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Conservation Genetics

, Volume 16, Issue 1, pp 43–58 | Cite as

Molecules support morphology: species status of South Indian populations of the widely distributed Hanuman langur

  • N. C. Ashalakshmi
  • K. S. Chetan Nag
  • K. Praveen Karanth
Research Article

Abstract

The taxonomy of the Hanuman langur (Semnopithecus spp.), a widely distributed Asian colobine monkey, has been in a flux for a long time due to much disagreement between various classification schemes. However, results from a recent field-based morphological study were consistent with Hill’s (Ceylon J Sci 21:277–305, 1939) species level classification scheme. Here we tested the validity of S. hypoleucos and S. priam, the two South Indian species recognized by Hill. To this end, one mitochondrial and four nuclear markers were sequenced from over 72 non-invasive samples of Hanuman langurs and S. johnii collected from across India. The molecular data were subjected to various tree building methods. The nuclear data was also used in a Bayesian structure analysis and to determine the genealogical sorting index of each hypothesized species. Results from nuclear data suggest that the South Indian population of Hanuman langur consists of two units that correspond to the species recognized by Hill. However in the mitochondrial tree S. johnii and S. priam were polyphyletic probably due to retention of ancestral polymorphism and/or low levels of hybridization. Implications of these results on conservation of Hanuman langurs are also discussed.

Keywords

Systematics Semnopithecus Multi-locus Genetic distance Bayesian structure Genealogical sorting index 

Notes

Acknowledgments

This work was financially supported by the Department of Biotechnology, Government of India (BT/PR-7127/BCE/08/445/2006) and the ministry of Environment and Forests (MoEF), Government of India. We thank the forest departments of Maharashtra, Goa, Karnataka, Kerala, Tamil Nadu, and Andhra Pradesh for Forest permits to collect samples. We are grateful to Sunitha Ram, Dr. Uma Ramkrishnan, Kartik Bala, Manjunath Reddy, Ishan Agarwal, Aniruddha Datta-Roy, Achyuthan and R. S. Harve for providing us with the samples. We are also thankful to Avinash Kedumulor for drawing the maps.

Supplementary material

10592_2014_638_MOESM1_ESM.doc (34 kb)
Supplementary material 1 (DOC 35 kb)
10592_2014_638_MOESM2_ESM.pdf (270 kb)
Supplementary material 2 (PDF 271 kb)

