AI Chat Paper
Note: Please note that the following content is generated by AMiner AI. SciOpen does not take any responsibility related to this content.
{{lang === 'zh_CN' ? '文章概述' : 'Summary'}}
{{lang === 'en_US' ? '中' : 'Eng'}}
Chat more with AI
PDF (6 MB)
Collect
Submit Manuscript AI Chat Paper
Show Outline
Outline
Show full outline
Hide outline
Outline
Show full outline
Hide outline
Research Article | Open Access

Mitogenomic variation in the Black-throated Tit (Aegithalos concinnus): Conserved structure, concerted evolution of duplicate control regions and multiple distinct evolutionary lineages

Chuanyin Daia,b,c( )Fumin Leic
Key Laboratory of Ecology of Rare and Endangered Species and Environmental Protection (Guangxi Normal University), Ministry of Education, Guilin, 541006, China
Guangxi Key Laboratory of Rare and Endangered Animal Ecology, Guangxi Normal University, Guilin, 541006, China
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing, 100101, China
Show Author Information

Abstract

The mitochondrial genome is a prominent research topic due to its indispensable role in organisms and its application in many research disciplines. However, few studies have investigated intraspecies mitogenomic variation. In this study, 69 mitogenomes of the Black-throated Tit (Aegithalos concinnus) were assembled and annotated from a large number of short reads generated using high-throughput sequencing technology. Comparative analyses revealed that mitogenomic characteristics such as length, gene and nucleotide composition, codon usage, and duplicated control regions were relatively conserved despite substantial intraspecies morphological changes. Yet, all the individuals from the subspecies A. c. iredalei had one more nucleotide in the 12S rRNA than the other studied subspecies. Phylogenetic analyses showed five distinct lineages based on the complete mitogenomes and the 13 combined protein-coding genes, whereas only four lineages were observed when using the duplicate control regions. Most interestingly, each lineage had both copies of the control regions of the comprising individuals, indicating that the paralogous control regions were more similar than the orthologous sequences from the distinct lineages. This suggested the control regions had undergone concerted evolution. The Black-throated Tit has complex evolutionary history and needs further investigating the taxonomic status of these lineages, as well as the underlying evolutionary processes. Our findings call for more research on intraspecies mitogenomic variation.

References

 

Akiyama, T., Nishida, C., Momose, K., Onuma, M., Takami, K., Masuda, R., 2017. Gene duplication and concerted evolution of mitochondrial DNA in crane species. Mol. Phylogenet. Evol. 106, 158-163.

 

Ballard, J.W.O., Pichaud, N., 2014. Mitochondrial DNA: more than an evolutionary bystander. Funct. Ecol. 28, 218-231.

 

Boore, J.L., 1999. Animal mitochondrial genomes. Nucleic Acids Res. 27, 1767-1780.

 

Burton, R.S., Barreto, F.S., 2012. A disproportionate role for mt DNA in Dobzhansky–Muller incompatibilities? Mol. Ecol. 21, 4942-4957.

 

Castresana, J., 2000. Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol. Biol. Evol. 17, 540-552.

 

Chong, R.A., Mueller, R.L., 2013. Low metabolic rates in salamanders are correlated with weak selective constraints on mitochondrial genes. Evolution 67, 894-899.

 

Dai, C., Hao, Y., He, Y., Lei, F., 2017. The absence of reproductive isolation between non-sister and deeply diverged mitochondrial lineages of the black-throated tit (Aegithalos concinnus) revealed by a multilocus genetic analysis in a contact zone. BMC Evol. Biol. 17, 266.

 

Dai, C., Zhao, N., Wang, W., Lin, C., Gao, B., Yang, X., et al., 2011. Profound climatic effects on two East Asian black-throated tits (Aves: aegithalidae), revealed by ecological niche models and phylogeographic analysis. PLoS One 6, e29329.

 

Das, J., 2006. The role of mitochondrial respiration in physiological and evolutionary adaptation. Bioessays 28, 890-901.

