Phylogenetic insights on the delineation of Mysore and Malabar subspecies of the Grey Slender Loris Loris lydekkerianus in southern India
DOI:
https://doi.org/10.11609/jott.8491.15.9.23827-23835Keywords:
Grey Slender Loris, Malabar Slender Loris, molecular dating, Mysore Slender Loris, phylogeneticsAbstract
Slender lorises are a threatened genus of small and nocturnal strepsirrhine primates confined to India and Sri Lanka. The Grey Slender Loris Loris lydekkerianus is divided into several subspecies based on morphological variation and geographical distribution but not supported by molecular data. We investigated the phylogenetic divergence of two subspecies of the Grey Slender Loris in southern India: the Mysore Slender Loris Loris lydekkerianus ssp. lydekkerianus and the Malabar Slender Loris Loris lydekkerianus ssp. malabaricus. We generated whole genome shotgun sequence data and assembled the whole mitochondrial genomes of representative individuals from their distribution in southern India and compared them with publicly available mitogenomes of other lorises. We found that the Mysore and Malabar Slender Lorises vary by 2.09% in the COX1 and CYTB gene regions. Further, phylogenetic analysis of 13 protein-coding and two ribosomal RNA genes in the mitochondrial genome showed that the Mysore and Malabar Slender Lorises form distinct monophyletic clades that diverged about 1.049 million years ago, shortly after the divergence of Red Slender Loris Loris tardigradus. Considering this relatively high sequence variation and evolutionary divergence together with their already established morphological differences and geographically distinct habitats, we propose to recognize the Mysore and Malabar Slender Lorises as two distinct species Loris lydekkerianus and Loris malabaricus.
References
Bernt, M., A. Donath, F. Jühling, F. Externbrink, C. Florentz, G. Fritzsch, J. Pütz, M. Middendorf & P.F. Stadler (2013). MITOS: improved de novo metazoan mitochondrial genome annotation. Molecular Phylogenetics and Evolution 69(2): 313–319. https://doi.org/10.1016/j.ympev.2012.08.023
Bouckaert, R., J. Heled, D. Kühnert, T. Vaughan, C.-H. Wu, D. Xie, M.A. Suchard, A. Rambaut & A.J. Drummond (2014). BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Computational Biology 10(4): e1003537. https://doi.org/10.1371/journal.pcbi.1003537
Chen, S., Y. Zhou, Y. Chen & J. Gu (2018). fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 34(17): i884–i890. https://doi.org/10.1093/bioinformatics/bty560
Dittus, W., M. Singh, S.N. Gamage, H.N. Kumara, A. Kumar & K.A.I. Nekaris (2022). Loris lydekkerianus (amended version of 2020 assessment). The IUCN Red List of Threatened Species 2022: e.T44722A217741551. Downloaded on 28 March 2023. https://doi.org/10.2305/IUCN.UK.2022-1.RLTS.T44722A217741551.en
Finstermeier, K., D. Zinner, M. Brameier, M. Meyer, E. Kreuz, M. Hofreiter & C. Roos (2013). A mitogenomic phylogeny of living primates. PLoS ONE 8(7): e69504. https://doi.org/10.1371/journal.pone.0069504
Gnanaolivu, S.D., M. Campera, K.A.I. Nekaris, V. Nijman, R. Satish, S. Babu & M. Singh (2022). Medicine, black magic and supernatural beings: Cultural rituals as a significant threat to slender lorises in India. People and Nature 4(4): 1007–1019. https://doi.org/10.1002/pan3.10336
Government of Tamil Nadu (2022). Notification of Kadavur Slender Loris Sanctuary in Karur and Dindigul districts of the Wild Life (Protection) Act, 1972. [G.O. Ms. No. 175, Environment, Climate Change and Forests (FR.5), 12th October 2022] No. II(2)/ECCF/809(a)/2022.
Groves, C.P. (2001). Primate taxonomy. Smithsonian Institution Press, Washington (DC), 350 pp.
Harrison, T. (2010). Later tertiary Lorisiformes, pp. 875–912. In: Werdelin, L. & W.J. Sanders (eds.). Cenozoic Mammals of Africa. University of California Press, California, 1008 pp.
Helfrich, P., E. Rieb, G. Abrami, A. Lücking & A. Mehler (2018). TreeAnnotator: Versatile Visual Annotation of Hierarchical Text Relations. In: Proceedings of the Eleventh International Conference on Language Resources and Evaluation (LREC 2018). European Language Resources Association (ELRA), Miyazaki, Japan.
