International Journal of Primatology

, Volume 35, Issue 1, pp 32–54

The Use (and Misuse) of Phylogenetic Trees in Comparative Behavioral Analyses

  • Luca Pozzi
  • Christina M. Bergey
  • Andrew S. Burrell
Article

Abstract

Phylogenetic comparative methods play a critical role in our understanding of the adaptive origin of primate behaviors. To incorporate evolutionary history directly into comparative behavioral research, behavioral ecologists rely on strong, well-resolved phylogenetic trees. Phylogenies provide the framework on which behaviors can be compared and homologies can be distinguished from similarities due to convergent or parallel evolution. Phylogenetic reconstructions are also of critical importance when inferring the ancestral state of behavioral patterns and when suggesting the evolutionary changes that behavior has undergone. Improvements in genome sequencing technologies have increased the amount of data available to researchers. Recently, several primate phylogenetic studies have used multiple loci to produce robust phylogenetic trees that include hundreds of primate species. These trees are now commonly used in comparative analyses and there is a perception that we have a complete picture of the primate tree. But how confident can we be in those phylogenies? And how reliable are comparative analyses based on such trees? Herein, we argue that even recent molecular phylogenies should be treated cautiously because they rely on many assumptions and have many shortcomings. Most phylogenetic studies do not model gene tree diversity and can produce misleading results, such as strong support for an incorrect species tree, especially in the case of rapid and recent radiations. We discuss implications that incorrect phylogenies can have for reconstructing the evolution of primate behaviors and we urge primatologists to be aware of the current limitations of phylogenetic reconstructions when applying phylogenetic comparative methods.

Keywords

Coalescence Gene tree-species tree Molecular phylogenetics Supermatrix Supertree 

References

  1. Ané, C., Larget, B., Baum, D. A., Smith, S. D., & Rokas, A. (2007). Bayesian estimation of concordance among gene trees. Molecular Biology and Evolution, 24, 412–426.PubMedGoogle Scholar
  2. Arnason, U., Adegoke, J. A., Gullberg, A., Harley, E. H., Janke, A., & Kullberg, M. (2008). Mitogenomic relationships of placental mammals and molecular estimates of their divergences. Gene, 421, 37–51.PubMedGoogle Scholar
  3. Arnold, C., Matthews, L. J., & Nunn, C. L. (2010). The 10kTrees website: A new online resource for primate phylogeny. Evolutionary Anthropology: Issues, News, and Reviews, 19, 114–118.Google Scholar
  4. Arnold, C., & Nunn, C. L. (2010). Phylogenetic targeting of research effort in evolutionary biology. The American Naturalist, 176, 601–612.PubMedGoogle Scholar
  5. Benefit, B. R., & McCrossin, M. L. (1991). Ancestral facial morphology of Old World higher primates. Proceedings of the National Academy of Sciences of the USA, 88, 5267–5271.PubMedGoogle Scholar
  6. 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.Google Scholar
  7. Bininda-Emonds, O. R. P. (2004). The evolution of supertrees. Trends in Ecology & Evolution, 19, 315–322.Google Scholar
  8. Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., et al. (2007). The delayed rise of present-day mammals. Nature, 446, 507–512.PubMedGoogle Scholar
