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Mitogenomics of endemic Ethiopian shrews: looking for footprints of adaptive evolution along a remarkable altitudinal gradient

  • Elena D. Zemlemerova ORCID logo EMAIL logo , Valeria A. Komarova ORCID logo and Leonid A. Lavrenchenko ORCID logo
Published/Copyright: April 7, 2025
Mammalia
From the journal Mammalia

Abstract

Mitochondria provide most of energy in animal cells through oxidative phosphorylation; therefore, the evaluation of selective pressures on the mitochondrial genome can yield valuable insights into evolution of adaptations to different energy requirements within unique environments. The distribution of East African shrews is directly related to an altitudinal gradient, implying their high level of adaptive divergence and making them a unique model for revealing molecular mechanisms of the adaptation. Here we analysed signs of adaptive evolution in 17 mitogenomes of endemic Ethiopian white-toothed shrews (three ecotypes of Crocidura glassi s.l.) that replace each other in adjacent altitudinal belts of the Bale Massif, possibly indicating large adaptive divergence. To test this hypothesis, we used a combination of different methods besides classic tests of selection; we also analysed physicochemical changes of amino acid properties in protein-coding genes. None of the analyses yielded significant results on positive selection. We can theorize that purifying selection might have been a common selection pattern for mitochondrial genes in C. glassi s.l. ecotypes. Finally, different environmental adaptations – reflecting organisms’ various strategies and possibly important in white-toothed shrews – are discussed.


Corresponding author: Elena D. Zemlemerova, A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninsky Pr. 33, Moscow 119081, Russia, E-mail:

Award Identifier / Grant number: №23-74-01098

Acknowledgments

We are indebted to the Ethiopian Wildlife Conservation Authority (EWCA) for the permission to work in the Bale Mountains National Park. We thank the warden and staff of the Bale Mountains National Park for the use of the Park buildings and equipment. We are grateful to the JERBE Coordinators Dr. Andrei Darkov (Joint Ethio-Russian Biological Expedition, Fourth Phase – JERBE-IV) and Ato Girma Yosef (Ethiopian Ministry of Science and Technology) for management of the expedition in the field and in Addis Ababa. The English language was corrected by shevchuk-editing.com.

  1. Research ethics: All fieldwork complied with legal regulations in Ethiopia and sampling was carried out with the permission of the Ethiopian Wildlife Conservation Authority (no. EWCA ref. no. 31/336/05; 20/03/2013).

  2. Informed consent: Not applicable.

  3. Author contributions: All authors have accepted responsibility for the entire content of the submitted manuscript and have approved it.

  4. Use of Large Language Models, AI and Machine Learning Tools: None declared.

  5. Conflict of interest: The authors state no conflict of interest.

  6. Research funding: This study was funded by the Russian Science Foundation (RSF) No. 23-74-01098 (https://rscf.ru/en/project/23-74-01098/).

  7. Data availability: All data are available in the Section of Mammalogy of the Zoological Museum of Moscow University and the sequences obtained can be accessed via GenBank.

References

Almeida, D., Maldonado, E., Vasconcelos, V., and Antunes, A. (2015). Adaptation of the mitochondrial genome in cephalopods: enhancing proton translocation channels and the subunit interactions. PLoS One 10: e0135405, https://doi.org/10.1371/journal.pone.0135405.Search in Google Scholar PubMed PubMed Central

Arya, M., Ghosh, A., Tyagi, K., Tyagi, I., Bisht, S.S., and Kumar, V. (2024). Characterization of complete mitochondrial genome of badri breed of Bos indicus (Bovidae: Bovinae): selection pressure and comparative analysis. Biochem. Genet., https://doi.org/10.1007/s10528–024–10691–y (Epub ahead of print).10.1007/s10528-024-10691-ySearch in Google Scholar PubMed

Ballard, J.W.O. and Kreitman, M. (1995). Is mitochondrial DNA a strictly neutral marker? Trends Ecol. Evol. 10: 485–488, https://doi.org/10.1016/s0169-5347(00)89195-8.Search in Google Scholar PubMed

