Skip to main content

Advertisement

SpringerLink
Log in

Genetic Analysis of the Indri Reveals No Evidence of Distinct Subspecies

  • Published:
International Journal of Primatology Aims and scope Submit manuscript

Abstract

Subspecies were traditionally defined by identifying gaps between phenotypes across the geographic range of a species, and may represent important units in the development of conservation strategies focused on preserving genetic diversity. Previous taxonomic research proposed that phenotypic variation between scattered Indri indri populations warranted the naming of two distinct subspecies, I. i. indri and I. i. variegatus. We tested these subspecific designations using mitochondrial sequence data generated from the control region or D-loop (569 bp) and a large section (2362 bp) of multiple genes and tRNAs known as Pastorini’s fragment and nuclear microsatellite markers. This study used 114 samples of I. indri from 12 rainforest sites in eastern Madagascar, encompassing the entire range of the species. These genetic samples represent multiple populations from low- and high-elevation forests from both putative subspecies. Molecular analyses of the mitochondrial sequence data did not support the two proposed subspecies. Furthermore, the microsatellite analyses showed no significant differences across the range beyond population level differentiation. This study demonstrates the utility of incorporating multiple lines of evidence in addition to phenotypic traits to define species or subspecies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Allnutt, T. F., Ferrier, S., Manion, G., Powell, G. V. N., Ricketts, T. H., et al. (2008). A method for quantifying biodiversity loss and its application to a 50-year record of deforestation across Madagascar. Conservation Letters, 1, 173–181.

    Article  Google Scholar 

  • Allnutt, T. F., Powell, G. V. N., Ferrier, S., Ricketts, T. H., Steininger, M. K., & Manion, G. (2004). Quantifying biodiversity loss in Madagascar using biological inventories, environmental data and a 50 year record of deforestation. In Society for Conservation Biology Meetings, July 30–August 22, 2004, New York.

  • Andriantompohavana, R., Lei, R., Zaonarivelo, J. R., Engberg, S. E., Nalanirina, G., et al. (2007). Molecular phylogeny and taxonomic revision of the woolly lemurs, genus Avahi (Primates: Lemuriforms). Special Publications of the Museum, Texas Tech University, 51, 1–59.

    Google Scholar 

  • Andriantompohavana, R., Zaonarivelo, J. R., Engberg, S. E., Randriamampionona, R., McGuire, S. M., et al. (2006). Mouse lemurs of northwestern Madagascar with a description of a new species at Lokobe Special Reserve. Occasional Publications of the Museum, Texas Tech University, 259, 1–23.

    Google Scholar 

  • Baker, C. S., Perry, A., Bannister, J., Weinrich, M. T., Abernathy, R. B., et al. (1993). Abundant mitochondrial variation and world-wide population structure in hump-backed whales. Proceeding of the National Academy of Sciences of the USA, 90, 8239–8243.

    Article  CAS  Google Scholar 

  • Bandelt, H.-J., Forster, P., & Rohl, A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biological and Evolution, 16, 37–48.

    Article  CAS  Google Scholar 

  • Barton, N. H., & Hewitt, G. M. (1985). Analysis of hybrid zones. Annual Review of Ecology, Evolution, and Systematics, 16, 113–148.

    Article  Google Scholar 

  • Callen, D. F., Thompson, A. D., Shen, Y., Phillips, H. A., Richards, R. I., et al. (1993). Incidence and origin of “null” alleles in the (AC)n microsatellite markers. American Journal of Human Genetics, 52, 922–927.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chapuis, M. P., & Estoup, A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biological and Evolution, 24(3), 621–631.

    Article  CAS  Google Scholar 

  • Del Pero, M., Crovella, S., Cervella, P., Ardito, G., & Rumpler, Y. (1995). Phylogenetic relationships among Malagasy lemurs as revealed by mitochondrial DNA sequence analysis. Primates, 36(3), 431–440.

