Volume 45 Issue 1
Jan.  2024
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Yu-Ran Li, Zheng-Wei Wang, Richard T. Corlett, Wen-Bin Yu. Comparative analyses of mitogenomes in the social bees with insights into evolution of long inverted repeats in the Meliponini. Zoological Research, 2024, 45(1): 160-175. doi: 10.24272/j.issn.2095-8137.2023.169
Citation: Yu-Ran Li, Zheng-Wei Wang, Richard T. Corlett, Wen-Bin Yu. Comparative analyses of mitogenomes in the social bees with insights into evolution of long inverted repeats in the Meliponini. Zoological Research, 2024, 45(1): 160-175. doi: 10.24272/j.issn.2095-8137.2023.169

Comparative analyses of mitogenomes in the social bees with insights into evolution of long inverted repeats in the Meliponini

doi: 10.24272/j.issn.2095-8137.2023.169
The newly sequenced and assembled mitogenomes of Meliponini can be downloaded from NCBI (accession numbers in Supplementary Table S4). All the newly assembled mitogenomes can be downloaded from China National Center for Bioinformation (Supplementary Table S5) (PRJCA021965) and Science Data Bank databases (DOI: 10.57760/sciencedb.j00139.00088).
Supplementary data to this article can be found online.
The authors declare that they have no competing interests.
W.B.Y., R.T.C., and Y.R.L. conceived and designed the research; Z.W.W. and Y.R.L. collected and identified samples; Y.R.L. and W.B.Y. analyzed the data and interpreted results; Y.R.L. and W.B.Y. wrote draft of the manuscript; all authors revised and approved the final version of the manuscript.
Funds:  This study was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB31000000), Science and Technology Basic Resources Investigation Program of China (2021FY100200), Yunnan Revitalization Talent Support Program “Young Talent” and "Innovation Team" Projects, and the 14th Five-Year Plan of Xishuangbanna Tropical Botanical Garden, Chinese Academy of Science (XTBG-1450101)
More Information
  • The insect mitogenome is typically a compact circular molecule with highly conserved gene contents. Nonetheless, mitogenome structural variations have been reported in specific taxa, and gene rearrangements, usually the tRNAs, occur in different lineages. Because synapomorphies of mitogenome organizations can provide information for phylogenetic inferences, comparative analyses of mitogenomes have been given increasing attention. However, most studies use a very few species to represent the whole genus, tribe, family, or even order, overlooking potential variations at lower taxonomic levels, which might lead to some incorrect inferences. To provide new insights into mitogenome organizations and their implications for phylogenetic inference, this study conducted comparative analyses for mitogenomes of three social bee tribes (Meliponini, Bombini, and Apini) based on the phylogenetic framework with denser taxonomic sampling at the species and population levels. Comparative analyses revealed that mitogenomes of Apini and Bombini are the typical type, while those of Meliponini show diverse variations in mitogenome sizes and organizations. Large inverted repeats (IRs) cause significant gene rearrangements of protein coding genes (PCGs) and rRNAs in Indo-Malay/Australian stingless bee species. Molecular evolution analyses showed that the lineage with IRs have lower dN/dS ratios for PCGs than lineages without IRs, indicating potential effects of IRs on the evolution of mitochondrial genes. The finding of IRs and different patterns of gene rearrangements suggested that Meliponini is a hotspot in mitogenome evolution. Unlike conserved PCGs and rRNAs whose rearrangements were found only in the mentioned lineages within Meliponini, tRNA rearrangements are common across all three tribes of social bees, and are significant even at the species level, indicating that comprehensive sampling is needed to fully understand the patterns of tRNA rearrangements, and their implications for phylogenetic inference.
  • The newly sequenced and assembled mitogenomes of Meliponini can be downloaded from NCBI (accession numbers in Supplementary Table S4). All the newly assembled mitogenomes can be downloaded from China National Center for Bioinformation (Supplementary Table S5) (PRJCA021965) and Science Data Bank databases (DOI: 10.57760/sciencedb.j00139.00088).
    Supplementary data to this article can be found online.
    The authors declare that they have no competing interests.
