Comparative and population mitogenomic analyses of Madagascar's extinct, giant 'subfossil' lemurs

Journal of Human Evolution

Volumn 79, Issue , 2015, Pages 45-54

  Kistler, Logan ^a   Ratan, Aakrosh ^a   Godfrey, Laurie R ^b   Crowley, Brooke E ^c   Hughes, Cris E ^d   Lei, Runhua ^e   Cui, Yinqiu ^d   Wood, Mindy L ^e   Muldoon, Kathleen M ^f   Andriamialison, Haingoson ^g   McGraw, John J ^a   Tomsho, Lynn P ^a   Schuster, Stephan C ^a,h   Miller, Webb ^a   Louis, Edward E ^e   Yoder, Anne D ⁱ   Malhi, Ripan S ^d   Perry, George H ^a  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b UNIVERSITY OF MASSACHUSETTS   (United States)

^c UNIVERSITY OF CINCINNATI   (United States)

^d UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

^e Henry Doorly Zoo   (United States)

^f MIDWESTERN UNIVERSITY   (United States)

^g UNIVERSITY OF ANTANANARIVO   (Madagascar)

^h NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

ⁱ DUKE UNIVERSITY   (United States)

Author keywords

Conservation genomics; Extinction genomics; Human environment interactions; Malagasy biodiversity; Paleogenomics

Indexed keywords

BODY SIZE; COMPARATIVE STUDY; DNA; EXTINCTION RISK; GENOMICS; NATURE-SOCIETY RELATIONS; POPULATION GENETICS; POPULATION SIZE; PRIMATE; TAXONOMY;

MADAGASCAR;

LEMUR; LEMURIDAE;

DNA;

ANIMAL; BODY SIZE; CLASSIFICATION; FOSSIL; GENETICS; GENOMICS; LEMURIDAE; MADAGASCAR; PALEONTOLOGY; PHYLOGENY; PHYSIOLOGY; PROCEDURES; SPECIES EXTINCTION;

ANIMALS; BODY SIZE; DNA; EXTINCTION, BIOLOGICAL; FOSSILS; GENOMICS; LEMUR; MADAGASCAR; PALEONTOLOGY; PHYLOGENY;

EID: 84921784454     PISSN: 00472484     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jhevol.2014.06.016     Document Type: Article

References (84)