    Article  Google Scholar 

  • Dieringer, D., & Schlötterer, C. (2002). Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Molecular Ecology Notes, 1(3), 167–169.

    Google Scholar 

  • Evanno, G., Regnaut, S., & Goudet, J. (2005). Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Molecular Ecology, 14, 2611–2620.

    Article  CAS  PubMed  Google Scholar 

  • Excoffier, L., Laval, G., & Schneider, S. (2005). Arlequin version 3.0: an integrated software package for population genetics data analysis. Evolution Bioinformatics Online, 1, 47–50.

    CAS  Google Scholar 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Glessner, K. D. G., & Britt, A. (2005). Population density and home range size of Indri indri in a protected low altitude rain forest. International Journal of Primatology, 26(4), 855–872.

    Article  Google Scholar 

  • Gmelin, J. F. (1788). Caroli a Linné systema naturae per regna tria naturae, secundum classes, ordines, genera, species, cum characteribus, differentiis, synonymis, locis. Tomus I. Editio decima tertia, aucta, reformata, 42 pp. Lipsiae, G. E. Beer.

  • Golden, C. (2005). Eaten to endangerment: Mammal hunting and the bushmeat trade in Madagascar’s Makira forest. M.S. thesis, Harvard University.

  • Goodman, S. M., & Jungers, W. L. (2014). Extinct Madagascar: Picturing the Island's Past. Chicago: University of Chicago Press.

    Google Scholar 

  • Goudet, J. (1995). FSTAT, a computer program to test F-statistics. Journal of Heredity, 86, 485–486.

    Google Scholar 

  • Goudet, J. (1999). PCA-GEN for windows. Switzerland: Institute of Ecology, University of Lausanne.

    Google Scholar 

  • Goudet, J. (2001). FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). Updated from Goudet, J. (1995).

  • Green, C., & Sussman, R. W. (1990). Deforestation history of the eastern rain forests of Madagascar from satellite images. Science, 248, 212–215.

    Article  CAS  PubMed  Google Scholar 

  • Groves, C. P. (2001). Primate taxonomy (pp. 86–88). Washington, DC: Smithsonian Institution Press.

    Google Scholar 

  • Guindon, S., Dufayard, J. F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010). New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Systematic Biology, 59, 307–321.

    Article  CAS  PubMed  Google Scholar 

  • Harper, G. J., Steininger, M. K., Tucker, C. J., Juhn, D., & Hawkins, F. (2007). Fifty years of deforestation and forest fragmentation in Madagascar. Environmental Conservation, 34(4), 1–9.

    Article  Google Scholar 

  • Hoffman, J. I., & Amos, W. (2005). Microsatellite genotyping errors: detection approaches, common sources and consequences for parental exclusion. Molecular Ecology, 14, 599–612.

    Article  CAS  PubMed  Google Scholar 

  • Huelsenbeck, J. P., & Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogeny. Bioinformatics, 17, 754–755.

    Article  CAS  PubMed  Google Scholar 

  • IUCN. (2015). IUCN Red list of threatened species. www.iucnredlist.org (Accessed November 12, 2015).

  • Jenkins, M. D. (Ed.). (1990). Madagascar: An environmental profile. Gland: IUCN.

    Google Scholar 

  • Jensen, J. L., Bohonak, A. J., & Kelley, S. T. (2005). Isolation by distance, web service. BMC Genetics, 6, 13. v. 3.23 http://ibdws.sdsu.edu/.

  • Junge, R. E., & Louis, E. E., Jr. (2002). Medical evaluation of free-ranging primates in Betampona Reserve, Madagascar. Lemur News, 7, 23–25.

    Google Scholar 

  • Jungers, W. L., Godfrey, L. R., Simons, E. L., & Chatrath, P. S. (1995). Subfossil Indri indri from the Ankarana Massif of northern Madagascar. American Journal of Physical Anthropology, 97(4), 357–366.