    W.B.Y., R.T.C., and Y.R.L. conceived and designed the research; Z.W.W. and Y.R.L. collected and identified samples; Y.R.L. and W.B.Y. analyzed the data and interpreted results; Y.R.L. and W.B.Y. wrote draft of the manuscript; all authors revised and approved the final version of the manuscript.
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  • [1]
    Almeida EAB, Bossert S, Danforth BN, et al. 2023. The evolutionary history of bees in time and space. Current Biology, 33(16): 3409−3422.e6. doi: 10.1016/j.cub.2023.07.005
    Arias MC, Sheppard WS. 2005. Phylogenetic relationships of honey bees (Hymenoptera: Apinae: Apini) inferred from nuclear and mitochondrial DNA sequence data. Molecular Phylogenetics and Evolution, 37(1): 25−35. doi: 10.1016/j.ympev.2005.02.017
    Bankevich A, Nurk S, Antipov D, et al. 2012. SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. Journal of Computational Biology, 19(5): 455−477. doi: 10.1089/cmb.2012.0021
    Beckenbach AT. 2011. Mitochondrial genome sequences of representatives of three families of scorpionflies (Order Mecoptera) and evolution in a major duplication of coding sequence. Genome, 54(5): 368–376.
    Bernt M, Donath A, Jühling F, et al. 2013. MITOS: improved de novo Metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution, 69(2): 313−319. doi: 10.1016/j.ympev.2012.08.023
    Blaimer BB, Santos BF, Cruaud A, et al. 2023. Key innovations and the diversification of Hymenoptera. Nature Communications, 14(1): 1212. doi: 10.1038/s41467-023-36868-4
    Boore JL. 1999. Animal mitochondrial genomes. Nucleic Acids Research, 27(8): 1767−1780. doi: 10.1093/nar/27.8.1767
    Cameron SA, Hines HM, Williams PH. 2007. A comprehensive phylogeny of the bumble bees (Bombus). Biological Journal of the Linnean Society, 91(1): 161−188. doi: 10.1111/j.1095-8312.2007.00784.x
    Cameron SL. 2014. Insect mitochondrial genomics: implications for evolution and phylogeny. Annual Review of Entomology, 59: 95−117. doi: 10.1146/annurev-ento-011613-162007
    Cardinal S, Buchmann SL, Russell AL. 2018. The evolution of floral sonication, a pollen foraging behavior used by bees (Anthophila). Evolution, 72(3): 590−600. doi: 10.1111/evo.13446
    Cardinal S, Straka J, Danforth BN. 2010. Comprehensive phylogeny of apid bees reveals the evolutionary origins and antiquity of cleptoparasitism. Proceedings of the National Academy of Sciences of the United States of America, 107(37): 16207−16211.
    Christy BY, Roesma Dahelmi DI. 2019. Phylogenetic analysis of Tetragonula minangkabau and other species using cytochrome B gene. Sciendo, 63(1): 117−124.
    Clary DO, Wolstenholme DR. 1985. The mitochondrial DNA molecule of Drosophila yakuba: nucleotide sequence, gene organization, and genetic code. Journal of Molecular Evolution, 22(3): 252−271. doi: 10.1007/BF02099755
    Costa MA, Del Lama MA, Melo GAR, et al. 2003. Molecular phylogeny of the stingless bees (Apidae, Apinae, Meliponini) inferred from mitochondrial 16S rDNA sequences. Apidologie, 34(1): 73−84. doi: 10.1051/apido:2002051
    Danforth BN, Cardinal S, Praz C, et al. 2013. The impact of molecular data on our understanding of bee phylogeny and evolution. Annual Review of Entomology, 58: 57−78. doi: 10.1146/annurev-ento-120811-153633
    de Paula Freitas FC, Lourenço AP, Nunes FMF, et al. 2020. The nuclear and mitochondrial genomes of Frieseomelitta varia – a highly eusocial stingless bee (Meliponini) with a permanently sterile worker caste. BMC Genomics, 21(1): 386. doi: 10.1186/s12864-020-06784-8
    Dickey AM, Kumar V, Morgan JK, et al. 2015. A novel mitochondrial genome architecture in thrips (Insecta: Thysanoptera): extreme size asymmetry among chromosomes and possible recent control region duplication. BMC Genomics, 16(1): 439. doi: 10.1186/s12864-015-1672-4
    Dowling DK, Wolff JN. 2023. Evolutionary genetics of the mitochondrial genome: insights from Drosophila. Genetics, 224(3): iyad036.