  9. Bininda-Emonds, O. R. P., Gittleman, J. L., & Steel, M. A. (2002). The super(tree) of life: Procedures, Problems, and Prospects. Annual Review of Ecology and Systematics, 33, 265–289.Google Scholar
  10. Blair, M. E., & Melnick, D. J. (2012). Genetic evidence for dispersal by both sexes in the Central American squirrel monkey, Saimiri oerstedii citrinellus. American Journal of Primatology, 74, 37–47.Google Scholar
  11. Blomberg, S. P., Garland, T., & Ives, A. R. (2003). Testing for phylogenetic signal in comparative data: Behavioral traits are more labile. Evolution, 57, 717–745.PubMedGoogle Scholar
  12. Bowler, M., Knogge, C., Heymann, E. W., & Zinner, D. (2012). Multilevel societies in New World primates? Flexibility may characterize the organization of Peruvian red uakaris (Cacajao calvus ucayalii). International Journal of Primatology, 33, 1110–1124.PubMedCentralPubMedGoogle Scholar
  13. Burrell, A. S., Jolly, C. J., Tosi, A. J., & Disotell, T. R. (2009). Mitochondrial evidence for the hybrid origin of the kipunji, Rungwecebus kipunji (Primates: Papionini). Molecular Phylogenetics and Evolution, 51, 340–348.PubMedGoogle Scholar
  14. Chan, Y.-C., Roos, C., Inoue-Murayama, M., Inoue, E., Shih, C.-C., Pei, K. J.-C., et al. (2010). Mitochondrial genome sequences effectively reveal the phylogeny of Hylobates gibbons. PloS One, 5, e14419.PubMedCentralPubMedGoogle Scholar
  15. Chatterjee, H. J., Ho, S. Y. W., Barnes, I., & Groves, C. (2009). Estimating the phylogeny and divergence times of primates using a supermatrix approach. BMC Evolutionary Biology, 9, 259.PubMedCentralPubMedGoogle Scholar
  16. Chaves, P. B., Alvarenga, C. S., Possamai, C. D. B., Dias, L. G., Boubli, J. P., Strier, K. B., et al. (2011). Genetic diversity and population history of a critically endangered primate, the northern muriqui (Brachyteles hypoxanthus). PloS One, 6, e20722.PubMedCentralPubMedGoogle Scholar
  17. Chiou, K. L., Pozzi, L., Lynch Alfaro, J. W., & Di Fiore, A. (2011). Pleistocene diversification of living squirrel monkeys (Saimiri spp.) inferred from complete mitochondrial genome sequences. Molecular Phylogenetics and Evolution, 59, 736–745.PubMedGoogle Scholar
  18. Cortés-Ortiz, L., Duda, T. F., Canales-Espinosa, D., García-Orduña, F., Rodríguez-Luna, E., & Bermingham, E. (2007). Hybridization in large-bodied New World primates. Genetics, 176, 2421–2425.PubMedGoogle Scholar
  19. Cronin, J., & Sarich, V. (1976). Molecular evidence for dual origin of mangabeys among Old World monkeys. Nature, 260, 700–702.PubMedGoogle Scholar
  20. Davenport, T. R. B., Stanley, W. T., Sargis, E. J., De Luca, D. W., Mpunga, N. E., Machaga, S. J., et al. (2006). A new genus of African monkey, Rungwecebus: Morphology, ecology, and molecular phylogenetics. Science, 312, 1378–1381.PubMedGoogle Scholar
  21. Degnan, J. H., & Rosenberg, N. A. (2006). Discordance of species trees with their most likely gene trees. PLoS Genetics, 2, e68.PubMedCentralPubMedGoogle Scholar
  22. Degnan, J. H., & Rosenberg, N. A. (2009). Gene tree discordance, phylogenetic inference and the multispecies coalescent. Trends in Ecology & Evolution, 24, 332–340.Google Scholar
  23. Delsuc, F., Brinkmann, H., & Philippe, H. (2005). Phylogenomics and the reconstruction of the tree of life. Nature Reviews Genetics, 6, 361–375.PubMedGoogle Scholar
  24. Detwiler, K. M., Burrell, A. S., & Jolly, C. J. (2005). Conservation implications of hybridization in African Cercopithecine monkeys. International Journal of Primatology, 26, 661–684.Google Scholar