    Article  CAS  PubMed  Google Scholar 

  • Louis, E. E., Jr., Coles, M. S., Andriantompohavana, R., Sommer, J. A., Engberg, S., et al. (2006a). Revision of the mouse lemurs (Microcebus) of eastern Madagascar. International Journal of Primatology, 27, 347–389.

    Article  Google Scholar 

  • Louis, E. E., Jr., Engberg, S. E., Lei, R., Geng, H., Sommer, J. A., et al. (2006b). Molecular and morphological analyses of the sportive lemurs (family Megaladapidae: genus Lepilemur) reveals 11 previously unrecognized species. Special Publications of the Museum, Texas Tech University, 49, 1–47.

    Google Scholar 

  • Marshall, T. C., Slate, J., Kruuk, L. E. B., & Pemberton, J. M. (1998). Statistical confidence for likelihood-based paternity inference in natural populations. Molecular Ecology, 7(5), 639–655.

    Article  CAS  PubMed  Google Scholar 

  • Mayor, M. I., Sommer, J. A., Houck, M. L., Zaonarivelo, J., Wright, P. C., Ingram, C., et al. (2004). Specific status of Propithecus spp. International Journal of Primatology, 25(4), 875–900.

    Article  Google Scholar 

  • Mittermeier, R. A., Louis, E. E., Jr., Richardson, M., Schwitzer, C., Lagrand, O., et al. (2010). Lemurs of Madagascar (3rd ed., pp. 578–595). Washington, DC: Conservation International.

    Google Scholar 

  • Nei, M. (1987). Molecular evolutionary genetics. New York: Columbia University Press.

    Google Scholar 

  • Nei, M., & Li, W. H. (1979). Mathematical model for studying genetic variation in terms of restriction endonucleases. Proceeding of the National Academy of Sciences of the USA, 76, 5269–5273.

    Article  CAS  Google Scholar 

  • Nicoll, M. E., & Lagrand, O. (1993). AVHRR-LAC estimates of forested area in Madagascar, 1990. International Journal of Remote Sensing, 14, 1463–1475.

    Article  Google Scholar 

  • Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by author. Uppsala: Evolutionary Biology Centre.

    Google Scholar 

  • Padial, J. M., Miralles, A., De la Riva, I., & Vences, M. (2010). The integrative future of taxonomy. Frontiers in Zoology, 7, 16.

    Article  PubMed  PubMed Central  Google Scholar 

  • Pastorini, J., Forstner, M. R. J., & Martin, R. D. (2000). Relationships among brown lemurs (Eulemur fulvus) based on mitochondrial DNA sequences. Molecular Phylogenetics and Evolution, 16, 418–429.

    Article  CAS  PubMed  Google Scholar 

  • Pastorini, J., Martin, R. D., Ehresmann, P., Zimmermann, E., & Forstner, M. R. J. (2001). Molecular phylogeny of the lemur family Cheirogaleidae (primates) based on mitochondrial DNA evidence. Molecular Phylogenetics and Evolution, 19, 45–56.

    Article  CAS  PubMed  Google Scholar 

  • Posada, D., & Crandall, K. A. (1998). Modeltest: testing the model of DNA substitution. Bioinformatics, 14, 817–818.

    Article  CAS  PubMed  Google Scholar 

  • Powzyk, J., & Thalmann, U. (2003). Indri indri, Indri. In S. M. Goodman & J. P. Benstead (Eds.), The natural history of Madagascar (pp. 1342–1345). Chicago and London: University of Chicago Press.

    Google Scholar 

  • Prada, C., DeBiasse, M. B., Neigel, J. E., Yednock, B., Stake, J. L., et al. (2014). Genetic species delineation among branching Caribbean Porites corals. Coral Reefs, 33, 1019–1030.

    Article  Google Scholar 

  • Pritchard, J. K., Stephens, M., & Donnelly, P. (2000). Inference of population structure using multilocus genotype data. Genetics, 155, 945–959.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Rambaut, A., & Drummond, A. J. (2009) Tracer v1.5. Available from http://beast.bio.ed.ac.uk/Tracer.