    Dowton M, Austin AD. 1999. Evolutionary dynamics of a mitochondrial rearrangement ‘‘hot spot’’ in the hymenoptera. Molecular Biology and Evolution, 16(2): 298−309. doi: 10.1093/oxfordjournals.molbev.a026111
    Dowton M, Cameron SL, Dowavic JI, et al. 2009. Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Molecular Biology and Evolution, 26(7): 1607−1617. doi: 10.1093/molbev/msp072
    Dowton M, Castro LR, Campbell SL, et al. 2003. Frequent mitochondrial gene rearrangements at the Hymenopteran nad3–nad5 junction. Journal of Molecular Evolution, 56(5): 517−526. doi: 10.1007/s00239-002-2420-3
    Engel MS, Rasmussen C, Ayala R, et al. 2023. Stingless bee classification and biology (Hymenoptera, Apidae): a review, with an updated key to genera and subgenera. ZooKeys, 1172: 239−312. doi: 10.3897/zookeys.1172.104944
    Forbes AA, Bagley RK, Beer MA, et al. 2018. Quantifying the unquantifiable: why Hymenoptera, not Coleoptera, is the most speciose animal order. BMC Ecology, 18(1): 21. doi: 10.1186/s12898-018-0176-x
    Françoso E, Zuntini AR, Ricardo PC, et al. 2023. Rapid evolution, rearrangements and whole mitogenome duplication in the Australian stingless bees Tetragonula (Hymenoptera: Apidae): a steppingstone towards understanding mitochondrial function and evolution. International Journal of Biological Macromolecules, 242: 124568. doi: 10.1016/j.ijbiomac.2023.124568
    Gao FL, Chen CJ, Arab DA, et al. 2019. EasyCodeML: a visual tool for analysis of selection using CodeML. Ecology and Evolution, 9(7): 3891−3898. doi: 10.1002/ece3.5015
    Gonçalves LT, Françoso E, Deprá M. 2023. Mitochondrial phylogenomics of bumblebees, Bombus (Hymenoptera: Apidae): a tale of structural variation, shifts in selection constraints, and tree discordance. Zoological Journal of the Linnean Society. doi: 10.1093/zoolinnean/zlad174.
    Greiner S, Lehwark P, Bock R. 2019. OrganellarGenomeDRAW (OGDRAW) version 1.3. 1: expanded toolkit for the graphical visualization of organellar genomes. Nucleic Acids Research, 47(W1): W59−W64. doi: 10.1093/nar/gkz238
    Grüter C. 2020. Stingless Bees: Their Behaviour, Ecology and Evolution. Cham: Springer.
    Guindon S, Dufayard JF, Lefort V, et al. 2010. New algorithms and methods to estimate maximum–likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59(3): 307−321. doi: 10.1093/sysbio/syq010
    He B, Su TJ, Wu YP, et al. 2018. Phylogenetic analysis of the mitochondrial genomes in bees (Hymenoptera: Apoidea: Anthophila). PLoS One, 13(8): e0202187. doi: 10.1371/journal.pone.0202187
    Hunt GJ. 1997. Insect DNA extraction protocol. In: Micheli MR, Bova R. Fingerprinting Methods Based on Arbitrarily Primed PCR. Berlin: Springer.
    Jin JJ, Yu WB, Yang JB, et al. 2018. GetOrganelle: a simple and fast pipeline for de novo assembly of a complete circular chloroplast genome using genome skimming data. BioRxiv, 4: 256479.
