International Journal of Primatology

, Volume 35, Issue 1, pp 55–70 | Cite as

The Promise and Practicality of Population Genomics Research with Endangered Species

Article

Abstract

Recent technological advances have dramatically reduced the cost of DNA sequencing. In addition, these methods require lower DNA quantities and qualities than did the previous generation of molecular techniques. As a result, genomic-scale studies of natural populations of endangered species, including those using noninvasively collected samples, are increasingly feasible. Such studies have the potential to advance our understanding of behavior, demography, evolutionary ecology, biogeography, and population history, and to contribute to the prioritization of conservation efforts. I point to a number of salient examples. However, there are also some current limitations and challenges associated with this scale of population genomics research in nonhuman, nonmodel species. Here, I describe the practicalities of the present state of this research while providing what is intended to be a straightforward walkthrough of the technology and methods involved.

Keywords

Conservation genomics Massively parallel sequencing Nonmodel species Population genomics 

References

  1. Albert, T. J., Molla, M. N., Muzny, D. M., Nazareth, L., Wheeler, D., Song, X., et al. (2007). Direct selection of human genomic loci by microarray hybridization. Nature Methods, 4(11), 903–905.Google Scholar
  2. Allendorf, F. W., Hohenlohe, P. A., & Luikart, G. (2010). Genomics and the future of conservation genetics. Nature Reviews Genetics, 11(10), 697–709.PubMedCrossRefGoogle Scholar
  3. Amato, K. R., Yeoman, C. J., Kent, A., Righini, N., Carbonero, F., Estrada, A., et al. (2013). Habitat degradation impacts black howler monkey (Alouatta pigra) gastrointestinal microbiomes. The ISME Journal, 7(7), 1344–1353.Google Scholar
  4. Arandjelovic, M., Guschanski, K., Schubert, G., Harris, T. R., Thalmann, O., Siedel, H., et al. (2009). Two-step multiplex polymerase chain reaction improves the speed and accuracy of genotyping using DNA from noninvasive and museum samples. Molecular Ecology Resources, 9, 28–36.Google Scholar
  5. Baird, N. A., Etter, P. D., Atwood, T. S., Currey, M. C., Shiver, A. L., Lewis, Z. A., et al. (2008). Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One, 3(10), e3376.Google Scholar
  6. Bell, O., Tiwari, V. K., Thoma, N. H., & Schubeler, D. (2011). Determinants and dynamics of genome accessibility. Nature Reviews Genetics, 12(8), 554–564.PubMedCrossRefGoogle Scholar
  7. Bergey, C. M., Pozzi, L., Disotell, T. R., & Burrell, A. S. (2013). A new method for genome-wide marker development and genotyping holds great promise for molecular primatology. International Journal of Primatology, 34(2), 303–314.CrossRefGoogle Scholar
  8. Bock, C. (2012). Analysing and interpreting DNA methylation data. Nature Reviews Genetics, 13(10), 705–719.PubMedCrossRefGoogle Scholar
  9. Briggs, A. W., Good, J. M., Green, R. E., Krause, J., Maricic, T., Stenzel, U., et al. (2009). Targeted retrieval and analysis of five Neandertal mtDNA genomes. Science, 325, 318–321.Google Scholar
  10. Buchan, J. C., Archie, E. A., van Horn, R. C., Moss, C. J., & Alberts, S. C. (2005). Locus effects and sources of error in noninvasive genotyping. Molecular Ecology Notes, 5, 680–683.CrossRefGoogle Scholar