  25. Di Fiore, A., & Rendall, D. (1994). Evolution of social organization: A reappraisal for primates by using phylogenetic methods. Proceedings of the National Academy of Sciences of the USA, 91, 9941–9945.PubMedGoogle Scholar
  26. Disotell, T. R. (1994). Generic level relationships of the Papionini (Cercopithecidae). American Journal of Physical Anthropology, 94, 47–57.PubMedGoogle Scholar
  27. Dobson, S. D. (2012). Coevolution of facial expression and social tolerance in macaques. American Journal of Primatology, 74, 229–235.PubMedGoogle Scholar
  28. Dunbar, R. I. M. (1984). Reproductive decisions: An economic analysis of gelada baboon social strategies. Princeton, NJ: Princeton University Press.Google Scholar
  29. Edgar, R. C. (2004). MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792–1797.PubMedCentralPubMedGoogle Scholar
  30. Edwards, S. V. (2009). Is a new and general theory of molecular systematics emerging? Evolution, 63, 1–19.PubMedGoogle Scholar
  31. Fabre, P.-H., Rodrigues, A., & Douzery, E. J. P. (2009). Patterns of macroevolution among Primates inferred from a supermatrix of mitochondrial and nuclear DNA. Molecular Phylogenetics and Evolution, 53, 808–825.Google Scholar
  32. Felsenstein, J. (1985). Phylogenies and the comparative method. American Naturalist, 125, 1–15.Google Scholar
  33. Finarelli, J. A., & Flynn, J. J. (2006). Ancestral state reconstruction of body size in the Caniformia (Carnivora, Mammalia): The effects of incorporating data from the fossil record. Systematic Biology, 55, 301–313.PubMedGoogle Scholar
  34. Finstermeier, K., Zinner D., Brameier M., Meyer M., Kreuz E., Hofreiter M., et al. (2013). A mitogenomic phylogeny of living primates. PloS One 8.7, e69504.Google Scholar
  35. Fleagle, J., & McGraw, W. (1999). Skeletal and dental morphology supports diphyletic origin of baboons and mandrills. Proceedings of the National Academy of Sciences of the USA, 96, 1157–1161.PubMedGoogle Scholar
  36. Galat-Luong, A., Galat, G., & Hagell, S. (2006). The social and ecological flexibility of Guinea baboons: Implications for Guinea baboon social organization and male strategies. In L. Swedell & S. Leigh (Eds.), Reproduction and fitness in baboons: Behavioral, ecological, and life history perspectives (pp. 105–121). New York: Springer.Google Scholar
  37. Garland, T., Harvey, P., & Ives, A. (1992). Procedures for the analysis of comparative data using phylogenetically independent contrasts. Systematic Biology, 41, 18–32.Google Scholar
  38. Gilbert, C. C. (2007). Craniomandibular morphology supporting the diphyletic origin of mangabeys and a new genus of the Cercocebus/Mandrillus clade, Procercocebus. Journal of Human Evolution, 53, 69–102.PubMedGoogle Scholar
  39. Gligor, M., Ganzhorn, J. U., Rakotondravony, D., Ramilijaona, O. R., Razafimahatratra, E., Zischler, H., et al. (2009). Hybridization between mouse lemurs in an ecological transition zone in southern Madagascar. Molecular Ecology, 18, 520–533.PubMedGoogle Scholar
  40. Grafen, A. (1989). The phylogenetic regression. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 326, 119–157.PubMedGoogle Scholar
  41. Green, R. E., Krause, J., Briggs, A. W., Maricic, T., Stenzel, U., Kircher, M., et al. (2010). A draft sequence of the Neandertal genome. Science, 328, 710–722.PubMedGoogle Scholar
  42. Grueter, C. C., Chapais, B., & Zinner, D. (2012). Evolution of multilevel social systems in nonhuman primates and humans. International Journal of Primatology, 33, 1002–1037.PubMedCentralPubMedGoogle Scholar