 

Detmer, S.A., Chan, D.C., 2007. Functions and dysfunctions of mitochondrial dynamics. Nat. Rev. Mol. Cell Biol. 8, 870-879.

 

Eberhard, J.R., Wright, T.F., 2016. Rearrangement and evolution of mitochondrial genomes in parrots. Mol. Phylogenet. Evol. 94, 34-46.

 

Edwards, S., Bensch, S., 2009. Looking forwards or looking backwards in avian phylogeography? A comment on Zink and Barrowclough 2008. Mol. Ecol. 18, 2930-2936.

 

Edwards, S.V., Kingan, S.B., Calkins, J.D., Balakrishnan, C.N., Jennings, W.B., Swanson, W.J., et al., 2005. Speciation in birds: genes, geography, and sexual selection. P. Natl. Acad. Sci. USA 102, 6550-6557.

 

Fields, P.D., Obbard, D.J., McTaggart, S.J., Galimov, Y., Little, T.J., Ebert, D., 2018. Mitogenome phylogeographic analysis of a planktonic crustacean. Mol. Phylogenet. Evol. 129, 138-148.

 

Françoso, E., Zuntini, A.R., Ricardo, P.C., Santos, P.K.F., de Souza Araujo, N., Silva, J.P.N., 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. Int. J. Biol. Macromol. 242, 124568.

 

Gissi, C., Pesole, G., Mastrototaro, F., Iannelli, F., Guida, V., Griggio, F., 2010. Hypervariability of ascidian mitochondrial gene order: exposing the myth of deuterostome organelle genome stability. Mol. Biol. Evol. 27, 211-215.

 

Hebert, P.D., Cywinska, A., Ball, S.L., DeWaard, J.R., 2003. Biological identifications through DNA barcodes. Proc. R. Soc. Biol. Sci. Ser. B 270, 313-321.

 

Hill, G.E., 2015. Mitonuclear ecology. Mol. Biol. Evol. 32, 1917-1927.

 

Hill, G.E., 2016. Mitonuclear coevolution as the genesis of speciation and the mitochondrial DNA barcode gap. Ecol. Evol. 6, 5831-5842.

 

Hill, G.E., 2017. The mitonuclear compatibility species concept. Auk 134, 393-409.

 

Hill, G.E., 2019. Reconciling the mitonuclear compatibility species concept with rampant mitochondrial introgression. Integr. Comp. Biol. 59, 912-924.

 

Jin, J., Yu, W., Yang, J., Song, Y., DePamphilis, C.W., Yi, T., et al., 2020. GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biol. 21, 241.

 

Johansson, U.S., Ericson, P.G., Fjeldså, J., Irestedt, M., 2016. The phylogenetic position of the world's smallest passerine, the Pygmy Bushtit Psaltria exilis. Ibis 158, 519-529.

 

Johnsen, A., Kearns, A.M., Omland, K.E., Anmarkrud, J.A., 2017. Sequencing of the complete mitochondrial genome of the common raven Corvus corax (Aves: Corvidae) confirms mitogenome-wide deep lineages and a paraphyletic relationship with the Chihuahuan raven C. cryptoleucus. PLoS One 12, e0187316.

 

Kalyaanamoorthy, S., Minh, B.Q., Wong, T.K., Von Haeseler, A., Jermiin, L.S., 2017. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat. Methods 14, 587-589.

 

Kong, L., Li, Y., Kocot, K.M., Yang, Y., Qi, L., Li, Q., et al., 2020. Mitogenomics reveals phylogenetic relationships of Arcoida (Mollusca, Bivalvia) and multiple independent expansions and contractions in mitochondrial genome size. Mol. Phylogenet. Evol. 150, 106857.

 

Kumar, S., Stecher, G., Li, M., Knyaz, C., Tamura, K., 2018. Mega X: molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35, 1547-1549.