  11. Burbano, H. A., Hodges, E., Green, R. E., Briggs, A. W., Krause, J., Meyer, M., et al. (2010). Targeted investigation of the Neandertal genome by array-based sequence capture. Science, 328(5979), 723–725.Google Scholar
  12. Degnan, P. H., Pusey, A. E., Lonsdorf, E. V., Goodall, J., Wroblewski, E. E., Wilson, M. L., et al. (2012). Factors associated with the diversification of the gut microbial communities within chimpanzees from Gombe National Park. Proceedings of the National Academy of Sciences of the USA, 109(32), 13034–13039.Google Scholar
  13. Ekblom, R., Farrell, L. L., Lank, D. B., & Burke, T. (2012). Gene expression divergence and nucleotide differentiation between males of different color morphs and mating strategies in the ruff. Ecology & Evolution, 2(10), 2485–2505.CrossRefGoogle Scholar
  14. Ekblom, R., & Galindo, J. (2011). Applications of next generation sequencing in molecular ecology of non-model organisms. Heredity, 107(1), 1–15.PubMedCrossRefGoogle Scholar
  15. Fonseca, N. A., Rung, J., Brazma, A., & Marioni, J. C. (2012). Tools for mapping high-throughput sequencing data. Bioinformatics, 28(24), 3169–3177.PubMedCrossRefGoogle Scholar
  16. Gayral, P., Weinert, L., Chiari, Y., Tsagkogeorga, G., Ballenghien, M., & Galtier, N. (2011). Next-generation sequencing of transcriptomes: A guide to RNA isolation in nonmodel animals. Molecular Ecology Resources, 11(4), 650–661.PubMedCrossRefGoogle Scholar
  17. George, R. D., McVicker, G., Diederich, R., Ng, S. B., MacKenzie, A. P., Swanson, W. J., et al. (2011). Trans genomic capture and sequencing of primate exomes reveals new targets of positive selection. Genome Research, 21(10), 1686–1694.Google Scholar
  18. Glenn, T. C. (2011). Field guide to next-generation DNA sequencers. Molecular Ecology Resources, 11(5), 759–769.PubMedCrossRefGoogle Scholar
  19. Gnirke, A., Melnikov, A., Maguire, J., Rogov, P., LeProust, E. M., Brockman, W., et al. (2009). Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nature Biotechnology, 27, 182–189.Google Scholar
  20. Guschanski, K., Krause, J., Sawyer, S., Valente, L. M., Bailey, S., Finstermeier, K., et al. (2013). Next-generation museomics disentangles one of the largest primate radiations. Systematic Biology, 62(4), 539–554.Google Scholar
  21. Hohenlohe, P. A., Day, M. D., Amish, S. J., Miller, M. R., Kamps-Hughes, N., Boyer, M. C., et al. (2013). Genomic patterns of introgression in rainbow and westslope cutthroat trout illuminated by overlapping paired-end RAD sequencing. Molecular Ecology, 22(11), 3002–3013.Google Scholar
  22. International Human Genome Sequencing Consortium. (2004). Finishing the euchromatic sequence of the human genome. Nature, 431, 931–945.CrossRefGoogle Scholar
  23. Jennings, T. N., Knaus, B. J., Mullins, T. D., Haig, S. M., & Cronn, R. C. (2011). Multiplexed microsatellite recovery using massively parallel sequencing. Molecular Ecology Resources, 11(6), 1060–1067.PubMedCrossRefGoogle Scholar
  24. Kohn, M. H. (2010). Noninvasive genome sampling in chimpanzees. Molecular Ecology, 19(24), 5328–5331.PubMedCrossRefGoogle Scholar
  25. Kuczynski, J., Lauber, C. L., Walters, W. A., Parfrey, L. W., Clemente, J. C., Gevers, D., et al. (2012). Experimental and analytical tools for studying the human microbiome. Nature Reviews Genetics, 13(1), 47–58.Google Scholar
  26. Leffler, E. M., Bullaughey, K., Matute, D. R., Meyer, W. K., Segurel, L., Venkat, A., et al. (2012). Revisiting an old riddle: What determines genetic diversity levels within species? PLoS Biology, 10(9), e1001388.Google Scholar