Bartáková, V., Bryjová, A., Nicolas, V., Lavrenchenko, L.A., and Bryja, J. (2021). Mitogenomics of the endemic Ethiopian rats: looking for footprints of adaptive evolution in sky islands. Mitochondrion 57: 182–191, https://doi.org/10.1016/j.mito.2020.12.015.Search in Google Scholar PubMed

Baxter, R.M., Dippenaar, N.J., and Meester, J. (1981). The moult pattern of some southern African Soricidae. Mammalia 45: 355–361, https://doi.org/10.1515/mamm.1981.45.3.355.Search in Google Scholar

Bertrand, J.A., Delahaie, B., Bourgeois, Y.X., Duval, T., García-Jiménez, R., Cornuault, J., Bujol, B., Thébaud, C., and Milá, B. (2016). The role of selection and historical factors in driving population differentiation along an elevational gradient in an island bird. J. Evol. Biol. 29: 824–836, https://doi.org/10.1111/jeb.12829.Search in Google Scholar PubMed

Boore, J.L. (1999). Animal mitochondrial genomes. Nucleic Acids Res. 27: 1767–1780, https://doi.org/10.1093/nar/27.8.1767.Search in Google Scholar PubMed PubMed Central

Boratyński, Z., Melo-Ferreira, J., Alves, P.C., Berto, S., Koskela, E., Pentikäinen, O.T., Tarroso, P., Ylilauri, M., and Mappes, T. (2014). Molecular and ecological signs of mitochondrial adaptation: consequences for introgression? Heredity 113: 277–286, https://doi.org/10.1038/hdy.2014.28.Search in Google Scholar PubMed PubMed Central

Bryja, J., Kostin, D., Meheretu, Y., Šumbera, R., Bryjová, A., Kasso, M., Mikula, O., and Lavrenchenko, L.A. (2018). Reticulate Pleistocene evolution of Ethiopian rodent genus along remarkable altitudinal gradient. Mol. Phylogenet. Evol. 118: 75–87, https://doi.org/10.1016/j.ympev.2017.09.020.Search in Google Scholar PubMed

Burtscher, J., Mallet, R.T., Pialoux, V., Millet, G.P., and Burtscher, M. (2022). Adaptive responses to hypoxia and/or hyperoxia in humans. Antioxid. Redox Signaling 37: 887–912, https://doi.org/10.1089/ars.2021.0280.Search in Google Scholar PubMed

da Fonseca, R.R., Johnson, W.E., O’Brien, S.J., Ramos, M.J., and Antunes, A. (2008). The adaptive evolution of the mammalian mitochondrial genome. BMC Genomics 9: 1–22.10.1186/1471-2164-9-119Search in Google Scholar PubMed PubMed Central

Dippenaar, N.J. (1980). New species of Crocidura from Ethiopia and Northern Tanzania (mammalia: Soricidae). Ann. Transvaal Mus. 32: 125–154.Search in Google Scholar

Dosek, A., Ohno, H., Acs, Z., Taylor, A.W., and Radak, Z. (2007). High altitude and oxidative stress. Respir. Physiol. Neurobiol. 158: 128–131, https://doi.org/10.1016/j.resp.2007.03.013.Search in Google Scholar PubMed

Fontanillas, P., Dépraz, A., Giorgi, M.S., and Perrin, N. (2005). Nonshivering thermogenesis capacity associated to mitochondrial DNA haplotypes and gender in the greater white‐toothed shrew, Crocidura russula. Mol. Ecol. 14: 661–670, https://doi.org/10.1111/j.1365-294x.2004.02414.x.Search in Google Scholar PubMed

Friedrich, J. and Wiener, P. (2020). Selection signatures for high‐altitude adaptation in ruminants. Anim. Genet. 51: 157–165, https://doi.org/10.1111/age.12900.Search in Google Scholar PubMed

Galtier, N., Nabholz, B., Glémin, S., and Hurst, G.D.D. (2009). Mitochondrial DNA as a marker of molecular diversity: a reappraisal. Mol. Ecol. 18: 4541–4550, https://doi.org/10.1111/j.1365-294x.2009.04380.x.Search in Google Scholar