References

  1. Arnold ML, Meyer A (2006) Natural hybridization in primates: one evolutionary mechanism. Zoology 109(4):261–276PubMedCrossRefGoogle Scholar
  2. Campana M, Hunt H, Jones H, White J (2011) CorrSieve: software for summarizing and evaluating structure output. Mol Ecol Resour 11:349–352PubMedCrossRefGoogle Scholar
  3. Cavalli-Sforza LL, Edwards AW (1967) Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19:233–257PubMedCentralPubMedGoogle Scholar
  4. Chellam R (1985) Langurs of Mundanthurai. Blackbuck 1:20–26Google Scholar
  5. Choudhury AU (2007) The eastern limit of distribution of the Hanuman Langur Semnopithecus entellus Dufresene. J Bombay Nat Hist Soc 104:199–200Google Scholar
  6. Cummings MP, Neel MC, Shaw KL (2008) A genealogical approach to quantifying lineage divergence. Evolution 62:2411–2422PubMedCrossRefGoogle Scholar
  7. Davies AG (1994) Colobine populations. In: Davies AG, Oates JF (eds) Colobine monkeys: their ecology, behaviour and evolution. Cambridge University Press, Cambridge, pp 285–310Google Scholar
  8. de Queiroz K (1998) The general lineage concept of species, species criteria, and the process of speciation: a conceptual unification and terminological recommendations. In: Howard DJ, Berlocher SH (eds) Endless forms: species and speciation. Oxford University Press, Oxford, pp 57–75Google Scholar
  9. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56(6):879–886PubMedCrossRefGoogle Scholar
  10. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  11. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedCentralPubMedGoogle Scholar
  12. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedCentralPubMedGoogle Scholar
  13. Funk DJ, Omland KE (2003) Species-level paraphyly and polyphyly: frequency, causes, and consequences, with insights from animal mitochondrial DNA. Annu Rev Ecol Evol Syst 34:397–423CrossRefGoogle Scholar
  14. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7(4):457–472CrossRefGoogle Scholar
  15. Greenwood PJ (1980) Mating systems, philopatry, and dispersal in birds and mammals. Anim Behav 28:1140–1162CrossRefGoogle Scholar
  16. Groeneveld LF, Weisrock DW, Rasoloarison RM, Yoder AD, Kappeler PM (2009) Species delimitation in lemurs: multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus. BMC Evol Biol 9:30PubMedCentralPubMedCrossRefGoogle Scholar
  17. Groves CP (2001) Primate taxonomy. Smithsonian Institution Press, WashingtonGoogle Scholar
  18. Groves CP (2012) Species concept in primates American. J Primatol 74(8):687–691CrossRefGoogle Scholar
  19. Hill WCO (1939) An annotated systematic list of the leaf-monkeys. Ceylon J Sci 21:277–305Google Scholar
  20. Hoelzer GA (1997) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees revisited. Evolution 51:622–626CrossRefGoogle Scholar
  21. Hoelzer GA, Wallman J, Melnick DJ (1998) The effects of social structure, geographical structure, and population size on the evolution of mitochondrial DNA: II. Molecular clocks and the lineage sorting period. J Mol Evol 47:21–31PubMedCrossRefGoogle Scholar
  22. Hohmann G (1988) Analyses of loud calls provide new evidence for hybridisation between two Asian leaf monkeys (Presbytis johnii, P. entellus). Folia Primatol 51:209–213PubMedCrossRefGoogle Scholar
  23. Hohmann G (1991) New evidence for hybridization in Presbytis johnii and Presbytis entellus. J Bombay Nat Hist Soc 88:315–319Google Scholar
  24. Hudson RR, Kaplan NL (1985) Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111:147–164PubMedCentralPubMedGoogle Scholar
  25. Jin L, Chakraborty R (1994) Estimation of Genetic distance and coefficient of gene diversity from single-probe multilocus DNA fingerprinting data. Mol Biol Evol 11(1):120–127PubMedGoogle Scholar
  26. Joly S, Bruneau A (2006) Incorporating allelic variation for reconstructing the evolutionary history of organisms from multiple genes: an example from Rosa in North America. Syst Biol 55:623–636PubMedCrossRefGoogle Scholar
  27. Karanth KP (2008) Primate numts and reticulate evolutions of capped and golden leaf monkeys (Primates: Colobinae). J Biosci 33:761–770PubMedCrossRefGoogle Scholar
  28. Karanth KP (2010) Molecular systematics and conservation of the langurs and leaf monkeys of South Asia. J Genet 89(4):393–399PubMedCrossRefGoogle Scholar
  29. Karanth PK, Singh L, Collura R, Stewart C-B (2008) Molecular phylogeny and biogeography of langurs and leaf monkeys of South Asia (Primates: Colobinae). Mol Phylogenet Evol 46:683–694PubMedCrossRefGoogle Scholar
  30. Karanth PK, Singh L, Stewart C-B (2010) Mitochondrial and nuclear markers suggest Hanuman langur (Primates: Colobinae) polyphyly: implications for their species status. Mol Phylogenet Evol 54:627–633PubMedCrossRefGoogle Scholar
  31. Koenig A, Borries C (2001) Socioecology of Hanuman langurs: the story of their success. Evol Anthropol 10(4):122–137CrossRefGoogle Scholar
  32. Kubatko LS, Gibbs HL, Bloomquist EW (2011) Inferring species-level phylogenies and taxonomic distinctiveness using multilocus data in Sistrurus rattlesnakes. Syst Biol 60:393–409PubMedCrossRefGoogle Scholar
  33. Langella O (2000) POPULATIONS 1.2.28. Accessed from http://www.cnrs-gif.fr/pge. March 2004
  34. Leavitt SD, Johnson L, Clair LLS (2011) Species delimitation and evolution in morphologically and chemically diverse communities of the lichen-forming genus Xanthoparmelia (Parmeliaceae, Ascomycota) in western North America. Am J Bot 98:175–188PubMedCrossRefGoogle Scholar
