Morphological characterization of a brown lemur hybrid zone (Eulemur rufifrons × E. cinereiceps)

American Journal of Physical Anthropology

Volumn 145, Issue 1, 2011, Pages 55-66

  Delmore, Kira E ^a,c   Louis Jr , Edward E ^b   Johnson, Steig E ^a  

^a UNIVERSITY OF CALGARY   (Canada)

^b Henry Doorly Zoo   (United States)

^c UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Eulemur; hybridization; Madagascar; morphological variation

Indexed keywords

ARTICLE; BODY MASS; HABITAT; HYBRIDIZATION; LEMURIDAE; MORPHOLOGY; NONHUMAN; SEX DIFFERENCE; SKINFOLD THICKNESS;

ANIMALS; ANTHROPOMETRY; FEMALE; GENETICS, POPULATION; HAIR; HYBRIDIZATION, GENETIC; LEMUR; MADAGASCAR; MALE; PHENOTYPE; POLYMORPHISM, GENETIC; PRINCIPAL COMPONENT ANALYSIS;

EID: 79954530833     PISSN: 00029483     EISSN: 10968644     Source Type: Journal    
DOI: 10.1002/ajpa.21466     Document Type: Article

References (80)

1. Aguiar LM, Pie MR, Passos FC,. 2008. Wild mixed groups of howler species (Alouatta caraya and Alouatta clamitans) and new evidence for their hybridization. Primates 49: 149-152. (Pubitemid 351385777)
2. Alberts SC, Altmann J,. 2001. Immigration and hybridization patterns of yellow and anubis baboons in and around Amboseli. Kenya. Am J Primatol 53: 139-154. (Pubitemid 32337478)
3. Allen J,. 1877. The influence of physical conditions in the genesis of species. Radical Rev 1: 108-140.
4. Andersson M,. 1994. Sexual selection. Princeton: Princeton University Press.
5. Arnold M, Meyer A,. 2006. Natural hybridization in primates: one evolutionary mechanism. Zoology 109: 261-276. (Pubitemid 44572717)
6. Baden AL, Brenneman RA, Louis EE Jr,. 2008. Morphometrics of wild black-and-white ruffed lemurs [Varecia variegata; Kerr, 1792]. Am J Primatol 70: 913-926.
7. Barton NH, Hewitt GM,. 1985. Analysis of hybrid zones. Annu Rev Ecol Syst 16: 113-148.
8. Bergman TJ, Beehner JC,. 2003. Social system of a hybrid baboon group (Papio anubis × P. hamadryas). Int J Primatol 25: 1313-1330. (Pubitemid 39351389)
9. Bergman TJ, Phillips-Conroy JE, Jolly CJ,. 2008. Behavioral variation and reproductive success of male baboons (Papio anubis × Papio hamadryas) in a hybrid social group. Am J Primatol 70: 136-147. (Pubitemid 351218685)
10. Burell AS, Jolly CJ, Tosi AJ, Disotell TR,. 2009. Mitochondrial evidence for the hybrid origin of the kipunji. Rungwecebus kipunji (Primates: Papionini). Mol Phylogenet Evol 51: 340-348.
11. Butynski TM,. 1990. Comparative ecology of blue monkeys (Cercopithecus mitis) in high- and low-density subpopulations. Ecol Monogr 60: 1-26. (Pubitemid 120025820)
12. Bynum EL, Bynum DZ, Supriatna J,. 1997. Confirmation and location of the hybrid zone between wild populations of Macaca tonkeana and Macaca hecki in central Sulawesi. Indonesia. Am J Primatol 43: 181-209. (Pubitemid 27486552)
13. Bynum N,. 2002. Morphological variation with a macaque hybrid zone. Am J Primatol 118: 45-49. (Pubitemid 34327045)
14. Ciani AC, Stanyon R, Scheffrahn W, Sampurno B,. 1989. Evidence of gene flow between Sulawesi macaques. Am J Primatol 17: 257-270.
15. Clark MR, O'Neil JAS,. 1999. Morphometric comparison of Chinese-origin and Indian-derived rhesus monkeys (Macaca mulatta). Am J Primatol 4: 335-346. (Pubitemid 29167436)
16. Coyne JA, Orr HA,. 2004. Speciation. Sunderland, Massachusettes: Sinauer Associates, Inc.