  27. Li, H., & Durbin, R. (2009). Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinformatics, 25(14), 1754–1760.PubMedCrossRefGoogle Scholar
  28. Li, H., Handsaker, B., Wysoker, A., Fennell, T., Ruan, J., Homer, N., et al. (2009). The sequence alignment/map format and SAMtools. Bioinformatics, 25(16), 2078–2079.Google Scholar
  29. Li, H., & Homer, N. (2010). A survey of sequence alignment algorithms for next-generation sequencing. Brief Bioinformatics, 11(5), 473–483.PubMedCrossRefGoogle Scholar
  30. Mardis, E. R. (2008). Next-generation DNA sequencing methods. Annual Review of Genomics and Human Genetics, 9, 387–402.PubMedCrossRefGoogle Scholar
  31. Maricic, T., Whitten, M., & Paabo, S. (2010). Multiplexed DNA sequence capture of mitochondrial genomes using PCR products. PLoS One, 5(11), e14004.PubMedCentralPubMedCrossRefGoogle Scholar
  32. Mason, V. C., Li, G., Helgen, K. M., & Murphy, W. J. (2011). Efficient cross-species capture hybridization and next-generation sequencing of mitochondrial genomes from noninvasively sampled museum specimens. Genome Research, 21(10), 1695–1704.PubMedCrossRefGoogle Scholar
  33. McKelvey, K. S., & Schwartz, M. K. (2004). Genetic errors associated with population estimation using non-invasive molecular tagging: Problems and new solutions. Journal of Wildlife Management, 68, 439–448.CrossRefGoogle Scholar
  34. McKenna, A., Hanna, M., Banks, E., Sivachenko, A., Cibulskis, K., Kernytsky, A., et al. (2010). The Genome Analysis Toolkit: A MapReduce framework for analyzing next-generation DNA sequencing data. Genome Research, 20(9), 1297–1303.Google Scholar
  35. Miller, W., Hayes, V. M., Ratan, A., Petersen, D. C., Wittekindt, N. E., Miller, J., et al. (2011). Genetic diversity and population structure of the endangered marsupial Sarcophilus harrisii (Tasmanian devil). Proceedings of the National Academy of Sciences of the USA, 108(30), 12348–12353.Google Scholar
  36. Miller, W., Schuster, S. C., Welch, A. J., Ratan, A., Bedoya-Reina, O. C., Zhao, F., et al. (2012). Polar and brown bear genomes reveal ancient admixture and demographic footprints of past climate change. Proceedings of the National Academy of Sciences of the USA, 109(36), E2382–E2390.Google Scholar
  37. Nielsen, R., Paul, J. S., Albrechtsen, A., & Song, Y. S. (2011). Genotype and SNP calling from next-generation sequencing data. Nature Reviews Genetics, 12(6), 443–451.PubMedCentralPubMedCrossRefGoogle Scholar
  38. Noonan, J. P., Coop, G., Kudaravalli, S., Smith, D., Krause, J., Alessi, J., et al. (2006). Sequencing and analysis of Neanderthal genomic DNA. Science, 314(5802), 1113–1118.Google Scholar
  39. Ouborg, N. J., Pertoldi, C., Loeschcke, V., Bijlsma, R. K., & Hedrick, P. W. (2010). Conservation genetics in transition to conservation genomics. Trends in Genetics, 26(4), 177–187.PubMedCrossRefGoogle Scholar
  40. Parga, J. A., Sauther, M. L., Cuozzo, F. P., Jacky, I. A., & Lawler, R. R. (2012). Evaluating ring-tailed lemurs (Lemur catta) from southwestern Madagascar for a genetic population bottleneck. American Journal of Physical Anthropology, 147(1), 21–29.PubMedCrossRefGoogle Scholar
  41. Peery, M. Z., Kirby, R., Reid, B. N., Stoelting, R., Doucet-Beer, E., Robinson, S., et al. (2012). Reliability of genetic bottleneck tests for detecting recent population declines. Molecular Ecology, 21(14), 3403–3418.Google Scholar