  35. Minhas RA, Ahmed KB, Awan MS, Dar NI (2010) Social organization and reproductive biology of Himalayan Grey Langur (Semnopithecus entellus ajax) in Machiara National Park, Azad Kashmir (Pakistan). Pak J Zool 42(2):143–156Google Scholar
  36. Moore WS (1995) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718–726CrossRefGoogle Scholar
  37. Nag KSC, Pramod P, Karanth KP (2011a) Taxonomic implications of a field study of morphotypes of Hanuman langurs (Semnopithecus entellus) in peninsular India. Int J Primatol 32:830–848CrossRefGoogle Scholar
  38. Nag KSC, Pramod P, Karanth KP (2011b) Natural range extension, sampling artifact, or human mediated translocations? Range limits of Northern type Semnopithecus entellus (Dufresne, 1797) (Primates: Cercopithecidae: Colobinae) in peninsular India. J Threat Taxa 3(8):2028–2032CrossRefGoogle Scholar
  39. Nag C, Karanth KP, Gururaja KV (2014) Delineating ecological boundaries of Hanuman langur species complex in peninsular India using MaxEnt modeling approach. PLoS One 9(2):e87804PubMedCrossRefGoogle Scholar
  40. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. J Mol Evol 19:153–170PubMedCrossRefGoogle Scholar
  41. Newton PN (1988) The variable social organization of Hanuman langur (Presbytis entellus), infanticide, and the monopolization of females. Int J Primatol 9:59–77CrossRefGoogle Scholar
  42. Newton PN, Dunbar RIM (1994) Colobine monkey society. In: Davies AG, Oates JF (eds) Colobine monkeys: their ecology, behaviour and evolution. Cambridge University Press, Cambridge, pp 311–346Google Scholar
  43. Oates JF, Davies AG, Delson E (1994) The diversity of living colobines. In: Davies AG, Oates JF (eds) Colobine monkeys: their ecology, behaviour and evolution. Cambridge University Press, Cambridge, pp 45–73Google Scholar
  44. Osterholz M, Walter L, Roos C (2008) Phylogenetic position of the langur genera Semnopithecus and Trachypithecus among Asian colobines, and genus affiliations of their species groups. BMC Evol Biol 8:58PubMedCentralPubMedCrossRefGoogle Scholar
  45. Peng Z, Elango N, Wildman DE, Yi SV (2009) Primate phylogenomics: developing numerous nuclear non-coding, non-repetitive markers for ecological and phylogenetic applications and analysis of evolutionary rate variation. BMC Genomics 10:247PubMedCentralPubMedCrossRefGoogle Scholar
  46. Pettengill JB, Neel MC (2011) A sequential approach using genetic and morphological analyses to test species status: the case of United States federally endangered Agalinis acuta (Orobanchaceae). Am J Bot 98:859–871PubMedCrossRefGoogle Scholar
  47. Pocock RI (1939) The fauna of British India, including Ceylon and Burma—Mammalia, vol 1, primates and carnivora (in part). Taylor and Francis, London, pp 97–163Google Scholar
  48. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14(9):817–818PubMedCrossRefGoogle Scholar
  49. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedCentralPubMedGoogle Scholar
  50. Retief JD, Dixon GH (1993) Evolution of pro-protamine P2 genes in primates. Eur J Biochem 214:609–615Google Scholar
  51. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574PubMedCrossRefGoogle Scholar
  52. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  53. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedCrossRefGoogle Scholar
  54. Sakalidis ML, Hardy GESJ, Burgess TI (2011) Use of the Genealogical Sorting Index (GSI) to delineate species boundaries in the Neofusicoccum parvumNeofusicoccum ribis species complex. Mol Phylogenet Evol 60(3):333–344PubMedCrossRefGoogle Scholar
  55. Sambrook J, Russell D (2001) Preparation of genomic DNA from mouse tails and other small samples. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, pp 6.23–6.27Google Scholar
  56. Sharma G, Ram C, Devilal N, Rajpurohit LS (2011) Study of man-monkey conflict and its management in Jodhpur, Rajasthan (India). J Evol Biol Res 3(1):1–3Google Scholar
  57. Stephens M, Smith N, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989PubMedCentralPubMedCrossRefGoogle Scholar
  58. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.10b. Sinauer Associates, SunderlandGoogle Scholar
  59. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10(3):512–526PubMedGoogle Scholar
  60. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599PubMedCrossRefGoogle Scholar
  61. Tosi AJ, Morales JC, Melnick DJ (2003) Paternal, maternal and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution 57:1419–1435PubMedCrossRefGoogle Scholar
  62. Vallet D, Petit EJ, Gatti S, Levréro S, Ménard N (2008) A new 2CTAB/PCI method improves DNA amplification success from faeces of Mediterranean (Barbary macaques) and tropical (lowland gorillas) primates. Conserv Genet 9:677–680CrossRefGoogle Scholar
  63. Weisrock DW, Rasoloarison RM, Fiorentino I, Ralison JM, Goodman SM, Kappeler PM, Yoder AD (2010) Delimiting species without nuclear monophyly in Madagascar’s mouse lemurs. PLoS One 5:1–13CrossRefGoogle Scholar
  64. Zhang Y-W, Ryder OA, Zhang Y-P (2003) Intra- and interspecific variation of the CCR5 gene in higher primates. Mol Biol Evol 20:1722–1729PubMedCrossRefGoogle Scholar
  65. Zinner D, Arnold ML, Roos C (2011) The strange blood: natural hybridization in primates. Evol Anthropol 20(3):96–103PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2014

Authors and Affiliations

  • N. C. Ashalakshmi
    • 1
  • K. S. Chetan Nag
    • 1
  • K. Praveen Karanth
    • 1
  1. 1.Centre for Ecological SciencesIndian Institute of ScienceBangaloreIndia

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