17. Dalecky A, Kerdelhué C, Johnson S, Razafindratsika V, Razafiarimalala A, Overdorff D, Rasplus J-Y,. 2003. Malagasy Ficus (Moraceae) and associated fauna. In:, Goodman S, Benstead J, editors. The natural history of Madagascar. Chicago: University of Chicago Press. p 322-334.
18. Delmore KE,. 2009. Maintenance of stability in the Andringitra Brown Lemur Hybrid Zone. Master's thesis. Calgary: University of Calgary.
19. Detwiler KM, Burrell AS, Jolly CJ,. 2005. Conservation implications of hybridization in African cercopithecine monkeys. Int J Primatol 26: 661-684. (Pubitemid 40850060)
20. Djlelati R, Brun B, Rumpler Y,. 1997. Meiotic study of hybrids in the genus Eulemur and taxonomic considerations. Am J Primatol 42: 235-245. (Pubitemid 27288688)
21. Evans BJ, Supriatna J, Melnick DJ,. 2001. Hybridization and population genetics of two macaque species in Sulawesi. Indonesia. Evolution 55: 1686-1702. (Pubitemid 32908230)
22. Fleagle JG,. 1999. Primate adaptation and evolution. San Diego: Academic Press.
23. Fooden J,. 1997. Tail length variation in Macaca fascicularis and M. mulatta. Primates 38: 221-231.
24. Fooden J, Albrecht JH,. 1999. Tail-length evolution in fascicularis-group macaques (Cercopithecidae: Macaca). Int J Primatol 20: 431-440. (Pubitemid 29345326)
25. Froehlich JW, Supriatna J,. 1996. Secondary integradation between Macaca maurus and M. tonkeana in South Sulawesi, and the species status of M. togeanus. In:, Fa J, editor. Evolution and ecology of macaque societies. Cambridge: Cambridge University Press. p 43-70. (Pubitemid 27003813)
26. Gerson JS,. 1999. Size in Eulemur fulvus rufus from western Madagascar: sexual dimorphism and ecogeographic variation. Am J Phys Anthropol Suppl 28: 134.
27. Gerson JS,. 2000. Social relationships in wild red-fronted brown lemurs (Eulemur fulvus rufus). Ph.D. dissertation. Durham: Duke University.
28. Glander KE, Wright PC, Daniels PS, Merenlender AM,. 1992. Morphometrics and testicle size of rain forest lemur species from southeastern Madagascar. J Hum Evol 22: 1-17.
29. Gligor M, Ganzhorn JU, Rakotondravony D, Ramilijaona OR, Razafimahatratra E, Zischler H, Hapke A,. 2009. Hybridization between mouse lemurs in an ecological transition zone in southern Madagascar. Mol Ecol 18: 520-533.
30. Goodman SM, Andrianarimisa A,. 1996. Meteorology. Fieldiana: Zoology 85: 20-23.
31. Goodman SM, Ganzhorn JU,. 2004. Biogeography of lemurs in the humid forests of Madagascar: the role of elevational distribution and rivers. J Biogeogr 31: 47-55. (Pubitemid 38106649)
32. Goodman SM, Rasolonandrasana B,. 1999. Introduction. In:, Goodman S, Rasolonandrasana B, editors. Inventaire biologique de la réserve spéciale du Pic d'Ivohibe et du couloir forestier qui la relie au Parc National d'Andringitra. Antananarivo: Centre d'information et de documentation scientifique and technique. p 1-21.
33. Goodman SM, Razafindratsita V,. 2001. Introduction. In:, Goodman S, Razafindratsita V, editors. Inventaire biologique du Parc National de Ranomafana et du couloir forestier qui la relie au Parc National d'Andringitra. Antananarivo: Centre d'information et de documentation scientifique et technique. p 1-20.
34. Groves CP,. 2001. Primate taxonomy. Washington, DC: Smithsonian Institution Press.
35. Groves CP,. 2007. Red-fronted lemurs are not the same as red lemurs. Australasian Primatol 18 (Abstract): 23.
36. Hamada Y, Suryobroto B, Goto S, Malaivijitnond S,. 2008. Morphological and body color variation in Thai Macaca fascicularis fascicularis north and south of the Isthmus of Kra. Int J Primatol 29: 1271-1294.