  42. Perry, G. H., Louis, E. E., Jr., Ratan, A., Bedoya-Reina, O. C., Burhans, R. C., Lei, R., et al. (2013). Aye-aye population genomic analyses highlight an important center of endemism in northern Madagascar. Proceedings of the National Academy of Sciences of the USA, 110(15), 5823–5828.Google Scholar
  43. Perry, G. H., Marioni, J. C., Melsted, P., & Gilad, Y. (2010). Genomic-scale capture and sequencing of endogenous DNA from feces. Molecular Ecology, 19(24), 5332–5344.PubMedCentralPubMedCrossRefGoogle Scholar
  44. Perry, G. H., Melsted, P., Marioni, J. C., Wang, Y., Bainer, R., Pickrell, J. K., et al. (2012a). Comparative RNA sequencing reveals substantial genetic variation in endangered primates. Genome Research, 22(4), 602–610.Google Scholar
  45. Perry, G. H., Reeves, D., Melsted, P., Ratan, A., Miller, W., Michelini, K., et al. (2012b). A Genome sequence resource for the aye-aye (Daubentonia madagascariensis), a nocturnal lemur from Madagascar. Genome Biology and Evolution, 4(2), 126–135.Google Scholar
  46. Pompanon, F., Deagle, B. E., Symondson, W. O., Brown, D. S., Jarman, S. N., & Taberlet, P. (2012). Who is eating what: Diet assessment using next generation sequencing. Molecular Ecology, 21(8), 1931–1950.PubMedCrossRefGoogle Scholar
  47. Quemere, E., Amelot, X., Pierson, J., Crouau-Roy, B., & Chikhi, L. (2012). Genetic data suggest a natural prehuman origin of open habitats in northern Madagascar and question the deforestation narrative in this region. Proceedings of the National Academy of Sciences of the USA, 109(32), 13028–13033.PubMedCrossRefGoogle Scholar
  48. Shokralla, S., Spall, J. L., Gibson, J. F., & Hajibabaei, M. (2012). Next-generation sequencing technologies for environmental DNA research. Molecular Ecology, 21(8), 1794–1805.PubMedCrossRefGoogle Scholar
  49. St. John, J., & Quinn, T. W. (2008). Rapid capture of DNA targets. Biotechniques, 44(2), 259–264.PubMedCrossRefGoogle Scholar
  50. Steiner, C. C., Putnam, A. S., Hoeck, P. E. A., & Ryder, O. A. (2013). Conservation genomics of threatened animal species. Annual Review of Animal Biosciences, 1, 261–281.CrossRefGoogle Scholar
  51. Taberlet, P., Waits, L. P., & Luikart, G. (1999). Noninvasive genetic sampling: Look before you leap. Trends in Ecology & Evolution, 14(8), 323–327.CrossRefGoogle Scholar
  52. The 1000 Genomes Project Consortium. (2010). A map of human genome variation from population-scale sequencing. Nature, 467, 1061–1073.PubMedCentralCrossRefGoogle Scholar
  53. Tung, J., Primus, A., Bouley, A. J., Severson, T. F., Alberts, S. C., & Wray, G. A. (2009). Evolution of a malaria resistance gene in wild primates. Nature, 460(7253), 388–391.PubMedGoogle Scholar
  54. Van Bortle, K., & Corces, V. G. (2012). Nuclear organization and genome function. Annual Review of Cell and Developmental Biology, 28, 163–187.PubMedCentralPubMedCrossRefGoogle Scholar
  55. Wang, Z., Gerstein, M., & Snyder, M. (2009). RNA-Seq: A revolutionary tool for transcriptomics. Nature Reviews Genetics, 10(1), 57–63.PubMedCentralPubMedCrossRefGoogle Scholar
  56. Zhao, S., Zheng, P., Dong, S., Zhan, X., Wu, Q., Guo, X., et al. (2013). Whole-genome sequencing of giant pandas provides insights into demographic history and local adaptation. Nature Genetics, 45(1), 67–71.4.Google Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  1. 1.Departments of Anthropology and BiologyPennsylvania State UniversityUniversity ParkUSA

Personalised recommendations