Abstract
The cavity-nesting honeybee, Apis nigrocincta, only inhabits the tropical forests of Sulawesi, Sangihe and Mindanao Islands, which are designated as biodiversity hotspots and one of the important areas for biological conservation. In the present study, for the first time, we analyzed the complete mitochondrial genome of A. nigrocincta from two regions in Sangihe Island, Indonesia. The mitochondrial genome of A. nigrocincta consists of a circular molecule of approximately 1.5 kb that includes 13 protein-coding genes (PCGs), 22 tRNA genes, 2 rRNA genes, and one AT-rich control region. Two A. nigrocincta had AT mitochondrial genome contents of approximately 84.57 and 84.23%. Start codons ATT, ATG and ATA were found in 13 PCGs. Stop codons TAA and TAG were observed in 12 PCGs and the ND2 gene, respectively. The heavy (H)-strand was predicted to have 9 PCGs and 14 tRNA genes, while the light (L)-strand was predicted to contain 4 PCGs, 8 tRNA, and 2 rRNA genes. All tRNA genes formed typical cloverleaf secondary structures, except for tRNA-Ser(AGN) and tRNA-His. The 104 mutation sites that differed between the A. nigrocincta from two regions in Sangihe Island, Indonesia were evenly distributed throughout the mitochondrial genome. The phylogenetic relationship, inferred using 13 PCGs (based on the maximum likelihood), was consistent with that reported in previous studies that predicted a sister relationship between A. nigrocincta and A. cerana. We discovered that the genetic distance between the A. nigrocincta varieties on Sangihe Island is 0.0067, indicating that they maintained a high genetic diversity on this island.
References
Arias MC, Sheppard WS (2005) Phylogenetic relationships of honey bees Hymenoptera: Apinae: Apini) inferred from nuclear and mitochondrial DNA sequence data. Mol Phyl Evol 37:25–35. https://doi.org/10.1016/j.ympev.2005.02.017
Bernt M, Donath A, Jühling F, Externbrink F, Florentz C, Fritzsch G, Pütz J, Middendorf M, Stadler PF (2013) MITOS: improved de novo metazoan mitochondrial genome annotation. Mol Phyl Evol 69:313–319. https://doi.org/10.1016/j.ympev.2012.08.023
Damus MS, Otis GW (1997) A morphometric analysis of Apis cerana F and Apis nigrocincta smith populations from Southeast Asia. Apidologie 28:309–323. https://doi.org/10.1051/apido/2010008
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. https://doi.org/10.1080/23802359.2017.1318683
Hadisoesilo S, Otis GW (1996a) Two distinct populations of cavity-nesting honey bees (Hymenoptera: Apidae) in South Sulawesi, Indonesia. J Kans Entomol Soc 68:399–407. http://www.jstor.org/stable/25085613
Hadisoesilo S, Otis GW (1996b) Drone flight times confirm the species status of Apis nigrocincta Smith, 1861 to be a species distinct from Apis cerana F 1793, in Sulawesi. Apidologie 27:361–369. https://doi.org/10.1051/apido:19960504
Hadisoesilo S, Otis GW (1998) Differences in drone capping of Apis cerana and Apis nigrocincta. J Apic Res 37:11–15. https://doi.org/10.1080/00218839.1998.11100948
Jobb G, von Haeseler A, Strimmer K (2004) TREEFINDER: a powerful graphical analysis environment for molecular phylogenetics. BMC Evol Biol 4:18. https://doi.org/10.1186/1471-2148-4-18
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 Entmol 35:226–233. https://doi.org/10.1111/j.1365-3113.2009.00504.x
Myers N, Mittermeier RA, Cristina G, Da Fonseca GAB, Jennifer K (2000) Biodiversity hotspots for conservation priorities. Nature 403:853–858. https://doi.org/10.1038/35002501
Okuyama H, Wakamiya T, Fujiwara A, Washitani I, Takahashi J (2017a) Complete mitochondrial genome of the honeybee Apis cerana native to two remote islands in Japan. Conserv Genet Resour. https://doi.org/10.1007/s12686-017-0721-5
Okuyama H, Tingek S, Takahashi J (2017b) The complete mitochondrial genome of the cavity-nesting honeybee, Apis cerana (Insecta: Hymenoptera: Apidae) from Borneo. Mitochondrial DNA Part B 2:475–476. https://doi.org/10.1080/23802359.2017.1361344
Otis GW (1996) Distributions of recently recognized species of honey bees (Hymenoptera: Apidae; Apis) in Asia. J Kans Entomol Soc 69:311–333. http://www.jstor.org/stable/25085727
Shinmura Y, Okuyama H, Kiyoshi T, Lin CP, Kadowaki T, Takahashi J (2017) The complete mitochondrial genome and genetic distinction of the Taiwanese honeybee, Apis cerana (Hymenoptera: Apidae). Conserv Genet Res. https://doi.org/10.1007/s12686-017-0879-x
Smith DR, Hagen RH (1996) The biogeography of Apis cerana as revealed by mitochondrial DNA sequence data. J Kans Entomol Soc 69:249–310
Smith DR, Villafuerte L, Otis G, Palmer MR (2000) Biogeography of Apis cerana F. and A. nigrocincta Smith: insights from mtDNA studies. Apidologie 31:265–279. https://doi.org/10.1051/apido:2000121
Smith DR, Palmer MR, Otis G, Damus M (2003) Mitochondrial DNA and AFLP markers support species status of Apis nigrocincta. Insectes Soc 50:185–190. https://doi.org/10.1007/s00040-003-0645-9
Takahashi J, Nakamura J, Sasaki M, Tingek S, Akimoto S (2002) New haplotypes for the non-coding region of mitochondrial DNA in cavity-nesting honey bees Apis koschevnikovi and Apis nuluensis. Apidologie 33:25–31. https://doi.org/10.1051/apido:2001002
Takahashi J, Rai J, Wakamiya T, Okuyama H (2017) Characterization of the complete mitochondrial genome of the giant black Himalayan honeybee (Apis laboriosa) from Nepal. Conserv Genet Res. https://doi.org/10.1007/s12686-017-0765-6
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. https://doi.org/10.1093/molbev/mst197
Acknowledgements
We are grateful to Prof. Masami Sasaki for kindly providing data for helping our analysis.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors report no conflicts of interest.
Additional information
H. Randall Hepburn—Deceased 10 October 2014.
Rights and permissions
About this article
Cite this article
Takahashi, Ji., Hadisoesilo, S., Okuyama, H. et al. Analysis of the complete mitochondrial genome of Apis nigrocincta (Insecta: Hymenoptera: Apidae) on Sangihe Island in Indonesia. Conservation Genet Resour 10, 755–760 (2018). https://doi.org/10.1007/s12686-017-0922-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s12686-017-0922-y