1. Bazin E., Glemin S., Galtier N. Population size does not influence mitochondrial genetic diversity in animals. Science 2006, 312:570-572.
2. Benton M.J., Donoghue P.C. Paleontological evidence to date the tree of life. Mol. Biol. Evol. 2007, 24:26-53.
3. Briggs A.W., Stenzel U., Johnson P.L., Green R.E., Kelso J., Prufer K., Meyer M., Krause J., Ronan M.T., Lachmann M., Pääbo S. Patterns of damage in genomic DNA sequences from a Neandertal. Proc. Natl. Acad. Sci. 2007, 104:14616-14621.
4. Bronk Ramsey C. Bayesian analysis of radiocarbon dates. Radiocarbon 2009, 51:337-360.
5. Brunet M., Guy F., Pilbeam D., Mackaye H.T., Likius A., Ahounta D., Beauvilain A., Blondel C., Bocherens H., Boisserie J.R., de Bonis L., Coppens Y., Dejax J., Denys C., Duringer P., Eisenmann V., Fanone G., Fronty P., Geraads D., Lehmann T., Lihoreau F., Louchart A., Mahamat A., Merceron G., Mouchelin G., Otero O., Pelaez Campomanes P., Ponce de León M., Rage J.C., Sapanet M., Schuster M., Sudre J., Tassy P., Valentin X., Vignaud P., Viriot L., Zazzo A., Zollikofer C. Anew hominid from the Upper Miocene of Chad, Central Africa. Nature 2002, 418:145-151.
6. Burney D.A. Rates, patterns, and processes of landscape transformation and extinction in Madagascar. Extinctions in Near Time 1999, 145-164. Kluwer/Plenum, New York. R.D.E. MacPhee (Ed.).
7. Burney D.A., Burney L.P., Godfrey L.R., Jungers W.L., Goodman S.M., Wright H.T., Jull A.J. Achronology for late prehistoric Madagascar. J.Hum. Evol. 2004, 47:25-63.
8. Catlett K.K., Schwartz G.T., Godfrey L.R., Jungers W.L. "Life history space": A multivariate analysis of life history variation in extant and extinct Malagasy lemurs. Am. J. Phys. Anthropol. 2010, 142:391-404.
9. Chenna R., Sugawara H., Koike T., Lopez R., Gibson T.J., Higgins D.G., Thompson J.D. Multiple sequence alignment with the Clustal series of programs. Nucl. Acids Res. 2003, 31:3497-3500.
10. Crovella S., Montagnon D., Rakotosamimanana B., Rumpler Y. Molecular biology and systematics of an extinct lemur: Pachylemur insignis. Primates 1994, 35:519-522.
11. Crowley B.E. Arefined chronology of prehistoric Madagascar and the demise of the megafauna. Quatern. Sci. Rev. 2010, 29:2591-2603.
12. Crowley B.E., Godfrey L.R. Why all those spines? Anachronistic defenses in the Didiereoideae against now extinct lemurs. S.Afr. J. Sci. 2013, 109:1-7.
13. Crowley B.E., Godfrey L.R., Irwin M.T. Aglance to the past: subfossils, stable isotopes, seed dispersal, and lemur species loss in Southern Madagascar. Am. J. Primatol. 2011, 73:25-37.
14. Crowley B.E., Godfrey L.R., Guilderson T.P., Zermeno P., Koch P.L., Dominy N.J. Extinction and ecological retreat in a community of primates. Proc. Biol. Sci. 2012, 279:3597-3605.
15. Davies N., Schwitzer C. Lemur conservation status review: An overview of the lemur red-listing results 2012. Lemurs of Madagascar: A strategy for their Conservation 2013-2016 2013, 13-27. IUCN SSC Primate Specialist Group, Bristol Science and Conservation Foundation, and Conservation International, Bristol. C. Schwitzer, R.A. Mittermeier, N. Davies, S. Johnson, J. Ratsimbazafy, J. Razafindramanana, E.E. Louis, S. Rajaobelina (Eds.).
16. Dewar R.E., Richard A.F. Madagascar: A history of arrivals, what happened, and what will happen next. A.Rev. Anthropol. 2012, 41:495-517.
17. Dietl G.P., Flessa K.W. Conservation paleobiology: putting the dead to work. Trends Ecol. Evol. 2011, 26:30-37.
18. Drummond A.J., Ho S.Y., Phillips M.J., Rambaut A. Relaxed phylogenetics and dating with confidence. PLoS Biol. 2006, 4:e88.
19. Drummond A.J., Ho S.Y.W., Rawlence N., Rambaut A. ARough Guide to BEAST 1.4 2007, University of Auckland, Auckland, New Zealand.