Gao, F., Chen, C., Arab, D.A., Du, Z., He, Y., and Ho, S.Y. (2019). EasyCodeML: a visual tool for analysis of selection using CodeML. Ecol. Evol. 9: 3891–3898, https://doi.org/10.1002/ece3.5015.Search in Google Scholar PubMed PubMed Central

Gershoni, M., Templeton, A.R., and Mishmar, D. (2009). Mitochondrial bioenergetics as a major motive force of speciation. Bioessays 31: 642–650, https://doi.org/10.1002/bies.200800139.Search in Google Scholar PubMed

Graham, A.M., Lavretsky, P., Wilson, R.E., and McCracken, K.G. (2024). High-altitude adaptation is accompanied by strong signatures of purifying selection in the mitochondrial genomes of three Andean waterfowl. PLoS One 19: e0294842, https://doi.org/10.1371/journal.pone.0294842.Search in Google Scholar PubMed PubMed Central

Gutiérrez, E.G., Ortega, J., Savoie, A., and Baeza, J.A. (2023). The mitochondrial genome of the mountain wooly tapir, Tapirus pinchaque and a formal test of the effect of altitude on the adaptive evolution of mitochondrial protein coding genes in odd–toed ungulates. BMC Genomics 24: 527, https://doi.org/10.1186/s12864-023-09596-8.Search in Google Scholar PubMed PubMed Central

Hassanin, A., Ropiquet, A., Couloux, A., and Cruaud, C. (2009). Evolution of the mitochondrial genome in mammals living at high altitude: new insights from a study of the tribe Caprini (Bovidae, Antilopinae). J. Mol. Evol. 68: 293–310, https://doi.org/10.1007/s00239-009-9208-7.Search in Google Scholar PubMed

Huntley, B. and Webb, I.I.I., T. (1989). Migration: species’ response to climatic variations caused by changes in the earth’s orbit. J. Biogeogr. 16: 5–19, https://doi.org/10.2307/2845307.Search in Google Scholar

Irwin, D.M., Kocher, T.D., and Wilson, A.C. (1991). Evolution of the cytochrome b gene of mammals. J. Mol. Evol. 32: 128–144, https://doi.org/10.1007/bf02515385.Search in Google Scholar PubMed

James, J.E., Piganeau, G., and Eyre‐Walker, A. (2016). The rate of adaptive evolution in animal mitochondria. Mol. Ecol. 25: 67–78, https://doi.org/10.1111/mec.13475.Search in Google Scholar PubMed PubMed Central

Jin, Y., Wo, Y., Tong, H., Song, S., Zhang, L., and Brown, R.P. (2018). Evolutionary analysis of mitochondrially encoded proteins of toad-headed lizards, Phrynocephalus, along an altitudinal gradient. BMC Genomics 19: 1–11, https://doi.org/10.1186/s12864-018-4569-1.Search in Google Scholar PubMed PubMed Central

Keller, I., Alexander, J.M., Holderegger, R., and Edwards, P.J. (2013). Widespread phenotypic and genetic divergence along altitudinal gradients in animals. J. Evol. Biol. 26: 2527–2543, https://doi.org/10.1111/jeb.12255.Search in Google Scholar PubMed

Kimura, M. (1980). A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120, https://doi.org/10.1007/bf01731581.Search in Google Scholar PubMed

Kosakovsky Pond, S.L. and Frost, S.D. (2005). Datamonkey: rapid detection of selective pressure on individual sites of codon alignments. Bioinformatics 21: 2531–2533, https://doi.org/10.1093/bioinformatics/bti320.Search in Google Scholar PubMed

Kostin, D.S. and Lavrenchenko, L.A. (2018). Adaptation of rodents living in a highland: combination of mitochondrial introgression and convergent molecular evolution. Dokl. Biochem. Biophys. 483: 333–336, https://doi.org/10.1134/s160767291806011x.Search in Google Scholar