Herbert, T.D. (2023). The mid-Pleistocene climate transition. Annual Review of Earth and Planetary Sciences 51(1): 389–418. https://doi.org/10.1146/annurev-earth-032320-104209
Jin, J.J., W.B. Yu, J.B. Yang, Y. Song, C.W. DePamphilis, T.S. Yi & D.Z. Li (2020). GetOrganelle: a fast and versatile toolkit for accurate de novo assembly of organelle genomes. Genome Biology 21: 1–31. https://doi.org/10.1186/s13059-020-02154-5
Kumar, S., G. Stecher & K. Tamura (2016). MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33(7): 1870–1874. https://doi.org/10.1093/molbev/msw054
Kumara, H.N., K.A.I. Nekaris & M. Singh (2022a). Loris lydekkerianus ssp. lydekkerianus. The IUCN Red List of Threatened Species 2022: e.T44719A217742793. Downloaded on 28 March 2023. https://doi.org/10.2305/IUCN.UK.2022-1.RLTS.T44719A217742793.en
Kumara, H.N., K.A.I. Nekaris & M. Singh (2022b). Loris lydekkerianus ssp. malabaricus (amended version of 2020 assessment). The IUCN Red List of Threatened Species 2022: e.T44720A217744540. Downloaded on 28 March 2023. https://doi.org/10.2305/IUCN.UK.2022-1.RLTS.T44720A217744540.en
Kumara, H.N., M. Singh & S. Kumar (2006). Distribution, habitat correlates, and conservation of Loris lydekkerianus in Karnataka, India. International Journal of Primatology 27: 941–969. https://doi.org/10.1007/s10764-006-9054-z
Kumara, H.N., M. Irfan-Ullah & S. Kumar (2009). Mapping potential distribution of slender loris subspecies in peninsular India. Endangered Species Research 7: 29–38. https://doi.org/10.3354/esr00185
Kumara, H.N., R. Sasi, S. Chandran & S. Radhakrishna (2016). Distribution of the Grey Slender Loris (Loris lyddekerianus Cabrera, 1908) in Tamil Nadu, southern India. Folia Primatologica 87(5): 291–302. https://doi.org/10.1159/000452405
Kumara, H.N., M. Singh, M. Irfan-Ullah & S. Kumar (2013). Status, Distribution, and Conservation of Slender Lorises in India pp. 343–352. In: Masters, J., M. Gamba & F. Génin (eds.). Leaping Ahead: Advances in Prosimian Biology. Springer, New York, 410 pp.
Lanfear, R., P.B. Frandsen, A.M. Wright, T. Senfeld & B. Calcott (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. https://doi.org/10.1093/molbev/msw260
Minh, B.Q., H.A. Schmidt, O. Chernomor, D. Schrempf, M.D. Woodhams, A. von Haeseler & R. Lanfear (2020). IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era. Molecular Biology and Evolution 37(5): 1530–1534. https://doi.org/10.1093/molbev/msaa015
Morley, R.J. & H.P. Morley (2022). The prelude to the Holocene: tropical Asia during the Pleistocene, pp. 1–32. In: Kumaran, N. & P. Damodara (eds.). Holocene Climate Change and Environment. Elsevier, 661 pp.
Nekaris, K.A.I. (2014). Extreme primates: ecology and evolution of Asian lorises. Evolutionary Anthropology: Issues, News, and Reviews 23(5): 177–187. https://doi.org/10.1002/evan.21425
Nekaris, K.A.I. & D.T. Rasmussen (2003). Diet and feeding behavior of Mysore Slender Lorises. International Journal of Primatology 24(1): 33–46. https://doi.org/10.1023/A:1021442411455
Nijman, V., T. Robbins, A.J. Maddock & A. Ang (2020). Molecular phylogeny, taxonomy and conservation of slender Lorises. Primate Conservation 34: 143–151.
Radhakrishna, S. & H.N. Kumara (2010). Behavioural variation in the Mysore slender loris Loris lydekkerianus lydekkerianus. Current Science 99(9): 1226–1232.
Radhakrishna, S. & M. Singh (2002). Social behaviour of the slender loris (Loris tardigradus lydekkerianus). Folia Primatologica 73(4): 181–196. https://doi.org/10.1159/000065426
Radhakrishna, S. & M. Singh (2004). Reproductive biology of the slender loris (Loris lydekkerianus lydekkerianus). Folia Primatologica 75(1): 1–13. https://doi.org/10.1159/000073424
Rambaut, A. (2014). FigTree, a graphical viewer of phylogenetic trees. https://github.com/rambaut/figtree Accessed on 15 March 2023.
Rambaut, A., A.J. Drummond, D. Xie, G. Baele & M.A. Suchard (2018). Posterior summarization in Bayesian phylogenetics Using Tracer 1.7. Systematic Biology 67(5): 901–904. https://doi.org/10.1093/sysbio/syy032
Seiffert, E.R., E.L. Simons & Y. Attia (2003). Fossil evidence for an ancient divergence of lorises and galagos. Nature 422(6930): 421–424. https://doi.org/10.1038/nature01489
Sievers, F. & D.G. Higgins (2021). The Clustal Omega Multiple Alignment Package, pp. 3–16. In: Katoh, K. (ed.). Multiple Sequence Alignment: Methods and Protocols. Springer US, New York, 287 pp.
Singh, M., M. Singh, H.N. Kumara, S. Kumar, S.D. Gnanaoliu & R. Sasi (2021). A review of research on the distribution, ecology, behaviour, and conservation of the Slender Loris Loris lydekkerianus (Mammalia: Primates: Lorisidae) in India. Journal of Threatened Taxa 13(11): 19540–19552. https://doi.org/10.11609/jott.7562.13.11.19540-19552
Subramanian, B., S. Gao, M.J. Lercher, S. Hu & W.H. Chen (2019). Evolview v3: a webserver for visualization, annotation, and management of phylogenetic trees. Nucleic Acids Research 47(W1): W270–W275. https://doi.org/10.1093/nar/gkz357
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