    Jühling F, Pütz J, Bernt M et al. 2012. Improved systematic tRNA gene annotation allows new insights into the evolution of mitochondrial tRNA structures and into the mechanisms of mitochondrial genome rearrangements. Nucleic Acids Research, 40(7): 2833−2845. doi: 10.1093/nar/gkr1131
    Kapheim KM, Pan HL, Li C, et al. 2015. Genomic signatures of evolutionary transitions from solitary to group living. Science, 348(6239): 1139−1143. doi: 10.1126/science.aaa4788
    Kawakita A, Ascher JS, Sota T, et al. 2008. Phylogenetic analysis of the corbiculate bee tribes based on 12 nuclear protein–coding genes (Hymenoptera: Apoidea: Apidae). Apidologie, 39(1): 163−175. doi: 10.1051/apido:2007046
    Kolesnikov AA, Gerasimov ES. 2012. Diversity of mitochondrial genome organization. Biochemistry (Moscow), 77(13): 1424–1435.
    Lanfear R, Calcott B, Ho SYW, et al. 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Molecular Biology and Evolution, 29(6): 1695−1701. doi: 10.1093/molbev/mss020
    Lanfear R, Frandsen PB, Wright AM, et al. 2017. PartitionFinder 2: new methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34(3): 772−773.
    Langmead B, Salzberg SLJ. 2012. Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4): 357−359. doi: 10.1038/nmeth.1923
    Lavrov DV, Boore JL, Brown WM. 2002. Complete mtDNA sequences of two Millipedes suggest a new model for mitochondrial gene rearrangements: duplication and nonrandom loss. Molecular Biology and Evolution, 19(2): 163−169. doi: 10.1093/oxfordjournals.molbev.a004068
    Lhomme P, Hines HM. 2019. Ecology and evolution of cuckoo bumble bees. Annals of the Entomological Society of America, 112(3): 122−140. doi: 10.1093/aesa/say031
    Li H, Liu H, Shi AM, et al. 2012. The complete mitochondrial genome and novel gene arrangement of the unique–headed bug Stenopirates sp. (Hemiptera: Enicocephalidae). PLoS One, 7(1): e29419. doi: 10.1371/journal.pone.0029419
    Li H, Shao RF, Song F, et al. 2013. Mitochondrial genomes of two barklice, Psococerastis albimaculata and Longivalvus hyalospilus (Psocoptera: Psocomorpha): contrasting rates in mitochondrial gene rearrangement between major lineages of Psocodea. PLoS One, 8(4): e61685. doi: 10.1371/journal.pone.0061685
    Li YR, Wang ZW, Yu ZR, et al. 2021. Species diversity, morphometrics, and nesting biology of Chinese stingless bees (Hymenoptera, Apidae, Meliponini). Apidologie, 52(6): 1239−1255. doi: 10.1007/s13592-021-00899-x
    Lo N, Gloag RS, Anderson DL, et al. 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. Systematic Entomology, 35(2): 226−233. doi: 10.1111/j.1365-3113.2009.00504.x
    Melo GAR. 2020. Stingless bees (meliponini). In: Starr CK. Encyclopedia of Social Insects. Cham: Springer.
    Michener CD. 2007. The Bees of the World. 2nd ed. Baltimore: John Hopkins University Press.
    Moritz C, Dowling TE, Brown WM. 1987. Evolution of animal mitochondrial DNA: relevance for population biology and systematics. Annual Review of Ecology and Systematics, 18: 269−292. doi: 10.1146/annurev.es.18.110187.001413
    Oliveira DCSG, Raychoudhury R, Lavrov DV, et al. 2008. Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Molecular Biology and Evolution, 25(10): 2167−2180. doi: 10.1093/molbev/msn159
    Peters RS, Krogmann L, Mayer C, et al. 2017. Evolutionary history of the Hymenoptera. Current Biology, 27(7): 1013−1018. doi: 10.1016/j.cub.2017.01.027
    Quinn TW, Mindell DP. 1996. Mitochondrial gene order adjacent to the control region in crocodile, turtle, and tuatara. Molecular Phylogenetics and Evolution, 5(2): 344−351. doi: 10.1006/mpev.1996.0029
    Quinn TW, Wilson AC. 1993. Sequence evolution in and around the mitochondrial control region in birds. Journal of Molecular Evolution, 37(4): 417−425.