 

Kumazawa, Y., Ota, H., Nishida, M., Ozawa, T., 1996. Gene rearrangements in snake mitochondrial genomes: highly concerted evolution of control-region-like sequences duplicated and inserted into a tRNA gene cluster. Mol. Biol. Evol. 13, 1242-1254.

 

Lait, L.A., Marshall, H.D., Carr, S.M., 2018. Phylogeographic mitogenomics of Atlantic cod Gadus morhua: variation in and among trans-Atlantic, trans-Laurentian, Northern cod, and landlocked fjord populations. Ecol. Evol. 8, 6420-6437.

 

Lanfear, R., Calcott, B., Ho, S.Y., Guindon, S., 2012. PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29, 1695-1701.

 

Li, D.-H., Shi, W., Munroe, T.A., Gong, L., Kong, X.-Y., 2015. Concerted evolution of duplicate control regions in the mitochondria of species of the flatfish family Bothidae (Teleostei: Pleuronectiformes). PLoS One 10, e0134580.

 

Li, G., Zheng, B., Liu, G., 1982. Chinese Fauna Sinica (Aves). Science Press, Beijing.

 

Li, J., Lv, L., Wang, Y., Xi, B., Zhang, Z., 2012. Breeding biology of two sympatric Aegithalos tits with helpers at the nest. J. Ornithol. 153, 273-283.

 

Li, X., Huang, Y., Lei, F., 2015. Comparative mitochondrial genomics and phylogenetic relationships of the Crossoptilon species (Phasianidae, Galliformes). BMC Genom. 16, 42.

 

Liao, D., 1999. Concerted evolution: molecular mechanism and biological implications. Am. J. Hum. Genet. 64, 24-30.

 

Ling, C., Hamada, T., Gao, J., Zhao, G., Sun, D., Shi, W., 2015. MrBayes tgMC 3++: a high performance and resource-efficient GPU-oriented phylogenetic analysis method. IEEE ACM Trans. Comput. Biol. Bioinf 13, 845-854.

 

Lombardo, G., Rambaldi Migliore, N., Colombo, G., Capodiferro, M.R., Formenti, G., Caprioli, M., et al., 2022. The mitogenome relationships and phylogeography of barn swallows (Hirundo rustica). Mol. Biol. Evol. 39, msac113.

 

Lubbe, P., Rawlence, N.J., Kardailsky, O., Robertson, B.C., Day, R., Knapp, M., et al., 2022. Mitogenomes resolve the phylogeography and divergence times within the endemic New Zealand Callaeidae (Aves: Passerida). Zool. J. Linn. Soc. 196, 1451-1463.

 

Lv, Q., Hu, Y., Wen, L., Xu, P., Wang, J., Li, J., 2023. Does research activity affect nest survival of birds? A case study on the black-throated tit (Aegithalos concinnus). Biodivers. Sci. 31, 22570.

 

Lynch, M., 2006. The origins of eukaryotic gene structure. Mol. Biol. Evol. 23, 450-468.

 

Macey, J.R., Larson, A., Ananjeva, N.B., Fang, Z., Papenfuss, T.J., 1997. Two novel gene orders and the role of light-strand replication in rearrangement of the vertebrate mitochondrial genome. Mol. Biol. Evol. 14, 91-104.

 

Mackiewicz, P., Urantówka, A.D., Kroczak, A., Mackiewicz, D., 2019. Resolving phylogenetic relationships within Passeriformes based on mitochondrial genes and inferring the evolution of their mitogenomes in terms of duplications. Genome Biol. Evol. 11, 2824-2849.

 

Meng, G., Li, Y., Yang, C., Liu, S., 2019. MitoZ: a toolkit for animal mitochondrial genome assembly, annotation and visualization. Nucleic Acids Res. 47.

 

Mindell, D.P., Sorenson, M.D., Dimcheff, D.E., 1998. Multiple independent origins of mitochondrial gene order in birds. P. Natl. Acad. Sci. USA 95, 10693-10697.

 

Minh, B.Q., Schmidt, H.A., Chernomor, O., Schrempf, D., Woodhams, M.D., Von Haeseler, A., et al., 2020. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol. Biol. Evol. 37, 1530-1534.