  • Razafindraibe, H., Montagnon, D., Ravoarimanana, B. I., & Rumpler, Y. (2000). Interspecific nucleotide sequence differences in the cytochrome b gene of Indriidae (Primates, Strepsirini). Primates, 41(2), 189–197.

    Article  Google Scholar 

  • Reed, D. H., & Frankham, R. (2003). Correlation between fitness and genetic diversity. Conservation Biology, 17(1), 230–237.

    Article  Google Scholar 

  • Ronquist, F., & Huelsenbeck, J. P. (2003). MRBAYES 3: Bayesian phylogenetic inferences under mixed models. Bioinformatics, 19, 1572–1574.

    Article  CAS  PubMed  Google Scholar 

  • Rousset, F. (1997). Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics, 145, 1219–1228.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Roy, J., Gary, M., Stoinski, T., Robbins, M., & Vigilant, L. (2014). Fine-scale genetic structure analyses suggest further male than female dispersal in mountain gorillas. BMC Ecology, 14, 21.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rumpler, Y., Warter, S., Ishak, B., & Dutrillaux, B. (1988). Chromosome evolution in Malagasy lemurs: X. chromosome banding studies of Propithecus diadema edwardsi and Indri indri and phylogenetic relationships between all the species of Indriidae. American Journal of Primatology, 16, 63–71.

    Article  Google Scholar 

  • Sambrook, J., Fritch, E. F., & Maniatus, T. (1989). Molecular cloning: A laboratory manual (2nd ed.). New York: Cold Spring Harbor Press.

    Google Scholar 

  • Sikes, R. S., Gannon, W. L., & the Animal Care and Use Committee of the American Society of Mammalogists. (2011). Guidelines of the American Society of Mammalogists for the use of wild mammals in research. Journal of Mammalogy, 92(1), 235–253.

    Article  Google Scholar 

  • Slate, J., Marshall, T. C., & Pemberton, J. M. (2000). A retrospective assessment of the accuracy of the paternity inference program CERVUS. Molecular Ecology, 9(6), 801–808.

    Article  CAS  PubMed  Google Scholar 

  • Swofford, D. L. (2001). PAUP*. Phylogenetic analysis using parsimony (* and other methods) version 4.0b5. Sunderland: Sinauer Associates.

    Google Scholar 

  • Tamura, K., Dudley, J., Nei, M., & Kumar, S. (2007). MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24, 1596–1599.

    Article  CAS  PubMed  Google Scholar 

  • Telenius, H., Carter, N. P., Bebb, C. E., Nordenskjöb, M., Ponder, A. J., & Tunnacliffe, A. (1992). Degenerate oligonucleotide-primed PCR: general amplification of target DNA by a single degenerate primer. Genomics, 13, 718–725.

    Article  CAS  PubMed  Google Scholar 

  • Thalmann, U., Geissmann, T., Simona, A., & Mutschler, T. (1993). The indris of Anjanaharibe-Sud, northeastern Madagascar. International Journal of Primatology, 14(3), 357–381.

    Article  Google Scholar 

  • Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F., & Higgins, D. G. (1997). The ClustalX-Windows interface: flexible strategies for multiple sequence alignments aided by using quality analysis tools. Nucleic Acids Research, 25, 4876–4882.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van Oosterhout, C., Hutchinson, W. F., Wills, D. P. M., & Shipley, P. (2004). Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes, 4, 535–538.

    Article  Google Scholar 

  • Wyner, Y. M., Amato, G., & DeSalle, R. (1999). Captive breeding, reintroduction, and the conservation genetics of black and white ruffed lemurs, Varecia variegata variegata. Molecular Ecology, 8(S), 107–115.