    Ramírez SR, Nieh JC, Quental TB, et al. 2010. A molecular phylogeny of the stingless bee genus Melipona (Hymenoptera: Apidae). Molecular Phylogenetics and Evolution, 56(2): 519−525. doi: 10.1016/j.ympev.2010.04.026
    Rasmussen C, Camargo JMF. 2008. A molecular phylogeny and the evolution of nest architecture and behavior in Trigona s. s. (Hymenoptera: Apidae: Meliponini). Apidologie, 39(1): 102−118. doi: 10.1051/apido:2007051
    Rasmussen C, Cameron SA. 2007. A molecular phylogeny of the Old World stingless bees (Hymenoptera: Apidae: Meliponini) and the non-monophyly of the large genus Trigona. Systematic Entomology, 32(1): 26–39.
    Rasmussen C, Cameron SA. 2010. Global stingless bee phylogeny supports ancient divergence, vicariance, and long distance dispersal. Biological Journal of the Linnean Society, 99(1): 206−232.
    Rayko E. 1997. Organization, generation and replication of amphimeric genomes: a review. Gene, 199(1-2): 1−18. doi: 10.1016/S0378-1119(97)00357-0
    Reis MD, Yang ZH. 2011. Approximate likelihood calculation on a phylogeny for bayesian estimation of divergence times. Molecular Biology and Evolution, 28(7): 2161−2172. doi: 10.1093/molbev/msr045
    Revell LJ. 2012. Phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution, 3(2): 217−223. doi: 10.1111/j.2041-210X.2011.00169.x
    Ronquist F, Huelsenbeck JP. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics, 19(12): 1572−1574. doi: 10.1093/bioinformatics/btg180
    Roubik DW. 1989. Ecology and Natural History of Tropical Bees. Cambridge: Cambridge University Press.
    Rules T. 1968. IUPAC-IUB commission on biochemical nomenclature a one-letter notation for amino acid sequences. Journal of Biological Chemistry, 243(13): 3557−3559. doi: 10.1016/S0021-9258(19)34176-6
    Saito S, Tamura K, Aotsuka T. 2005. Replication origin of mitochondrial DNA in insects. Genetics, 171(4): 1695−1705. doi: 10.1534/genetics.105.046243
    Sakagami SF. 1978. Tetragonula Stingless bees of the continental Asia and Sri Lanka (Hymenoptera, Apidae) (with 124 text-figures, 1 plate and 36 tables). Journal of the Faculty of Science Hokkaido University, 21(2): 165−247.
    Sato M, Sato K. 2012. Maternal inheritance of mitochondrial DNA: degradation of paternal mitochondria by allogeneic organelle autophagy, allophagy. Autophagy, 8(3): 424−425. doi: 10.4161/auto.19243
    Shi Y, Chu Q, Wei DD, et al. 2016. The mitochondrial genome of booklouse, Liposcelis sculptilis (Psocoptera: Liposcelididae) and the evolutionary timescale of Liposcelis. Scientific Reports, 6: 30660.
    Shtolz N, Mishmar D. 2023. The metazoan landscape of mitochondrial DNA gene order and content is shaped by selection and affects mitochondrial transcription. Communications Biology, 6(1): 93. doi: 10.1038/s42003-023-04471-4
    Silvestre D, Arias MC. 2006. Mitochondrial tRNA gene translocations in highly eusocial bees. Genetics and Molecular Biology, 29(3): 572−575. doi: 10.1590/S1415-47572006000300030
    Stamatakis A. 2014. RAxML version 8: a tool for phylogenetic analysis and post–analysis of large phylogenies. Bioinformatics, 30(9): 1312−1313. doi: 10.1093/bioinformatics/btu033
    Stein DB, Palmer JD, Thompson WF. 1986. Structural evolution and flip–flop recombination of chloroplast DNA in the fern genus Osmunda. Current Genetics, 10(11): 835–841.
