Aye-aye population genomic analyses highlight an important center of endemism in northern Madagascar

Proceedings of the National Academy of Sciences of the United States of America

Volumn 110, Issue 15, 2013, Pages 5823-5828

  Perry, George H ^a   Louis, Edward E ^a   Ratan, Aakrosh ^b   Bedoya Reina, Oscar C ^b   Burhans, Richard C ^b   Lei, Runhua ^a   Johnson, Steig E ^c   Schuster, Stephan C ^b,d   Miller, Webb ^b  

^a PENNSYLVANIA STATE UNIVERSITY   (United States)

^b Henry Doorly Zoo   (United States)

^c UNIVERSITY OF CALGARY   (Canada)

^d NANYANG TECHNOLOGICAL UNIVERSITY   (Singapore)

Author keywords

Conservation genomics; Genomics of non model species; Landscape species concept

Indexed keywords

ARTICLE; AYE AYE; BIOGEOGRAPHY; GENE FLOW; GENE SEQUENCE; GENETIC VARIABILITY; LEMURIDAE; MADAGASCAR; NONHUMAN; POPULATION DENSITY; POPULATION GENETICS; PRIORITY JOURNAL; SINGLE NUCLEOTIDE POLYMORPHISM; SPECIES DIFFERENTIATION; SPECIES ENDEMICITY; SPECIES EXTINCTION;

EID: 84876061150     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1211990110     Document Type: Article

References (72)

1. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GA, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403(6772):853-858.
2. Vieites DR, et al. (2009) Vast underestimation of Madagascar' s biodiversity evidenced by an integrative amphibian inventory. Proc Natl Acad Sci USA 106(20):8267-8272.
3. Allnutt TF, et al. (2008) A method for quantifying biodiversity loss and its application to a 50-year record of deforestation across Madagascar. Conserv Lett 1(4):173-181.
4. Godfrey LR, Irwin MT (2007) The evolution of extinction risk: Past and present anthropogenic impacts on the primate communities of Madagascar. Folia Primatol (Basel) 78(5-6):405-419.
5. Mittermeier RA, et al. (2008) Lemur diversity in Madagascar. Int J Primatol 29(6):1607-1656.
6. Sterling EJ (1994) Taxonomy and distribution of Daubentonia: A historical perspective. Folia Primatol (Basel) 62(1-3):8-13.
7. Sterling EJ (1993) The behavioral ecology of the aye-aye on Nosy Mangabe, Madagascar. PhD dissertation (Yale University, New Haven, CT).
8. Ganzhorn JU, Abraham JP, Razanahoera-Rakotomalala M (1985) Some aspects of the natural history and food selection of Avahi laniger. Primates 26(4):452-463.
9. Schulke O (2005) Evolution of pair-living in Phaner furcifer. Int J Primatol 26(4):903-919.
10. Volampeno M S N, Masters JC, Downs CT (2011) Home range size in the blue-eyed black lemur (Eulemur flavifrons): Between dry and wet seasons. Mamm Biol 76(2):157-164.
11. Benadi G, Fichtel C, Kappeler P (2008) Intergroup relations and home range use in Verreaux' s sifaka (Propithecus verreauxi). Am J Primatol 70(10):956-965.
12. Mittermeier RA, et al. (2010) Lemurs of Madagascar (Conservation International, Arlington, VA), 3rd Ed.
13. Catlett KK, Schwartz GT, Godfrey LR, Jungers WL (2010) "Life history space": A multivariate analysis of life history variation in extant and extinct Malagasy lemurs. Am J Phys Anthropol 142(3):391-404.
14. Perry GH, et al. (2012) Comparative RNA sequencing reveals substantial genetic variation in endangered primates. Genome Res 22(4):602-610.
15. Sterling EJ (1994) Aye-ayes: Specialists on structurally defended resources. Folia Pri-matol (Basel) 62(1-3):142-154.
16. Erickson CJ (1994) Tap-scanning and extractive foraging in aye-ayes, Daubentonia madagascariensis. Folia Primatol (Basel) 62(1-3):125-135.
17. Goodman SM, Sterling EJ (1996) The utilization of Canarium (Burseraceae) seeds by vertebrates in the Reserve Naturelle Integrale d' Andringitra, Madagascar. Fieldiana Zoology 85:83-92.
18. Milliken GW, Ward JP, Erickson CJ (1991) Independent digit control in foraging by the aye-aye (Daubentonia madagascariensis). Folia Primatol (Basel) 56(4):219-224.
19. Lhota S, Junek T, Bartos L, Kubena AA (2008) Specialized use of two fingers in free-ranging aye-ayes (Daubentonia madagascariensis). Am J Primatol 70(8):786-795.
20. Franklin J (2010) Moving beyond static species distribution models in support of conservation biogeography. Divers Distrib 16(3):321-330.
21. Carroll C (2007) Interacting effects of climate change, landscape conversion, and harvest on carnivore populations at the range margin: Marten and lynx in the northern Appalachians. Conserv Biol 21(4):1092-1104.
22. Gregory SD, et al. (2012) Long-term field data and climate-habitat models show that orangutan persistence depends on effective forest management and greenhouse gas mitigation. PLoS ONE 7(9):e43846.
23. Gardner CJ (2011) IUCN management categories fail to represent new, multiple-use protected areas in Madagascar. Oryx 45(3):336-346.
24. Ouborg NJ, Pertoldi C, Loeschcke V, Bijlsma RK, Hedrick PW (2010) Conservation genetics in transition to conservation genomics. Trends Genet 26(4):177-187.
25. Allendorf FW, Hohenlohe PA, Luikart G (2010) Genomics and the future of conservation genetics. Nat Rev Genet 11(10):697-709.
26. Frankham R (2010) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143(9):1919-1927.
27. Ekblom R, Galindo J (2011) Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity (Edinb) 107(1):1-15.
28. The 1000 Genomes Project Consortium; Abecasis GR, et al. (2010) A map of human genome variation from population-scale sequencing. Nature 467(7319):1061-1073;
29. Erratum in: Nature (2011) 473(7348):544.
30. Schuster SC, et al. (2010) Complete Khoisan and Bantu genomes from southern Africa. Nature 463(7283):943-947.
31. Jones FC, et al.; Broad Institute Genome Sequencing Platform and Whole Genome Assembly Team (2012) The genomic basis of adaptive evolution in threespine sticklebacks. Nature 484(7392):55-61.
32. Everett MV, Grau ED, Seeb JE (2011) Short reads and nonmodel species: Exploring the complexities of next-generation sequence assembly and SNP discovery in the absence of a reference genome. Mol Ecol Resour 11(Suppl 1):93-108.
33. Geraldes A, et al. (2011) SNP discovery in black cottonwood (Populus trichocarpa) by population transcriptome resequencing. Mol Ecol Resour 11(Suppl 1):81-92.
34. Miller MR, et al. (2012) A conserved haplotype controls parallel adaptation in geographically distant salmonid populations. Mol Ecol 21(2):237-249.
35. Miller W, et al. (2012) Polar and brown bear genomes reveal ancient admixture and demographic footprints of past climate change. Proc Natl Acad Sci USA 109(36):E2382-E2390.
36. Miller W, et al. (2011) Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil). Proc Natl Acad Sci USA 108(30):12348-12353.