    Article  Google Scholar 

  • Zaonarivelo, J. R., Andriantompohavana, R., Engberg, S. E., Kelley, S. G., Randriamanana, J. C., et al. (2007a). Morphometric data for indri (Indri indri) collected from 10 forest fragments in eastern Madagascar. Lemur News, 12, 17–21.

    Google Scholar 

  • Zaonarivelo, J., Brenneman, R., Andriantompohavana, R., & Louis, E. E., Jr. (2010). Genetic diversity in ten indri (Indri indri) populations and compared to other lemur species. Lemur News, 15, 59–64.

    Google Scholar 

  • Zaonarivelo, J. R., Sommer, J. A., McGuire, S. M., Engberg, S. E., Brenneman, R. A., & Louis, E. E., Jr. (2007b). Isolation and characterization of twenty microsatellite marker loci from the indri (Indri indri) genome. Molecular Ecology Notes, 7, 25–28.

    Article  CAS  Google Scholar 

  • Zhang, D. X., & Hewitt, G. M. (1996). Nuclear integrations: challenges for mitochondrial DNA markers. Trends in Ecology and Evolution, 11, 247–251.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We acknowledge the Ministry of Environment and Eaux & Forêts (CAFF/CORE), Madagascar National Parks (MNP), Association FANAMBY, and the Department of Biological Anthropology, University of Antananarivo for their help. This project would not have been possible without the support of the staff of MICET and Omaha’s Henry Doorly Zoo & Aquarium (OHDZA) and the Madagascar Biodiversity Partnership (MBP), as well as Parc Botanique et Zoologique de Tsimbazaza, U.S. Fish & Wildlife Service, Bill and Berniece Grewcock, the Ahmanson Foundation, the Theodore F. and Claire M. Hubbard Family Foundation, and the James Family Foundation. We would also like to acknowledge John Callahan, Michael Bosetti, Nikola Miljkovic, Cynthia Frasier, Melissa Hawkins, The Peter Kiewitt Institute, Holland Computing Center, University of Nebraska Foundation, and the University of Nebraska at Omaha for their enthusiastic support for seeing this project through to completion. In addition, we would like to thank the editor and reviewers from the International Journal of Primatology for their thoughtful comments and suggestions on this manuscript.

Author information

Authors and Affiliations

  1. Giraffe Conservation Foundation, Purley Surrey CR8 1DU, U.K. and Omaha, Nebraska, 68106, USA

    Rick A. Brenneman

  2. Department of Mathematics and Sciences, State University of New York Polytechnic Institute, Utica, NY, 13502, USA

    Adam T. McLain

  3. Grewcock Center for Conservation and Research, Omaha’s Henry Doorly Zoo and Aquarium, Omaha, Nebraska, 68107, USA

    Justin M. Taylor, John R. Zaonarivelo, Runhua Lei, Rambinintsoa Andriantompohavana & Edward E. Louis Jr.

  4. Earth and Life Sciences Department, University of Antsiranana, Antsiranana, Madagascar

    John R. Zaonarivelo, Rambinintsoa Andriantompohavana & Edward E. Louis Jr.

  5. Conservation Fusion, Omaha, Nebraska, 68106, USA

    Susie M. McGuire

  6. Conservation International, Arlington, Virginia, 22202, USA

    Anthony B. Rylands

Authors
  1. Rick A. Brenneman
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adam T. McLain
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Justin M. Taylor
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. John R. Zaonarivelo
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Runhua Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Susie M. McGuire
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rambinintsoa Andriantompohavana
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Anthony B. Rylands
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Edward E. Louis Jr.
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Edward E. Louis Jr..

Electronic supplementary material

Below is the link to the electronic supplementary material.

ESM 1

(DOC 1327 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brenneman, R.A., McLain, A.T., Taylor, J.M. et al. Genetic Analysis of the Indri Reveals No Evidence of Distinct Subspecies. Int J Primatol 37, 460–477 (2016). https://doi.org/10.1007/s10764-016-9911-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10764-016-9911-3

Keywords

Search

Navigation