  43. Harris, E. E., & Disotell, T. R. (1998). Nuclear gene trees and the phylogenetic relationships of the mangabeys (Primates: Papionini). Molecular Biology and Evolution, 15, 892–900.PubMedGoogle Scholar
  44. Harrison, T. (2010). Apes among the tangled branches of human origins. Science, 327, 532.PubMedGoogle Scholar
  45. Harvey, P., Brown, A., Smith, J., & Nee, S. (1996). New uses for new phylogenies. Oxford: Oxford University Press.Google Scholar
  46. Harvey, P., & Pagel, M. (1991). The comparative method in evolutionary biology. Oxford Series in Ecology and Evolution, Vol 1. Oxford: Oxford University Press.Google Scholar
  47. Heled, J., & Drummond, A. J. (2010). Bayesian inference of species trees from multilocus data. Molecular Biology and Evolution, 27, 570–580.PubMedGoogle Scholar
  48. Henzi, P., & Barrett, L. (2003). Evolutionary ecology, sexual conflict, and behavioral differentiation among baboon populations. Evolutionary Anthropology, 12, 217–230.Google Scholar
  49. Henzi, S. P., & Barrett, L. (2005). The historical socioecology of savanna baboons (Papio hamadryas). Journal of Zoology, 265, 215–226.Google Scholar
  50. Hillis, D. M., Pollock, D. D., McGuire, J. A., & Zwickl, D. J. (2003). Is sparse taxon sampling a problem for phylogenetic inference? Systematic Biology, 52, 124–126.PubMedCentralPubMedGoogle Scholar
  51. Hinde, K., & Milligan, L. A. (2011). Primate milk: Proximate mechanisms and ultimate perspectives. Evolutionary Anthropology, 20, 9–23.PubMedGoogle Scholar
  52. Hodgson, J. A., Sterner, K. N., Matthews, L. J., Burrell, A. S., Rachana, A. J., Raaum, R. L., et al. (2009). Successive radiations, not stasis, in the South American primate fauna. Proceedings of the National Academy of Sciences of the USA, 106, 5534–5539.PubMedGoogle Scholar
  53. Jameson, N. M., Hou, Z.-C., Sterner, K. N., Weckle, A., Goodman, M., Steiper, M. E., et al. (2011). Genomic data reject the hypothesis of a prosimian primate clade. Journal of Human Evolution, 61, 295–305.PubMedGoogle Scholar
  54. Jolly, C. J. (1993). Species, subspecies, and baboon systematics. In W. H. Kimbell & L. B. Martin (Eds.), Species, species concepts, and primate evolution (pp. 67–107). New York: Plenum Press.Google Scholar
  55. Jolly, C. J. (2007). Baboons, mandrills, and mangabeys. Afro-papionin socioecology in a phylogenetic perspective. In C. J. Campbell, A. Fuentes, K. C. MacKinnon, M. Panger, & S. K. Bearder (Eds.), Primates in perspective (pp. 240–251). New York: Oxford University Press.Google Scholar
  56. Jolly, C. J. (2009). Fifty years of looking at human evolution. Current Anthropology, 50, 187–199.PubMedGoogle Scholar
  57. Jones, T., Ehardt, C. L., Butynski, T. M., Davenport, T. R. B., Mpunga, N. E., Machaga, S. J., et al. (2005). The highland mangabey Lophocebus kipunji: A new species of African monkey. Science, 308, 1161–1164.Google Scholar
  58. Kawai, M., Dunbar, R., Ohsawa, H., & Mori, U. (1983). Social organization of gelada baboons: Social units and definitions. Primates, 24, 13–24.Google Scholar
  59. Keller, C., Roos, C., Groeneveld, L. F., Fischer, J., & Zinner, D. (2010). Introgressive hybridization in southern African baboons shapes patterns of mtDNA variation. American Journal of Physical Anthropology, 142, 125–136.PubMedGoogle Scholar
  60. Knowles, L. L. (2009). Estimating species trees: Methods of phylogenetic analysis when there is incongruence across genes. Systematic Biology, 58, 463–467.PubMedGoogle Scholar
