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

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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.

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References

  1. Arnold ML, Meyer A (2006) Natural hybridization in primates: one evolutionary mechanism. Zoology 109(4):261–276

    PubMed  Article  Google Scholar 

  2. Campana M, Hunt H, Jones H, White J (2011) CorrSieve: software for summarizing and evaluating structure output. Mol Ecol Resour 11:349–352

    CAS  PubMed  Article  Google Scholar 

  3. Cavalli-Sforza LL, Edwards AW (1967) Phylogenetic analysis. Models and estimation procedures. Am J Hum Genet 19:233–257

    CAS  PubMed Central  PubMed  Google Scholar 

  4. Chellam R (1985) Langurs of Mundanthurai. Blackbuck 1:20–26

    Google Scholar 

  5. Choudhury AU (2007) The eastern limit of distribution of the Hanuman Langur Semnopithecus entellus Dufresene. J Bombay Nat Hist Soc 104:199–200

    Google Scholar 

  6. Cummings MP, Neel MC, Shaw KL (2008) A genealogical approach to quantifying lineage divergence. Evolution 62:2411–2422

    PubMed  Article  Google 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 285–310

  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 57–75

    Google Scholar 

  9. de Queiroz K (2007) Species concepts and species delimitation. Syst Biol 56(6):879–886

    PubMed  Article  Google 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 14:2611–2620

    CAS  PubMed  Article  Google Scholar 

  11. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    CAS  PubMed Central  PubMed  Google Scholar 

  12. Fu YX, Li WH (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709

    CAS  PubMed Central  PubMed  Google 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 34:397–423

    Article  Google Scholar 

  14. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences. Stat Sci 7(4):457–472

    Article  Google Scholar 

  15. Greenwood PJ (1980) Mating systems, philopatry, and dispersal in birds and mammals. Anim Behav 28:1140–1162

    Article  Google 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 9:30

    PubMed Central  PubMed  Article  Google Scholar 

  17. Groves CP (2001) Primate taxonomy. Smithsonian Institution Press, Washington

    Google Scholar 

  18. Groves CP (2012) Species concept in primates American. J Primatol 74(8):687–691

    Article  Google Scholar 

  19. Hill WCO (1939) An annotated systematic list of the leaf-monkeys. Ceylon J Sci 21:277–305

    Google Scholar 

  20. Hoelzer GA (1997) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees revisited. Evolution 51:622–626

    Article  Google 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 47:21–31

    CAS  PubMed  Article  Google 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 51:209–213

    CAS  PubMed  Article  Google Scholar 

  23. Hohmann G (1991) New evidence for hybridization in Presbytis johnii and Presbytis entellus. J Bombay Nat Hist Soc 88:315–319

    Google 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 111:147–164

    CAS  PubMed Central  PubMed  Google 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):120–127

    CAS  PubMed  Google 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 55:623–636

    PubMed  Article  Google Scholar 

  27. Karanth KP (2008) Primate numts and reticulate evolutions of capped and golden leaf monkeys (Primates: Colobinae). J Biosci 33:761–770

    CAS  PubMed  Article  Google Scholar 

  28. Karanth KP (2010) Molecular systematics and conservation of the langurs and leaf monkeys of South Asia. J Genet 89(4):393–399

    PubMed  Article  Google 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 46:683–694

    CAS  PubMed  Article  Google 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 54:627–633

    CAS  PubMed  Article  Google Scholar 

  31. Koenig A, Borries C (2001) Socioecology of Hanuman langurs: the story of their success. Evol Anthropol 10(4):122–137

    Article  Google Scholar 

  32. Kubatko LS, Gibbs HL, Bloomquist EW (2011) Inferring species-level phylogenies and taxonomic distinctiveness using multilocus data in Sistrurus rattlesnakes. Syst Biol 60:393–409

    PubMed  Article  Google 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 98:175–188

    PubMed  Article  Google 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):143–156

    Google Scholar 

  36. Moore WS (1995) Inferring phylogenies from mtDNA variation: mitochondrial-gene trees versus nuclear-gene trees. Evolution 49:718–726

    Article  Google 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 32:830–848

    Article  Google 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):2028–2032

    Article  Google 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):e87804

    PubMed  Article  Google Scholar 

  40. Nei M, Tajima F, Tateno Y (1983) Accuracy of estimated phylogenetic trees from molecular data. II. Gene frequency data. J Mol Evol 19:153–170

    CAS  PubMed  Article  Google Scholar 

  41. Newton PN (1988) The variable social organization of Hanuman langur (Presbytis entellus), infanticide, and the monopolization of females. Int J Primatol 9:59–77

    Article  Google 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 311–346

    Google 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 45–73

    Google 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 8:58

    PubMed Central  PubMed  Article  Google 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 10:247

    PubMed Central  PubMed  Article  Google 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 98:859–871

    PubMed  Article  Google 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 97–163

    Google Scholar 

  48. Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14(9):817–818

    CAS  PubMed  Article  Google Scholar 

  49. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Retief JD, Dixon GH (1993) Evolution of pro-protamine P2 genes in primates. Eur J Biochem 214:609–615

  51. Ronquist F, Huelsenbeck JP (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572–1574

    CAS  PubMed  Article  Google Scholar 

  52. Rosenberg NA (2004) Distruct: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138

    Article  Google Scholar 

  53. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497

    CAS  PubMed  Article  Google 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):333–344

    PubMed  Article  Google 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 6.23–6.27

    Google 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):1–3

    Google Scholar 

  57. Stephens M, Smith N, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989

    CAS  PubMed Central  PubMed  Article  Google Scholar 

  58. Swofford DL (2002) PAUP*: phylogenetic analysis using parsimony (*and other methods), version 4.10b. Sinauer Associates, Sunderland

    Google 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):512–526

    CAS  PubMed  Google Scholar 

  60. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    CAS  PubMed  Article  Google 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 57:1419–1435

    CAS  PubMed  Article  Google 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 9:677–680

    CAS  Article  Google 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 5:1–13

    Article  Google 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 20:1722–1729

    CAS  PubMed  Article  Google Scholar 

  65. Zinner D, Arnold ML, Roos C (2011) The strange blood: natural hybridization in primates. Evol Anthropol 20(3):96–103

    PubMed  Article  Google Scholar 

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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.

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Correspondence to K. Praveen Karanth.

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Ashalakshmi, N.C., Nag, K.S.C. & Karanth, K.P. Molecules support morphology: species status of South Indian populations of the widely distributed Hanuman langur. Conserv Genet 16, 43–58 (2015). https://doi.org/10.1007/s10592-014-0638-4

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Keywords

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