20. Drummond A.J., Suchard M.A., Xie D., Rambaut A. Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol. Biol. Evol. 2012, 29:1969-1973.
21. Frankham R. Relationship of genetic variation to population size in wildlife. Conserv. Biol. 1996, 10:1500-1508.
22. Frankham R. Genetics and extinction. Biol. Conserv. 2005, 126:131-140.
23. Frost S. African Pliocene and Pleistocene cercopithecid evolution and global climatic change. Hominin Environments in the East African Pliocene: An assessment of the Faunal Evidence 2007, 51-76. Springer, New York. R. Bobe, Z. Alemseged (Eds.).
24. Gnirke A., Melnikov A., Maguire J., Rogov P., LeProust E.M., Brockman W., Fennell T., Giannoukos G., Fisher S., Russ C., Gabriel S., Jaffe D.B., Lander E.S., Nusbaum C. Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat. Biotechnol. 2009, 27:182-189.
25. Godfrey L.R., Irwin M.T. The evolution of extinction risk: past and present anthropogenic impacts on the primate communities of Madagascar. Folia Primatol. 2007, 78:405-419.
26. Godfrey L.R., Semprebon G.M., Jungers W.L., Sutherland M.R., Simons E.L., Solounias N. Dental use wear in extinct lemurs: evidence of diet and niche differentiation. J.Hum. Evol. 2004, 47:145-169.
27. Godfrey L.R., Crowley B.E., Dumont E.R. Thinking outside the box: a lemur's take on hominin craniodental evolution. Proc. Natl. Acad. Sci. 2011, 108:E742.
28. Godfrey L.R., Schwartz G.T., Jungers W.L., Catlett K.K., Samonds K.E., King S.J., Muldoon K.M., Irwin M.T. Life history variation in Madagascar's giant extinct lemurs. Leaping Ahead: Developments in Primatology: Progress and Prospects 2013, 51-60. Springer, New York. J. Masters, M. Gamba, F. Genin (Eds.).
29. Goodman S.M., Raherilalao M.J., Muldoon K. Bird fossil from Ankilitelo Cave: Inference about Holocene environmental changes in southwestern Madagascar. Zootaxa 2013, 3750:534-548.
30. Guindon S., Dufayard J.F., Lefort V., Anisimova M., Hordijk W., Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 2010, 59:307-321.
31. Haile-Selassie Y. Late Miocene hominids from the Middle Awash, Ethiopia. Nature 2001, 412:178-181.
32. Hallam A., Wignall P.B. Mass Extinctions and their Aftermath 1997, Oxford University Press, Oxford.
33. Harper G.J., Steininger M.K., Tucker C.J., Juhn D., Hawkins F. Fifty years of deforestation and forest fragmentation in Madagascar. Environ. Conserv. 2007, 34:325-333.
34. Ivany L.C., Patterson W.P., Lohmann K.C. Cooler winters as a possible cause of mass extinctions at the Eocene/Oligocene boundary. Nature 2000, 407:887-890.
35. Janis C.M. Ungulate teeth, diets, and climatic changes at the Eocene/Oligocene boundary. Zoology-Analysis of Complex Systems 1997, 100:203-220.
36. Jernvall J., Wright P.C. Diversity components of impending primate extinctions. Proc. Natl. Acad. Sci. 1998, 95:11279-11283.
37. Jungers W.L., Demes B., Godfrey L.R. How big were the "Giant" extinct lemurs of Madagascar. Elwyn Simons: A Search for Origins 2008, 343-360. Springer, New York. J.G. Fleagle, C.C. Gilbert (Eds.).
38. Karanth K.P., Delefosse T., Rakotosamimanana B., Parsons T.J., Yoder A.D. Ancient DNA from giant extinct lemurs confirms single origin of Malagasy primates. Proc. Natl. Acad. Sci. 2005, 102:5090-5095.
39. Katoh K., Misawa K., Kuma K., Miyata T. MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002, 30:3059-3066.
40. Kircher M. Analysis of high-throughput ancient DNA sequencing data. Methods Mol. Biol. 2012, 840:197-228.
41. Leakey M. Evolution of Theropithecus in the Turkana Basin. Theropithecus: The Rise and Fall of a Primate Genus 1993, 85-123. Cambridge University Press, Cambridge. N.G. Jablonski (Ed.).
42. Letts B., Shapiro B. Case study: ancient DNA recovered from Pleistocene-age remains of a Florida armadillo. Methods Mol. Biol. 2012, 840:87-92.