  61. Kubatko, L. S., Carstens, B. C., & Knowles, L. L. (2009). STEM: Species tree estimation using maximum likelihood for gene trees under coalescence. Bioinformatics, 25, 971–973.Google Scholar
  62. Kubatko, L. S., & Degnan, J. H. (2007). Inconsistency of phylogenetic estimates from concatenated data under coalescence. Systematic Biology, 56, 17–24.PubMedGoogle Scholar
  63. Kummer, H. (1968). Social organization of hamadryas baboons. Chicago: The University of Chicago Press.Google Scholar
  64. Larget, B. R., Kotha, S. K., Dewey, C. N., & Ané, C. (2010). BUCKy: Gene tree/species tree reconciliation with Bayesian concordance analysis. Bioinformatics, 26, 2910–2911.Google Scholar
  65. Leaché, A. D., & Rannala, B. (2011). The accuracy of species tree estimation under simulation: A comparison of methods. Systematic Biology, 60, 126–137.PubMedGoogle Scholar
  66. Liu, L. (2008). BEST: Bayesian estimation of species trees under the coalescent model. Bioinformatics, 24, 2542–2543.Google Scholar
  67. Liu, L., Yu, L., & Edwards, S. V. (2010). A maximum pseudo-likelihood approach for estimating species trees under the coalescent model. BMC Evolutionary Biology, 10, 302.PubMedCentralPubMedGoogle Scholar
  68. Liu, L., Yu, L., Pearl, D. K., & Edwards, S. V. (2009). Estimating species phylogenies using coalescence times among sequences. Systematic Biology, 58, 468–477.PubMedGoogle Scholar
  69. MacLean, E. L., Matthews, L. J., Hare, B. A., Nunn, C. L., Anderson, R. C., Aureli, F., et al. (2012). How does cognition evolve? Phylogenetic comparative psychology. Animal Cognition, 15, 223–238.PubMedGoogle Scholar
  70. Maddison, W. P. (1997). Gene trees in species trees. Systematic Biology, 46, 523.Google Scholar
  71. Maddison, W. P., & Knowles, L. L. (2006). Inferring phylogeny despite incomplete lineage sorting. Systematic Biology, 55, 21.PubMedGoogle Scholar
  72. Matsui, A., Rakotondraparany, F., Munechika, I., Hasegawa, M., & Horai, S. (2009). Molecular phylogeny and evolution of prosimians based on complete sequences of mitochondrial DNAs. Gene, 441, 53–66.PubMedGoogle Scholar
  73. Matthews, L. J. (2012). Variations in sexual behavior among capuchin monkeys function for conspecific mate recognition: A phylogenetic analysis and a new hypothesis for female proceptivity in tufted capuchins. American Journal of Primatology, 74, 287–298.PubMedGoogle Scholar
  74. Meng, C., & Kubatko, L. S. (2009). Detecting hybrid speciation in the presence of incomplete lineage sorting using gene tree incongruence: A model. Theoretical Population Biology, 75, 35–45.PubMedGoogle Scholar
  75. Meyer, D., Rinaldi, I. D., Ramlee, H., Perwitasari-Farajallah, D., Hodges, J. K., & Roos, C. (2011). Mitochondrial phylogeny of leaf monkeys (genus Presbytis, Eschscholtz, 1821) with implications for taxonomy and conservation. Molecular Phylogenetics and Evolution, 59, 311–319.PubMedGoogle Scholar
  76. Montgomery, S. H., Capellini, I., Barton, R. A., & Mundy, N. I. (2010). Reconstructing the ups and downs of primate brain evolution: Implications for adaptive hypotheses and Homo floresiensis. BMC Biology, 8, 9.PubMedCentralPubMedGoogle Scholar
  77. Moore, W. (1995). Inferring phylogenies from mtDNA variation: Mitochondrial-gene trees versus nuclear-gene trees. Evolution, 49, 718–726.Google Scholar
  78. Mulder, M. B. (2001). Using phylogenetically based comparative methods in anthropology: More questions than answers. Evolutionary Anthropology, 10, 99–111.Google Scholar