 

Morales, H.E., Pavlova, A., Amos, N., Major, R., Kilian, A., Greening, C., et al., 2018. Concordant divergence of mitogenomes and a mitonuclear gene cluster in bird lineages inhabiting different climates. Nat. Ecol. Evol. 2, 1258-1267.

 

Morris-Pocock, J.A., Taylor, S.A., Birt, T.P., Friesen, V.L., 2010. Concerted evolution of duplicated mitochondrial control regions in three related seabird species. BMC Evol. Biol. 10, 14.

 

Mueller, R.L., Boore, J.L., 2005. Molecular mechanisms of extensive mitochondrial gene rearrangement in plethodontid salamanders. Mol. Biol. Evol. 22, 2104-2112.

 

Ogoh, K., Ohmiya, Y., 2007. Concerted evolution of duplicated control regions within an ostracod mitochondrial genome. Mol. Biol. Evol. 24, 74-78.

 

Päckert, M., Martens, J., Sun, Y.-H., 2010. Phylogeny of long-tailed tits and allies inferred from mitochondrial and nuclear markers (Aves: Passeriformes, Aegithalidae). Mol. Phylogenet. Evol. 55, 952-967.

 

Rand, D.M., Haney, R.A., Fry, A.J., 2004. Cytonuclear coevolution: the genomics of cooperation. Trends Ecol. Evol. 19, 645-653.

 

Roger, A.J., Muñoz-Gómez, S.A., Kamikawa, R., 2017. The origin and diversification of mitochondria. Curr. Biol. 27, R1177-R1192.

 

Rozewicki, J., Li, S., Amada, K.M., Standley, D.M., Katoh, K., 2019. MAFFT-DASH: integrated protein sequence and structural alignment. Nucleic Acids Res. 47, W5-W10.

 

Sammler, S., Ketmaier, V., Havenstein, K., Tiedemann, R., 2013. Intraspecific rearrangement of duplicated mitochondrial control regions in the luzon tarictic hornbill Penelopides manillae (Aves: Bucerotidae). J. Mol. Evol. 77, 199-205.

 

Saraste, M., 1999. Oxidative phosphorylation at the fin de siecle. Science 283, 1488-1493.

 

Schirtzinger, E.E., Tavares, E.S., Gonzales, L.A., Eberhard, J.R., Miyaki, C.Y., Sanchez, J.J., et al., 2012. Multiple independent origins of mitochondrial control region duplications in the order Psittaciformes. Mol. Phylogenet. Evol. 64, 342-356.

 

Shadel, G.S., Clayton, D.A., 1997. Mitochondrial DNA maintenance in vertebrates. Annu. Rev. Biochem. 66, 409-435.

 

Shao, R., Barker, S.C., Mitani, H., Aoki, Y., Fukunaga, M., 2005. Evolution of duplicate control regions in the mitochondrial genomes of metazoa: a case study with Australasian Ixodes ticks. Mol. Biol. Evol. 22, 620-629.

 

Shi, F., Yu, T., Xu, Y., Zhang, S., Niu, Y., Ge, S., et al., 2023. Comparative mitochondrial genomic analysis provides new insights into the evolution of the subfamily Lamiinae (Coleoptera: Cerambycidae). Int. J. Biol. Macromol. 225, 634-647.

 

Shi, W., Gong, L., Yu, H., 2020. Double control regions of some flatfish mitogenomes evolve in a concerted manner. Int. J. Biol. Macromol. 142, 11-17.

 

Sun, C.-H., Liu, H.-Y., Lu, C.-H., 2020. Five new mitogenomes of Phylloscopus (Passeriformes, Phylloscopidae): sequence, structure, and phylogenetic analyses. Int. J. Biol. Macromol. 146, 638-647.

 

Sun, C.-H., Liu, H.-Y., Min, X., Lu, C.-H., 2020. Mitogenome of the little owl Athene noctua and phylogenetic analysis of Strigidae. Int. J. Biol. Macromol. 151, 924-931.

