populations of blue catfish, Ictalurus furcatus, using genotyping-by-sequencing and subsequent SNP validation. Mol Ecol Resour. 14:1261–1270.
   PubMed Web of Science ®Google Scholar
• Lo N, Gloag RS, Anderson DL, Oldroyd BP. 2010. A molecular phylogeny of the genus Apis suggests that the giant honey bee of the Philippines, A. breviligula Maa, and the plains honey bee of southern India, A. indica Fabricius, are valid species. Syst Entomol. 35:226–233.
   Web of Science ®Google Scholar
• Lowe TM, Eddy SR. 1997. tRNAscan-SE: a program for improved detection of transfer RNA genes in genomic sequence. Nucleic Acids Res. 25:955–964.
   PubMed Web of Science ®Google Scholar
• Momot JP, Rothenbuhler WC. 1971. Behaviour genetics of nest cleaning in honeybees. VI. Interactions of age and genotype of bees, and nectar flow. J Apic Res. 10:11–21.
   Google Scholar
• Mõtus K, Raie A, Orro T, Chauzat M-P, Viltrop A. 2016. Epidemiology, risk factors and varroa mite control in the Estonian honey bee population. J Apic Res. 55:396–412.
   Web of Science ®Google Scholar
• Nazzi F, Pennacchio F. 2014. Disentangling multiple interactions in the hive ecosystem. Trends Parasitol. 30:556–560.
   PubMed Web of Science ®Google Scholar
• Neumann P, Carreck NL. 2010. Honey bee colony losses. J Apic Res. 49:1–6.
   Web of Science ®Google Scholar
• Ohtsuki T, Sato A, Watanabe Y, Watanabe K. 2002. A unique serine-specific elongation factor Tu found in nematode mitochondria. Nat Struct Biol. 9:669–673.
   PubMedGoogle Scholar
• Ojala D, Montoya J, Attardi G. 1981. tRNA punctuation model of RNA processing in human mitochondria. Nature. 290:470–474.
   PubMed Web of Science ®Google Scholar
• Pirk CW, Human H, Crewe RM, Van Engelsdorp D. 2014. A survey of managed honey bee colony losses in the Republic of South Africa-2009 to 2011. J Apic Res. 53:35–42.
   Web of Science ®Google Scholar
• Rinderer TE, Harris JW, Hunt GJ, De Guzman LI. 2010. Breeding for resistance to Varroa destructor in North America. Apidologie. 41:409–424.
   Web of Science ®Google Scholar
• Raffiudin R, Crozier RH. 2007. Phylogenetic analysis of honey bee behavioral evolution. Mol Phylogenetics Evol. 43:543–552.
   PubMed Web of Science ®Google Scholar
• Silva-Brandão KL, Silva O. A B N e, Brandão MM, Omoto C, Sperling FAH. 2015. Genotyping‐by‐sequencing approach indicates geographic distance as the main factor affecting genetic structure and gene flow in Brazilian populations of Grapholita molesta (Lepidoptera, Tortricidae). Evol Appl. 8:476–485.
   PubMed Web of Science ®Google Scholar
• Spötter A, Gupta P, Mayer M, Reinsch N, Bienefeld K. 2016. Genome-wide association study of a Varroa-specific defense behavior in honeybees (Apis mellifera). J Hered. 107:220–227.
   PubMed Web of Science ®Google Scholar
• Takahashi J, Wakamiya T, Kiyoshi T, Uchiyama H, Yajima S, Kimura K, Nomura T. 2016. The complete mitochondrial genome of the Japanese honeybee, Apis cerana japonica (Insecta: Hymenoptera: Apidae). Mitochondrial DNA Part B. 1:156–157.
   PubMed Web of Science ®Google Scholar
• Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. 2013. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 30:2725–2729.
   PubMed Web of Science ®Google Scholar
• Tan HW, Liu GH, Dong X, Lin RQ, Song HQ, Huang SY, Yuan ZG, Zhao GH, Zhu XQ. 2011. The complete mitochondrial genome of the Asiatic cavity-nesting honeybee Apis cerana (Hymenoptera: Apidae). PLoS One. 6:e23008.
   PubMed Web of Science ®Google Scholar
• Tang M, Tan M, Meng G, Yang S, Su X, Liu S, Song W, Li Y, Wu Q, Zhang A, et al. 2014. Multiplex sequencing of pooled mitochondrial genomes-a crucial step toward biodiversity analysis using mito-metagenomics. Nucleic Acids Res. 42:e166.
   PubMed Web of Science ®Google Scholar
• Thompson VC. 1964. Behaviour genetics of nest cleaning in honeybees. III. Effect of age of bees of a resistant line on their response to disease-killed brood. J Apic Res. 3:25–30.
   Google Scholar
• Van Engelsdorp D, Hayes J, Underwood RM, Caron D, Pettis J. 2011. A survey of managed honey bee colony losses in the USA, fall 2009 to winter 2010. J Apic Res. 50:1–10.
   Web of Science ®Google Scholar
• Wakamiya T, Tingek S, Okuyama H, Kiyoshi T, Takahashi JI. 2017. The complete mitochondrial genome of the cavity-nesting honeybee, Apis koschevnikovi (Insecta: Hymenoptera: Apidae). Mitochondrial DNA Part B. 2:24–25.
   PubMed Web of Science ®Google Scholar
• Wan X, Kim MI, Kim MJ, Kim I. 2012. Complete mitochondrial genome of the free-living earwig, Challia fletcheri (Dermaptera: Pygidicranidae) and phylogeny of polyneoptera. PLoS One. 7:e42056.
   PubMed Web of Science ®Google Scholar
• Wang AR, Kim MJ, Lee JY, Choi YS, Thapa R, Kim I. 2015. The mitochondrial genome of the black dwarf honey bee, Apis andreniformis (Hymenoptera: Apidae). Mitochondrial DNA. 26:914–916.
   PubMed Web of Science ®Google Scholar
• Wang AR, Kim MJ, Park JS, Choi YS, Thapa R, Lee KY, Kim I. 2013. Complete mitochondrial genome of the dwarf honeybee, Apis florea (Hymenoptera: Apidae). Mitochondrial DNA. 24:208–210.
   PubMed Web of Science ®Google Scholar
• Wolstenholme DR. 1992. Animal mitochondrial DNA: structure and evolution. Int Rev Cytol. 141:173–216.
   PubMed Web of Science ®Google Scholar