  79. Nabhan, A. R., & Sarkar, I. N. (2012). The impact of taxon sampling on phylogenetic inference: A review of two decades of controversy. Briefings in Bioinformatics, 13, 122–134.PubMedGoogle Scholar
  80. Nunn, C. L. (2011). The comparative approach in evolutionary anthropology and biology. Chicago: The University of Chicago Press.Google Scholar
  81. Nunn, C. L., & Barton, R. A. (2001). Comparative methods for studying primate adaptation and allometry. Evolutionary Anthropology, 10, 81–98.Google Scholar
  82. Nylander, J. A. A. (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University.Google Scholar
  83. O’Leary, M. A., Bloch, J. I., Flynn, J. J., Gaudin, T. J., Giallombardo, A., Giannini, N. P., et al. (2013). The placental mammal ancestor and the post-K-Pg radiation of placentals. Science, 339, 662–667.PubMedGoogle Scholar
  84. Olson, L. E., Sargis, E. J., Stanley, W. T., Hildebrandt, K. B. P., & Davenport, T. R. B. (2008). Additional molecular evidence strongly supports the distinction between the recently described African primate Rungwecebus kipunji (Cercopithecidae, Papionini) and Lophocebus. Molecular Phylogenetics and Evolution, 48, 789–794.PubMedGoogle Scholar
  85. Opie, C., Atkinson, Q. D., & Shultz, S. (2012). The evolutionary history of primate mating systems. Communicative & Integrative Biology, 5, 458–461.Google Scholar
  86. Owens, I. P. F. (2006). Where is behavioural ecology going? Trends in Ecology & Evolution, 21, 356–361.Google Scholar
  87. Pagel, M. (1994). Detecting correlated evolution on phylogenies: A general method for the comparative analysis of discrete characters. Proceedings of the Royal Society of London B: Biological Sciences, 255, 37–45.Google Scholar
  88. Pagel, M. (1999). Inferring the historical patterns of biological evolution. Nature, 401, 877–884.PubMedGoogle Scholar
  89. Pagel, M., & Meade, A. (2006). Bayesian analysis of correlated evolution of discrete characters by reversible-jump Markov chain Monte Carlo. The American Naturalist, 167, 808–825.PubMedGoogle Scholar
  90. Patzelt, A., Zinner, D., Fickenscher, G., Diedhiou, S., Camara, B., et al. (2011). Group composition of Guinea baboons (Papio papio) at a water place suggests fluid social organization. International Journal of Primatology, 32, 652–668.PubMedCentralPubMedGoogle Scholar
  91. Perelman, P., Johnson, W. E., Roos, C., Seuánez, H. N., Horvath, J. E., Moreira, M. A. M., et al. (2011). A molecular phylogeny of living primates. PLoS Genetics, 7.Google Scholar
  92. Perez, S. I., Klaczko, J., & Dos Reis, S. F. (2012). Species tree estimation for a deep phylogenetic divergence in the New World monkeys (Primates: Platyrrhini). Molecular Phylogenetics and Evolution, 65, 621–630.PubMedGoogle Scholar
  93. Plazzi, F., Ferrucci, R. R., & Passamonti, M. (2010). Phylogenetic representativeness: A new method for evaluating taxon sampling in evolutionary studies. BMC Bioinformatics, 11, 209.PubMedCentralPubMedGoogle Scholar
  94. Price, J. J., Clapp, M. K., & Omland, K. E. (2011). Where have all the trees gone? The declining use of phylogenies in animal behaviour journals. Animal Behaviour, 81, 667–670.Google Scholar
  95. Purvis, A. (1995). A composite estimate of primate phylogeny. Philosophical Transactions of the Royal Society of London B: Biological Sciences, 348, 405–421.PubMedGoogle Scholar