43. Li H., Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 2009, 25:1754-1760.
44. Li H., Handsaker B., Wysoker A., Fennell T., Ruan J., Homer N., Marth G., Abecasis G., Durbin R. The Sequence Alignment/Map format and SAMtools. Bioinformatics 2009, 25:2078-2079.
45. MacPhee R.D.E., Burney D.A. Dating of modified femora of extinct dwarf hippopotamus from southern Madagascar - implications for constraining human colonization and vertebrate extinction events. J.Archaeol. Sci. 1991, 18:695-706.
46. MacPhee R.D.E., Burney D.A., Wells N.A. Early Holocene chronology and environment of Ampasambazimba, a Malagasy subfossil lemur site. Int. J. Primatol. 1985, 6:463-489.
47. McCormac F.G., Hogg A.G., Blackwell P.G., Buck C.E., Higham T.F.G., Reimer P.J. SHCal04 Southern Hemisphere calibration, 0-11.0 cal kyr BP. Radiocarbon 2004, 46:1087-1092.
48. Meyer M., Kircher M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb. Protoc. 2010, 10.1101/pdb.prot5448.
49. Millar C.D., Huynen L., Subramanian S., Mohandesan E., Lambert D.M. New developments in ancient genomics. Trends Ecol. Evol. 2008, 23:386-393.
50. Minin V.N., Bloomquist E.W., Suchard M.A. Smooth skyride through a rough skyline: Bayesian coalescent-based inference of population dynamics. Mol. Biol. Evol. 2008, 25:1459-1471.
51. Mittermeier R.A., Gil P.R., Hoffman M., Pilgrim J., Brooks T., Mittermeier C.G., Lamoreus J., da Fonseca G.A.B. Hotspots Revisited: Earth's Biologically Richest and Most Endangered Terrestrial Ecoregions 2005, The University of Chicago Press, Washington, D.C.
52. Montagnon D., Ravaoarimanana B., Rakotosamimanana B., Rumpler Y. Ancient DNA from Megaladapis edwardsi (Malagasy subfossil): Preliminary results using partial cytochrome b sequence. Folia Primatol. 2001, 72:30-32.
53. Muldoon K.M. Paleoenvironment of Ankilitelo Cave (late Holocene, southwestern Madagascar): implications for the extinction of giant lemurs. J.Hum. Evol. 2010, 58:338-352.
54. Muldoon K.M., de Blieux D.D., Simons E.L., Chatrath P.S. The subfossil occurrence and paleoecological significance of small mammals at Ankilitelo Cave, southwestern Madagascar. J.Mammal. 2009, 90:1111-1131.
55. Mulligan C.J., Kitchen A., Miyamoto M.M. Comment on "Population size does not influence mitochondrial genetic diversity in animals". Science 2006, 314:1390.
56. Orlando L., Calvignac S., Schnebelen C., Douady C.J., Godfrey L.R., Hanni C. DNA from extinct giant lemurs links archaeolemurids to extant indriids. BMC Evol. Biol. 2008, 8:121.
57. Perez V.R., Godfrey L.R., Nowak-Kemp M., Burney D.A., Ratsimbazafy J., Vasey N. Evidence of early butchery of giant lemurs in Madagascar. J.Hum. Evol. 2005, 49:722-742.
58. Perry G.H. The promise and practicality of population genomics research with endangered species. Int. J. Primatol. 2014, 35:55-70.
59. Perry G.H., Louis E.E., Ratan A., Bedoya-Reina O.C., Burhans R.C., Lei R., Johnson S.E., Schuster S.C., Miller W. Aye-aye population genomic analyses highlight an important center of endemism in northern Madagascar. Proc. Natl. Acad. Sci. 2013, 110:5823-5828.
60. Peters R.H. The Ecological Implications of Body Size 1983, Cambridge University Press, Cambridge.
61. R Core Team R: A Language and Environment for Statistical Computing 2013, Austria, Vienna.
62. Rafferty K.L., Teaford M.F., Jungers W.L. Molar microwear of subfossil lemurs: Improving the resolution of dietary inferences. J.Hum. Evol. 2002, 43:645-657.
63. Reed F.A., Kontanis E.J., Kennedy K.A., Aquadro C.F. Ancient DNA prospects from Sri Lankan highland dry caves support an emerging global pattern. Am. J. Phys. Anthropol. 2003, 121:112-116.