Kostin, D.S., Kasso, M., Komarova, V.A., Martynov, A.A., Gromov, A.R., Alexandrov, D.Y., Bekele, A., Zewdie, C., Bryja, J., and Lavrenchenko, L.A. (2019). Taxonomic and genetic diversity of rodents from the Arsi Mountains (Ethiopia). Mammalia 83: 237–247, https://doi.org/10.1515/mammalia-2017-0135.Search in Google Scholar

Kumar, S., Stecher, G., and 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.Search in Google Scholar PubMed PubMed Central

Lanfear, R., Calcott, B., Ho, S.Y., and Guindon, S. (2012). PartitionFinder: combined selection of partitioning schemes and substitution models for phylogenetic analyses. Mol. Biol. Evol. 29: 1695–1701, https://doi.org/10.1093/molbev/mss020.Search in Google Scholar PubMed

Lavrenchenko, L.A., Bannikova, A.A., and Lebedev, V.S. (2009). Shrews (Crocidura spp.) endemic to Ethiopia: recent adaptive radiation of an ancient lineage. Dokl. Biol. Sci. 424: 57–60, https://doi.org/10.1134/s0012496609010177.Search in Google Scholar PubMed

Lavrenchenko, L.A., Voyta, L.L., and Hutterer, R. (2016). Diversity of shrews in Ethiopia, with the description of two new species of Crocidura (Mammalia: Lipotyphla: Soricidae). Zootaxa 4196: 38–60, https://doi.org/10.11646/zootaxa.4196.1.2.Search in Google Scholar PubMed

Maldonado, E., Sunagar, K., Almeida, D., Vasconcelos, V., and Antunes, A. (2014). IMPACT_S: integrated multiprogram platform to analyze and combine tests of selection. PLoS One 9: e96243, https://doi.org/10.1371/journal.pone.0096243.Search in Google Scholar PubMed PubMed Central

McClellan, D.A. and Ellison, D.D. (2010). Assessing and improving the accuracy of detecting protein adaptation with the TreeSAAP analytical software. Int. J. Bioinf. Res. Appl. 6: 120–133, https://doi.org/10.1504/ijbra.2010.032116.Search in Google Scholar

Meng, G., Li, Y., Yang, C., and Liu, S. (2019). MitoZ: a toolkit for mitochondrial genome assembly, annotation, and visualization. Nucleic Acids Res. 47: e63, https://doi.org/10.1093/nar/gkz173.Search in Google Scholar PubMed PubMed Central

Minh, B.Q., Nguyen, M.A.T., and Von Haeseler, A. (2013). Ultrafast approximation for phylogenetic bootstrap. Mol. Biol. Evol. 30: 1188–1195, https://doi.org/10.1093/molbev/mst024.Search in Google Scholar PubMed PubMed Central

Mizerovská, D., Mikula, O., Meheretu, Y., Bartáková, V., Bryjová, A., Kostin, D.S., Šumbera, R., Lavrenchenko, L.A., and Bryja, J. (2020). Integrative taxonomic revision of the Ethiopian endemic rodent genus Stenocephalemys (Muridae: Murinae: Praomyini) with the description of two new species. J. Vertebr. Biol. 69: 20031.10.25225/jvb.20031Search in Google Scholar

Mizerovská, D., Špoutil, F., Claude, J., Lavrenchenko, L.A., Procházka, J., Bryja, J., and Mikula, O. (2023). Parallel evolution of skull form in three rodent genera inhabiting steep elevational gradients of Ethiopian highlands. Evol. Biol. 50: 332–349, https://doi.org/10.1007/s11692-023-09608-1.Search in Google Scholar

Morales, H.E., Pavlova, A., Joseph, L., and Sunnucks, P. (2015). Positive and purifying selection in mitochondrial genomes of a bird with mitonuclear discordance. Mol. Ecol. 24: 2820–2837, https://doi.org/10.1111/mec.13203.Search in Google Scholar PubMed

Murrell, B., Wertheim, J.O., Moola, S., Weighill, T., Scheffler, K., and Kosakovsky Pond, S.L. (2012). Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 8: e1002764, https://doi.org/10.1371/journal.pgen.1002764.Search in Google Scholar PubMed PubMed Central