37. Harcourt AH,. 1995. Sexual selection and sperm competition in primates: What are male genitalia good for? Evol Anthropol 4: 121-129. (Pubitemid 126060510)
38. Harcourt AH, Schreier BM,. 2009. Diversity, body mass, and longitudinal gradients in primates. Int J Primatol 30: 283-300.
39. Harrison RG,. 1990. Hybrid zones: windows on evolutionary process. In:, Futuyma D, Antonovics J, editors. Oxford surveys in evolutionary biology. Oxford: Oxford University Press. p 69-128.
40. Irwin MT, Johnson SE, Wright PC,. 2005. The state of lemur conservation in south-eastern Madagascar: population and habitat assessments for diurnal and cathemeral lemurs using surveys, satellite imagery and GIS. Oryx 39: 204-218.
41. Johnson SE,. 2002. Ecology and speciation in brown lemurs: white-collared lemurs (Eulemur albocollaris) and hybrids (Eulemur albocollaris × Eulemur fulvus rufus) in southeastern Madagascar. Ph.D. dissertation. Austin: University of Texas.
42. Johnson SE, Gordon AD, Stumpf RM, Overdorff DJ, Wright PC,. 2005. Morphological variation in populations of Eulemur albocollaris and E. fulvus rufus. Int J Primatol 26: 1399-1416. (Pubitemid 43036842)
43. Johnson SE, Lei R, Martin SK, Irwin MT, Louis EEJ,. 2008. Does Eulemur cinereiceps exist? Preliminary evidence from genetics and ground surveys in southeastern Madagascar. Am J Primatol 70: 372-385.
44. Johnson SE, Overdorff DJ,. 1999. Census of brown lemurs (Eulemur fulvus sspp.) in southeastern Madagascar: methods-testing and conservation implications. Am J Primatol 47: 51-60. (Pubitemid 29025716)
45. Kappeler PM,. 1996. Intrasexual selection and phylogenetic constraints in the evolution of sexual canine dimorphism in strepsirhine primates. J Evol Biol 9: 43-65.
46. Lahann P, Schmid J, Ganzhorn JU,. 2006. Geographic variation in populations of Microcebus murinus in Madagascar: resource seasonality or Bergmann's rule? Int J Primatol 27: 938-999.
47. Lehman S, Mayor M, Wright P,. 2005. Ecogeographic size variation in sifakas: a test of the resource seasonality and resource quality hypotheses. Am J Phys Anthropol 126: 318-328. (Pubitemid 40223526)
48. Lewis RJ, Kappeler PM,. 2005. Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi in the Kirindy Forest. Am J Primatol 67: 347-364. (Pubitemid 43257874)
49. Louis EE Jr, Engberg SE, Lei R, Geng H, Sommer JA, Randriamampionona R, Randriamanana JC, Zaonarivelo JR, Andriantompohavana R, Randria G, Prosper, Ramaromilanto B, Rakotoarisoa G, Rooney A, Brenneman RA,. 2006. Molecular and morphological analyses of the sportive lemurs (Family Megaladapidae: Genus Lepilemur) reveals 11 previously unrecognized species. Texas Tech University Museum Special Publications SP 49: 1-47.
50. Louis EE Jr, Ratsimbazafy JH, Razakamaharauo VR, Pierson DJ, Barber RC, Brenneman RA,. 2005. Conservation genetics of black and white ruffed lemurs. Varecia variegata, from Southeastern Madagascar. Anim Conserv 8: 105-111. (Pubitemid 40383149)
51. Mittermeier RA, Ganzhorn JU, Konstant WR, Glander K, Tattersall I, Groves CP, Rylands AB, Hapke A, Ratsimbazafy J, Mayor MI, Louis Jr. EE, Rumpler Y, Schwitzer C, Rasoloarison RM,. 2008. Lemur diversity in Madagascar. Int J Primatol 29: 1607-1656.
52. Mittermeier RA, Langrand O, Lowry PP,. 2004. Madagascar and the Indian Ocean Islands. In:, Mittermeier RA, Gil PRG, Hoffmann M, editors. Hotspots revisited: earth's biologically richest and most endangered terrestrial ecoregions. Mexico City: Cemex. p 138-144.