  96. Raaum, R. L., Sterner, K. N., Noviello, C. M., Stewart, C.-B., & Disotell, T. R. (2005). Catarrhine primate divergence dates estimated from complete mitochondrial genomes: Concordance with fossil and nuclear DNA evidence. Journal of Human Evolution, 48, 237–257.PubMedGoogle Scholar
  97. Rasmussen, M. D., & Kellis, M. (2012). Unified modeling of gene duplication, loss, and coalescence using a locus tree. Genome Research, 22, 755–765.PubMedGoogle Scholar
  98. Reich, D., Green, R. E., Kircher, M., Krause, J., Patterson, N., Durand, E. Y., et al. (2010). Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature, 468, 1053–1060.PubMedGoogle Scholar
  99. Rendall, D., & Fiore, A. D. (1995). The road less traveled: Phylogenetic perspectives in primatology. Evolutionary Anthropology, 4, 43–52.Google Scholar
  100. Roberts, T. E., Davenport, T. R. B., Hildebrandt, K. B. P., Jones, T., Stanley, W. T., Sargis, E. J., et al. (2010). The biogeography of introgression in the critically endangered African monkey Rungwecebus kipunji. Biology Letters, 6, 233–237.PubMedCentralPubMedGoogle Scholar
  101. Rokas, A., Williams, B. L., King, N., & Carroll, S. B. (2003). Genome-scale approaches to resolving incongruence in molecular phylogenies. Nature, 425, 798–804.PubMedGoogle Scholar
  102. Ronquist, F., Teslenko, M., van der Mark, P., Ayres, D. L., Darling, A., Höhna, S., et al. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61, 539–542.PubMedGoogle Scholar
  103. Roos, C., Schmitz, J., & Zischler, H. (2004). Primate jumping genes elucidate strepsirrhine phylogeny. Proceedings of the National Academy of Sciences of the USA, 101, 10650.PubMedGoogle Scholar
  104. Sanderson, M., Purvis, A., & Henze, C. (1998). Phylogenetic supertrees: Assembling the trees of life. Trends in Ecology & Evolution, 13, 8–12.Google Scholar
  105. Scally, A., Dutheil, J. Y., Hillier, L. W., Jordan, G. E., Goodhead, I., Herrero, J., et al. (2012). Insights into hominid evolution from the gorilla genome sequence. Nature, 483, 169–175.PubMedCentralPubMedGoogle Scholar
  106. Sherman, P. (1988). The levels of analysis. Animal Behaviour, 36, 616–619.Google Scholar
  107. Song, S., Liu, L., Edwards, S. V., & Wu, S. (2012). Resolving conflict in eutherian mammal phylogeny using phylogenomics and the multispecies coalescent model. Proceedings of the National Academy of Sciences of the USA, 109, 14942–14947.PubMedGoogle Scholar
  108. Springer, M. S., Meredith, R. W., Gatesy, J., Emerling, C. A., Park, J., Rabosky, D. L., et al. (2012). Macroevolutionary dynamics and historical biogeography of primate diversification inferred from a species supermatrix. PloS One, 7, e49521.PubMedCentralPubMedGoogle Scholar
  109. Stamatakis, A. (2006). RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics, 22, 2688–2690.Google Scholar
  110. Stamatakis, A., Hoover, P., & Rougemont, J. (2008). A rapid bootstrap algorithm for the RAxML Web servers. Systematic Biology, 57, 758–771.PubMedGoogle Scholar
  111. Stamatakis, A., Ludwig, T., & Meier, H. (2005). RAxML-III: A fast program for maximum likelihood-based inference of large phylogenetic trees. Bioinformatics, 21, 456–463.Google Scholar
  112. Steiper, M. E., & Seiffert, E. R. (2012). Evidence for a convergent slowdown in primate molecular rates and its implications for the timing of early primate evolution. Proceedings of the National Academy of Sciences of the USA, 109, 6006–6011.PubMedGoogle Scholar