    Stothard P. 2000. The sequence manipulation suite: JAVASCRIPT programs for analyzing and formatting protein and DNA sequences. BioTechniques, 28(6): 1102−1104. doi: 10.2144/00286ir01
    Sweet AD, Johnson KP, Cameron SL. 2022. Independent evolution of highly variable, fragmented mitogenomes of parasitic lice. Communications Biology, 5(1): 677. doi: 10.1038/s42003-022-03625-0
    Sweet AD, Johnson KP, Cao YH, et al. 2021. Structure, gene order, and nucleotide composition of mitochondrial genomes in parasitic lice from Amblycera. Gene, 768: 145312. doi: 10.1016/j.gene.2020.145312
    Wang CY, Yang PL, Zhao M, et al. 2022. Unusual mitochondrial tRNA rearrangements in stingless bee Tetragonula pagdeni and phylogenetic analysis. Entomological Science, 25(4): e12526. doi: 10.1111/ens.12526
    Wang CY, Zhao M, Wang SJ, et al. 2021. The complete mitochondrial genome of Lepidotrigona flavibasis (Hymenoptera: Meliponini) and high gene rearrangement in Lepidotrigona mitogenomes. Journal of Insect Science, 21(3): 10. doi: 10.1093/jisesa/ieab038
    Wang CY, Zhao M, Xu HL, et al. 2020. Complete mitochondrial genome of the stingless bee Lepidotrigona terminata (Hymenoptera: Meliponinae) and phylogenetic analysis. Mitochondrial DNA Part B, 5(1): 752−753. doi: 10.1080/23802359.2020.1715298
    Wang WW, Lanfear R. 2019. Long–reads reveal that the chloroplast genome exists in two distinct versions in most plants. Genome Biology and Evolution, 11(12): 3372−3381.
    Wei SJ, Shi M, Sharkey MJ, et al. 2010. Comparative mitogenomics of Braconidae (Insecta: Hymenoptera) and the phylogenetic utility of mitochondrial genomes with special reference to Holometabolous insects. BMC Genomics, 11: 371. doi: 10.1186/1471-2164-11-371
    Wick RR, Schultz MB, Zobel J, et al. 2015. Bandage: interactive visualization of de novo genome assemblies. Bioinformatics, 31(20): 3350−3352. doi: 10.1093/bioinformatics/btv383
    Wicke S, Schneeweiss GM, DePamphilis CW, et al. 2011. The evolution of the plastid chromosome in land plants: gene content, gene order, gene function. Plant Molecular Biology, 76(3-5): 273−297. doi: 10.1007/s11103-011-9762-4
    Xiao JH, Jia JG, Murphy RW, et al. 2011. Rapid evolution of the mitochondrial genome in Chalcidoid wasps (Hymenoptera: Chalcidoidea) driven by parasitic lifestyles. PLoS One, 6(11): e26645. doi: 10.1371/journal.pone.0026645
    Yang ZH. 1998. Likelihood ratio tests for detecting positive selection and application to primate lysozyme evolution. Molecular Biology and Evolution, 15(5): 568−573. doi: 10.1093/oxfordjournals.molbev.a025957
    Yang ZH. 1997. PAML: a program package for phylogenetic analysis by maximum likelihood. Bioinformatics, 13(5): 555−556. doi: 10.1093/bioinformatics/13.5.555
    Yang ZH. 2007. PAML 4: phylogenetic analysis by maximum likelihood. Molecular Biology and Evolution, 24(7): 1586−1591.
    Yokobori SI, Fukuda N, Nakamura M, et al. 2004. Long–term conservation of six duplicated structural genes in cephalopod mitochondrial genomes. Molecular Biology and Evolution, 21(11): 2034−2046. doi: 10.1093/molbev/msh227
    Zhang DX, Hewitt GM. 1997. Insect mitochondrial control region: a review of its structure, evolution and usefulness in evolutionary studies. Biochemical Systematics and Ecology, 25(2): 99−120. doi: 10.1016/S0305-1978(96)00042-7
    Zhang DX, Szymura JM, Hewitt GM. 1995. Evolution and structural conservation of the control region of insect mitochondrial DNA. Journal of Molecular Evolution, 40(4): 382−391. doi: 10.1007/BF00164024
    Zheng BY, Cao LJ, Tang P, et al. 2018. Gene arrangement and sequence of mitochondrial genomes yield insights into the phylogeny and evolution of bees and sphecid wasps (Hymenoptera: Apoidea). Molecular Phylogenetics and Evolution, 124: 1−9. doi: 10.1016/j.ympev.2018.02.028
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