 

Tatarenkov, A., Avise, J.C., 2007. Rapid concerted evolution in animal mitochondrial DNA. Proc. R. Soc. Biol. Sci. Ser. B 274, 1795-1798.

 

Urantówka, A.D., Kroczak, A., Strzała, T., Zaniewicz, G., Kurkowski, M., Mackiewicz, P., 2021. Mitogenomes of Accipitriformes and Cathartiformes were subjected to ancestral and recent duplications followed by gradual degeneration. Genome Biol. Evol. 13, evab193.

 

Van Valen, L.M., Maiorana, V.C., 1980. The archaebacteria and eukaryotic origins. Nature 287, 248-250.

 

Wang, X., Huang, Y., Liu, N., Yang, J., Lei, F., 2015. Seven complete mitochondrial genome sequences of bushtits (Passeriformes, Aegithalidae, Aegithalos): the evolution pattern in duplicated control regions. Mitochondrial DNA 26, 350-356.

 

Wang, X., Liu, N., Zhang, H., Yang, X.-J., Huang, Y., Lei, F., 2015. Extreme variation in patterns of tandem repeats in mitochondrial control region of yellow-browed tits (Sylviparus modestus, Paridae). Sci. Rep. 5, 13227.

 

Wolff, J.N., Ladoukakis, E.D., Enríquez, J.A., Dowling, D.K., 2014. Mitonuclear interactions: evolutionary consequences over multiple biological scales. Philos. Trans. R. Soc. B 369, 20130443.

 

Wolstenholme, D.R., 1992. Animal mitochondrial DNA: structure and evolution. Int. Rev. Cytol. 141, 173-216.

 

Xiang, C.Y., Gao, F., Jakovlić, I., Lei, H.P., Hu, Y., Zhang, H., et al., 2023. Using PhyloSuite for molecular phylogeny and tree-based analyses. iMeta 2, e87.

 

Yang, C., Dong, X., Wang, Q., Hou, X., Yuan, H., Li, X., 2023. Mitochondrial genome characteristics of six Phylloscopus species and their phylogenetic implication. PeerJ 11, e16233.

 

Zardoya, R., 2020. Recent advances in understanding mitochondrial genome diversity. F1000Res 9, F1000.

 

Zhang, D., Gao, F., Jakovlić, I., Zou, H., Zhang, J., Li, W.X., et al., 2020. PhyloSuite: an integrated and scalable desktop platform for streamlined molecular sequence data management and evolutionary phylogenetics studies. Mol. Ecol. Resour. 20, 348-355.

 

Zhang, D., Tang, L., Cheng, Y., Hao, Y., Xiong, Y., Song, G., et al., 2019. "Ghost introgression" as a cause of deep mitochondrial divergence in a bird species complex. Mol. Biol. Evol. 36, 2375-2386.

 

Zink, R.M., Barrowclough, G.F., 2008. Mitochondrial DNA under siege in avian phylogeography. Mol. Ecol. 17, 2107-2121.

Avian Research
Article number: 100210

{{item.num}}

Comments on this article

Go to comment

< Back to all reports

Review Status: {{reviewData.commendedNum}} Commended , {{reviewData.revisionRequiredNum}} Revision Required , {{reviewData.notCommendedNum}} Not Commended Under Peer Review

Review Comment

Close
Close
Cite this article:
Dai C, Lei F. Mitogenomic variation in the Black-throated Tit (Aegithalos concinnus): Conserved structure, concerted evolution of duplicate control regions and multiple distinct evolutionary lineages. Avian Research, 2024, 15(4): 100210. https://doi.org/10.1016/j.avrs.2024.100210

162

Views

2

Downloads

0

Crossref

0

Web of Science

0

Scopus

0

CSCD

Altmetrics

Received: 20 August 2024
Revised: 22 October 2024
Accepted: 22 October 2024
Published: 28 October 2024
© 2024 The Authors.

This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).