  113. Sterner, K. N., Raaum, R. L., Zhang, Y.-P., Stewart, C.-B., & Disotell, T. R. (2006). Mitochondrial data support an odd-nosed colobine clade. Molecular Phylogenetics and Evolution, 40, 1–7.PubMedGoogle Scholar
  114. Szalay, F. S., & Delson, E. (1979). Evolutionary history of the primates. New York: Academic Press.Google Scholar
  115. Thomson, R. C., & Shaffer, H. B. (2010). Rapid progress on the vertebrate tree of life. BMC Biology, 8, 19.PubMedCentralPubMedGoogle Scholar
  116. Tinbergen, N. (1959). Comparative studies of the behaviour of gulls (Laridae): A progress report. Behaviour, 15, 1–70.Google Scholar
  117. Tinbergen, N. (1963). On aims and methods of ethology. Zeitschrift für Tierpsychologie, 20, 410–433.Google Scholar
  118. Ting, N., & Sterner, K. N. (2013). Primate molecular phylogenetics in a genomic era. Molecular Phylogenetics and Evolution, 66, 565–568.PubMedGoogle Scholar
  119. Townsend, J. P., & Leuenberger, C. (2011). Taxon sampling and the optimal rates of evolution for phylogenetic inference. Systematic Biology, 60, 358–365.PubMedGoogle Scholar
  120. Townsend, T. M., Mulcahy, D. G., Noonan, B. P., Sites, J. W., Kuczynski, C. A., Wiens, J. J., & Reeder, T. W. (2011). Phylogeny of iguanian lizards inferred from 29 nuclear loci, and a comparison of concatenated and species-tree approaches for an ancient, rapid radiation. Molecular Phylogenetics and Evolution, 61, 363–380.PubMedGoogle Scholar
  121. Weisrock, D. W., Smith, S. D., Chan, L. M., Biebouw, K., Kappeler, P. M., & Yoder, A. D. (2012). Concatenation and concordance in the reconstruction of mouse lemur phylogeny: An empirical demonstration of the effect of allele sampling in phylogenetics. Molecular Biology and Evolution, 29, 1615–1630.PubMedGoogle Scholar
  122. Wimmer, B., Tautz, D., & Kappeler, P. (2002). The genetic population structure of the gray mouse lemur (Microcebus murinus), a basal primate from Madagascar. Behavioral Ecology and Sociobiology, 52, 166–175.Google Scholar
  123. Yu, Y., Than, C., Degnan, J. H., & Nakhleh, L. (2011). Coalescent histories on phylogenetic networks and detection of hybridization despite incomplete lineage sorting. Systematic Biology, 60, 138–149.PubMedGoogle Scholar
  124. Zinner, D., Arnold, M. L., & Roos, C. (2009a). Is the new primate genus Rungwecebus a baboon? PLoS One, 4, 4859.Google Scholar
  125. Zinner, D., Arnold, M. L., & Roos, C. (2011). The strange blood: Natural hybridization in primates. Evolutionary Anthropology, 20, 96–103.Google Scholar
  126. Zinner, D., Groeneveld, L. F., Keller, C., & Roos, C. (2009b). Mitochondrial phylogeography of baboons (Papio spp.): Indication for introgressive hybridization? BMC Evolutionary Biology, 9, 83.Google Scholar
  127. Zinner, D., Wertheimer, J., Liedigk, R., Groeneveld, L. F., & Roos, C. (2013). Baboon phylogeny as inferred from complete mitochondrial genomes. American Journal of Physical Anthropology, 150, 133–140.PubMedCentralPubMedGoogle Scholar
  128. Zwickl, D. J., & Hillis, D. M. (2002). Increased taxon sampling greatly reduces phylogenetic error. Systematic Biology, 51, 588–598.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2013

Authors and Affiliations

  • Luca Pozzi
    • 1
    • 2
    • 3
  • Christina M. Bergey
    • 1
    • 2
  • Andrew S. Burrell
    • 1
  1. 1.Department of AnthropologyNew York UniversityNew YorkUSA
  2. 2.New York Consortium in Evolutionary PrimatologyNew YorkUSA
  3. 3.Behavioral Ecology and Sociobiology UnitGerman Primate CenterGöttingenGermany

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