64. Rohland N. DNA extraction of ancient animal hard tissue samples via adsorption to silica particles. Methods Mol. Biol. 2012, 840:21-28.
65. Schwartz G.T., Samonds K.E., Godfrey L.R., Jungers W.L., Simons E.L. Dental microstructure and life history in subfossil Malagasy lemurs. Proc. Natl. Acad. Sci. 2002, 99:6124-6129.
66. Schwartz G.T., Mahoney P., Godfrey L.R., Cuozzo F.P., Jungers W.L., Randria G.F. Dental development in Megaladapis edwardsi (Primates, Lemuriformes): implications for understanding life history variation in subfossil lemurs. J.Hum. Evol. 2005, 49:702-721.
67. Scott J.R., Godfrey L.R., Jungers W.L., Scott R.S., Simons E.L., Teaford M.F., Ungar P.S., Walker A. Dental microwear texture analysis of two families of subfossil lemurs from Madagascar. J.Hum. Evol. 2009, 56:405-416.
68. Seiffert E.R. Evolution and extinction of Afro-Arabian primates near the Eocene-Oligocene boundary. Folia Primatol. 2007, 78:314-327.
69. Seiffert E.R., Simons E.L., Attia Y. Fossil evidence for an ancient divergence of lorises and galagos. Nature 2003, 422:421-424.
70. Seligsohn D., Szalay F.S. Dental occlusion and the masticatory apparatus in Lemur and Varecia: Their bearing on the systematics of living and fossil primates. Prosimian Biology 1974, 543-561. Duckworth, London. R.D. Martin, G.A. Doyle, A.C. Walker (Eds.).
71. Shapiro L.J., Seiffert C.V.M., Godfrey L.R., Jungers W.L., Simons E.L., Randria G.F.N. Morphometric analysis of lumbar vertebrae in extinct Malagasy strepsirrhines. Am. J. Phys. Anthropol. 2005, 128:823-839.
72. Simons E.L. Lemurs: Old and new. Natural Change and Human Impacts in Madagascar 1997, 142-168. Smithsonian Press, Washington. S.M. Goodman, B.D. Patterson (Eds.).
73. Simons E.L., Burney D.A., Chatrath P.S., Godfrey L.R., Jungers W.L., Rakotosamimanana B. AMS C-14 dates for extinct lemurs from caves in the Ankarana Massif, northern Madagascar. Quatern. Res. 1995, 43:249-254.
74. Smith R.J., Jungers W.L. Body mass in comparative primatology. J.Hum. Evol. 1997, 32:523-559.
75. Stehlin H.G. Remarques sur les flancs de Mammiferes des couches éocénes et oligocines du Bassin de Pans. Bull. Soc. Geol. Fr. 1909, 4:488-520.
76. Stoneking M., Krause J. Learning about human population history from ancient and modern genomes. Nat. Rev. Genet. 2011, 12:603-614.
77. Tattersall I., Schwartz J.H. Craniodental morphology and the systematics of the Malagasy lemurs (Primates, Prosimii). Anthropol. Pap. Am. Mus. Nat. Hist. NY 1974, 52:139-192.
78. Thalmann U. Food resource characteristics in two nocturnal lemurs with different social behavior: Avahi occidentalis and Lepilemur edwardsi. Int. J. Primatol. 2001, 22:287-324.
79. Wade B.S., Houben A.J.P., Quaijtaal W., Schouten S., Rosenthal Y., Miller K.G., Katz M.E., Wright J.D., Brinkhuis H. Multiproxy record of abrupt sea-surface cooling across the Eocene-Oligocene transition in the Gulf of Mexico. Geology 2012, 40:159-162.
80. Wall C.E. The expanded mandibular condyle of the Megaladapidae. Am. J. Phys. Anthropol. 1997, 103:263-276.
81. Yoder A.D. Ancient DNA from Megaladapis edwardsi. Folia Primatol. 2001, 72:342-343.
82. Yoder A.D., Rakotosamimanana B., Parsons T.J. Ancient DNA in subfossil lemurs: methodological challenges and their solutions. New Directions in Lemur Studies 1999, 1-17. Plenum Press, New York. H. Rasaminanana, B. Rakotosamimanana, S. Goodman, J. Ganzhorn (Eds.).
83. Zachos J.C., Kump L.R. Carbon cycle feedbacks and the initiation of Antarctic glaciation in the earliest Oligocene. Global Planet. Change 2005, 47:51-66.
84. Zanazzi A., Kohn M.J., MacFadden B.J., Terry D.O. Large temperature drop across the Eocene-Oligocene transition in central North America. Nature 2007, 445:639-642.