37. Giardine B, et al. (2005) Galaxy: A platform for interactive large-scale genome analysis. Genome Res 15(10):1451-1455.
38. Goecks J, Nekrutenko A, Taylor J; Galaxy Team (2010) Galaxy: A comprehensive approach for supporting accessible, reproducible, and transparent computational research in the life sciences. Genome Biol 11(8):R86.
39. Perry GH, et al. (2012) A genome sequence resource for the aye-aye (Daubentonia madagascariensis), a nocturnal lemur from Madagascar. Genome Biol Evol 4(2):126-135.
40. Ratan A, Zhang Y, Hayes VM, Schuster SC, Miller W (2010) Calling SNPs without a reference sequence. BMC Bioinformatics 11:130.
41. Perry GH, Marioni JC, Melsted P, Gilad Y (2010) Genomic-scale capture and sequencing of endogenous DNA from feces. Mol Ecol 19(24):5332-5344.
42. Reich D, Thangaraj K, Patterson N, Price AL, Singh L (2009) Reconstructing Indian population history. Nature 461(7263):489-494.
43. Willing EM, Dreyer C, van Oosterhout C (2012) Estimates of genetic differentiation measured by F (ST) do not necessarily require large sample sizes when using many SNP markers. PLoS ONE 7(8):e42649.
44. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38(6):1358-1370.
45. Wright S (1951) The genetical structure of populations. Ann Eugen 15(4):323-353.
46. Perry GH, Martin RD, Verrelli BC (2007) Signatures of functional constraint at aye-aye opsin genes: The potential of adaptive color vision in a nocturnal primate. Mol Biol Evol 24(9):1963-1970.
47. Henn BM, Cavalli-Sforza LL, Feldman MW (2012) The great human expansion. Proc Natl Acad Sci USA 109(44):17758-17764.
48. Sterling EJ (1993) Patterns of range use and social organization in aye-ayes (Dau-bentonia madagascariensis) on Nosy Mangabe. Lemur Social Systems and Their Ecological Basis, eds Kappeler PM, Ganzhorn JU (Plenum, New York), pp 1-10.
49. Burney DA, et al. (2004) A chronology for late prehistoric Madagascar. J Hum Evol 47(1-2):25-63.
50. Dewar RE, Richard AF (2012) Madagascar: A history of arrivals, what happened, and what will happen next. Annu Rev Anthropol 41:495-517.
51. Green GM, Sussman RW (1990) Deforestation history of the eastern rain forests of madagascar from satellite images. Science 248(4952):212-215.
52. Harper GJ, Steininger MK, Tucker CJ, Juhn D, Hawkins F (2007) Fifty years of deforestation and forest fragmentation in Madagascar. Environ Conserv 34(4):325-333.
53. Fischer A, Pollack J, Thalmann O, Nickel B, Paabo S (2006) Demographic history and genetic differentiation in apes. Curr Biol 16(11):1133-1138.
54. Wilmé L, Goodman SM, Ganzhorn JU (2006) Biogeographic evolution of Madagascar' s microendemic biota. Science 312(5776):1063-1065.
55. Goodman SM, Ganzhorn JU (2004) Elevational ranges of lemurs in the humid forests of Madagascar. Int J Primatol 25(2):331-350.
56. Simberloff D (1998) Flagships, umbrellas, and keystones: Is single-species management passe in the landscape era? Biol Conserv 83(3):247-257.
57. Caro T (2010) Conservation by Proxy: Indicator, Umbrella, Keystone, Flagship and Other Surrogate Species (Island Press, Washington, DC).
58. Hess GR, et al. (2006) Effectiveness of biodiversity indicators varies with extent, grain, and region. Biol Conserv 132(4):448-457.
59. Sergio F, Newton I, Marchesi L, Pedrini P (2006) Ecologically justified charisma: Preservation of top predators delivers biodiversity conservation. J Appl Ecol 43(6):1049-1055.
60. Sanderson EW, Redford KH, Vedder A, Coppolillo PB, Ward SE (2002) A conceptual model for conservation planning based on landscape species requirements. Landsc Urban Plan 58(1):41-56.
61. Didier KA, et al. (2009) The Landscape Species Approach: Spatially-explicit conservation planning applied in the Adirondacks, USA, and San Guillermo-Laguna Brava, Argentina, landscapes. Oryx 43(4):476-487.
62. Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual (Cold Spring Harbor Lab Press, Cold Spring Harbor), 3rd Ed.
63. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics 25(14):1754-1760.
64. Li H, et al.; 1000 Genome Project Data Processing Subgroup (2009) The Sequence Alignment/Map format and SAMtools. Bioinformatics 25(16):2078-2079.
65. Li JZ, et al. (2008) Worldwide human relationships inferred from genome-wide patterns of variation. Science 319(5866):1100-1104.
66. Patterson N, Price AL, Reich D (2006) Population structure and eigenanalysis. PLoS Genet 2(12):e190.
67. Alexander DH, Novembre J, Lange K (2009) Fast model-based estimation of ancestry in unrelated individuals. Genome Res 19(9):1655-1664.
68. Ahn SM, et al. (2009) The first Korean genome sequence and analysis: Full genome sequencing for a socio-ethnic group. Genome Res 19(9):1622-1629.
69. Bentley DR, et al. (2008) Accurate whole human genome sequencing using reversible terminator chemistry. Nature 456(7218):53-59.
70. Fujimoto A, et al. (2010) Whole-genome sequencing and comprehensive variant analysis of a Japanese individual using massively parallel sequencing. Nat Genet 42(11):931-936.
71. Wang J, et al. (2008) The diploid genome sequence of an Asian individual. Nature 456(7218):60-65.
72. Andrainarivo C, et al. (2012) Daubentonia madagascariensis, 2008. International Union for the Conservation of Nature 2012: IUCN Red List of Threatened Species. Available at http://www.iucnredlist.org/details/6302/0. Accessed on March 01, 2012.