Murrell, B., Moola, S., Mabona, A., Weighill, T., Sheward, D., Kosakovsky Pond, S.L., and Scheffler, K. (2013). FUBAR: a fast, unconstrained Bayesian approximation for inferring selection. Mol. Biol. Evol. 30: 1196–1205, https://doi.org/10.1093/molbev/mst030.Search in Google Scholar PubMed PubMed Central

Nabhan, A.R. and Sarkar, I.N. (2012). The impact of taxon sampling on phylogenetic inference: a review of two decades of controversy. Briefings Bioinf. 13: 122–134, https://doi.org/10.1093/bib/bbr014.Search in Google Scholar PubMed PubMed Central

Nguyen, L.T., Schmidt, H.A., Von Haeseler, A., and Minh, B.Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol. Biol. Evol. 32: 268–274, https://doi.org/10.1093/molbev/msu300.Search in Google Scholar PubMed PubMed Central

Nielsen, R. (2005). Molecular signatures of natural selection. Annu. Rev. Genet. 39: 197–218, https://doi.org/10.1146/annurev.genet.39.073003.112420.Search in Google Scholar PubMed

Oliveira, F.G., Tapisso, J.T., Monarca, R.I., Cerveira, A.M., and Mathias, M.L. (2016). Phenotypic flexibility in the energetic strategy of the greater white-toothed shrew, Crocidura russula. J. Therm. Biol. 56: 10–17, https://doi.org/10.1016/j.jtherbio.2015.12.002.Search in Google Scholar PubMed

Pallares, L.F., Harr, B., Turner, L.M., and Tautz, D. (2014). Use of a natural hybrid zone for genomewide association mapping of craniofacial traits in the house mouse. Mol. Ecol. 23: 5756–5770, https://doi.org/10.1111/mec.12968.Search in Google Scholar PubMed

Pallares, L.F., Turner, L.M., and Tautz, D. (2016). Craniofacial shape transition across the house mouse hybrid zone: implications for the genetic architecture and evolution of between-species differences. Dev. Gene. Evol. 226: 173–186, https://doi.org/10.1007/s00427-016-0550-7.Search in Google Scholar PubMed PubMed Central

Ronquist, F., Teslenko, M., Van Der Mark, P., Ayres, D.L., Darling, A., Höhna, S., Larget, B., Liu, L., Suchard, M.A., and Huelsenbeck, J.P. (2012). MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst. Biol. 61: 539–542, https://doi.org/10.1093/sysbio/sys029.Search in Google Scholar PubMed PubMed Central

Rose, R., Golosova, O., Sukhomlinov, D., Tiunov, A., and Prosperi, M. (2019). Flexible design of multiple metagenomics classification pipelines with UGENE. Bioinformatics 35: 1963–1965, https://doi.org/10.1093/bioinformatics/bty901.Search in Google Scholar PubMed

Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular cloning: a laboratory manual. Cold Spring Harbor Lab. Press, New York.Search in Google Scholar

Shen, Y.-Y., Liang, L., Zhu, Z.-H., Zhou, W.-P., Irwin, D.M., and Zhang, Y.-P. (2010). Adaptive evolution of energy metabolism genes and the origin of flight in bats. PNAS 107: 8666–8671, https://doi.org/10.1073/pnas.0912613107.Search in Google Scholar PubMed PubMed Central

Smith, M.D., Wertheim, J.O., Weaver, S., Murrell, B., Scheffler, K., and Kosakovsky Pond, S.L. (2015). Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Mol. Biol. Evol. 32: 2389–2401, https://doi.org/10.1093/molbev/msv022.Search in Google Scholar PubMed PubMed Central

Sparti, A. (1990). Comparative temperature regulation of African and European shrew. Comp. Biochem. Physiol. Part A: Physiol. 97: 391–397, https://doi.org/10.1016/0300-9629(90)90629-7.Search in Google Scholar

Szalay, F.S. and Delson, E. (1979). Evolutionary history of the primates. Academic Press, New York.Search in Google Scholar

Tomasco, I.H. and Lessa, E.P. (2014). Two mitochondrial genes under episodic positive selection in subterranean octodontoid rodents. Gene 534: 371–378, https://doi.org/10.1016/j.gene.2013.09.097.Search in Google Scholar PubMed

Vogel, P. (1976). Energy consumption of European and African shrews. Acta Theriologica 21: 195–206, https://doi.org/10.4098/at.arch.76-18.Search in Google Scholar

Vogel, P., Burgener, M., Lardet, J.P., Genoud, M., and Frey, H. (1979). Influence de la température et de la nourriture disponible sur la torpeur chez la musaraigne musette (Crocidura russula) en captivité. Bulletin de la Société Vaudoise des Sciences Naturelles 74: 325–332.Search in Google Scholar

Weaver, S., Shank, S.D., Spielman, S.J., Li, M., Muse, S.V., and Kosakovsky Pond, S.L. (2018). Datamonkey 2.0: a modern web application for characterizing selective and other evolutionary processes. Mol. Biol. Evol. 35: 773–777, https://doi.org/10.1093/molbev/msx335.Search in Google Scholar PubMed PubMed Central

Woolley, S., Johnson, J., Smith, M.J., Crandall, K.A., and McClellan, D.A. (2003). TreeSAAP: selection on amino acid properties using phylogenetic trees. Bioinformatics 19: 671–672, https://doi.org/10.1093/bioinformatics/btg043.Search in Google Scholar PubMed

Yang, Z. and Nielsen, R. (2002). Codon-substitution models for detecting molecular adaptation at individual sites along specific lineages. Mol. Biol. Evol. 19: 908–917, https://doi.org/10.1093/oxfordjournals.molbev.a004148.Search in Google Scholar PubMed

Yang, Z., Nielsen, R., Goldman, N., and Pedersen, A.M.K. (2000). Codon–substitution models for heterogeneous selection pressure at amino acid sites. Genetics 155: 431–449, https://doi.org/10.1093/genetics/155.1.431.Search in Google Scholar PubMed PubMed Central

Yang, Z., Wong, W.S., and Nielsen, R. (2005). Bayes empirical bayes inference of amino acid sites under positive selection. Mol. Biol. Evol. 22: 1107–1118, https://doi.org/10.1093/molbev/msi097.Search in Google Scholar PubMed

Yu, L., Wang, X., Ting, N., and Zhang, Y. (2011). Mitogenomic analysis of Chinese snub-nosed monkeys: evidence of positive selection in NADH dehydrogenase genes in high-altitude adaptation. Mitochondrion 11: 497–503, https://doi.org/10.1016/j.mito.2011.01.004.Search in Google Scholar PubMed

Yuan, M.L., Zhang, L.J., Zhang, Q.L., Zhang, L., Li, M., Wang, X.T., Feng, R.Q., and Tang, P.A. (2020). Mitogenome evolution in ladybirds: potential association with dietary adaptation. Ecol. Evol. 10: 1042–1053, https://doi.org/10.1002/ece3.5971.Search in Google Scholar PubMed PubMed Central

Zemlemerova, E.D., Martynov, A.A., Sycheva, V.B., and Lavrenchenko, L.A. (2024). The usage of historical DNA and geometric morphometric approach for detecting the ecological diversification along a remarkable altitudinal gradient. Mamm. Biol. 104: 529–538.10.1007/s42991-024-00428-0Search in Google Scholar

Zhang, J., Nielsen, R., and Yang, Z. (2005). Evaluation of an improved branch-site likelihood method for detecting positive selection at the molecular level. Mol. Biol. Evol. 22: 2472–2479, https://doi.org/10.1093/molbev/msi237.Search in Google Scholar PubMed


Supplementary Material

This article contains supplementary material (https://doi.org/10.1515/mammalia-2024-0149).


Received: 2024-10-16
Accepted: 2025-03-04
Published Online: 2025-04-07

© 2025 Walter de Gruyter GmbH, Berlin/Boston

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