53. Moore WS,. 1977. An evaluation of narrow hybrid zones in vertebrates. Q Rev Biol 52: 263-277.
54. Muldoon KM, Simons EL,. 2007. Ecogeographic size variation in small-bodied subfossil primates from Ankilitelo. Southwestern Madagascar. Am J Phys Anthropol 134: 152-161. (Pubitemid 47438650)
55. Myers N, Mittermeier RA, Mittermeier CG, da Fonseca GAB, Kent J,. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853-858. (Pubitemid 30130979)
56. Overdorff DJ,. 1991. Ecological correlates to social structure in two prosimian primates: Eulemur fulvus rufus and Eulemur rubriventer in Madagascar. Ph.D. dissertation. Durham: Duke University.
57. Overdorff DJ,. 1993. Similarities, differences, and seasonal patterns in the diets of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park. Madagascar. Int J Primatol 14: 721-753. (Pubitemid 2008763)
58. Pastorini J, Forstner MRJ, Martin RD,. 2000. Relationships among brown lemurs (Eulemur fulvus) based on mitochondrial DNA sequences. Mol Phylogenet Evol 16: 418-429.
59. Pastorini J, Thalmann U, Martin RD,. 2003. A molecular approach to comparative phylogeography of extant Malagasy lemurs. Proc Natl Acad Sci USA 100: 5879-5884. (Pubitemid 36576901)
60. Pastorini J, Zaramody A, Curtis DJ, Nievergelt CM, Mundy NI,. 2009. Genetic analysis of hybridization and introgression between wild mongoose and brown lemurs. BMC Evol Biol 9: 32.
61. Paterson JD,. 1996. Coming to America: acclimation in macaque body structures and Bergmann's rule. Int J Primatol 17: 585-611. (Pubitemid 26352013)
62. Pereira ME, Kappeler PM,. 1997. Divergent systems of agnostic behaviour in Lemurid primates. Behaviour 134: 225-274.
63. Phillips-Conroy JE, Jolly CJ,. 1986. Changes in the structure of the baboon hybrid zone in the Awash National Park. Ethiopia. Am J Phys Anthropol 71: 337-350.
64. Plavcan JM, van Schaik CP,. 1992. Intrasexual competition and canine dimorphism in anthropoid primates. Am J Phys Anthropol 87: 461-477.
65. Plavcan JM, van Schaik CP,. 1997. Intrasexual competition and body weight dimorphism in anthropoid primates. Am J Phys Anthropol 103: 37-68. (Pubitemid 27240900)
66. Quinn GP, Keough MJ,. 2002. Experimental design and data analysis for biologists. Melbourne: Cambridge University Press.
67. Roberts TE, Davenport TRB, Hildebrandt KBP, Jones T, Stanley WT, Sargis EJ, Olson LE,. 2010. The biogeography of introgression in the critically endangered African monkey Rungwecebus kipunji. Biol Letters 6: 233-237.
68. Schillaci MA, Jones-Engel L, Lee BPY-H, Fuentes A, Aggimarangsee N, Engel GA, Sutthipat T,. 2007. Morphology and somatometric growth of long-tailed macaques (Macaca fascicularis fascicularis) in Singapore. Biol J Linn Soc Lond 92: 675-694. (Pubitemid 350221972)
69. de Souza Jesus A, Schunemann HE, Müller J, da Silva MA, Bicca-Marques JC,. 2010. Hybridization between Alouatta caraya and Alouatta guariba clamitans in captivity. Primates 51: 227-230.
70. Sterling E, Ramarason MG,. 1996. Rapid assessment of the primate fauna of the eastern slopes of the Réserve Naturelle Intégrale d'Andringitra. Madagascar. Fieldiana: Zoology 85: 293-305.
71. Struhsaker TT, Butynski TM, Lwanga JS,. 1988. Hybridization between redtail (Cercopithecus ascanius schmidt) and blue (C. mitis stuhlmanni) monkeys in the Kibale Forest, Uganda. In:, Gautier-Hion A, Bourlière F, Gautier J, Kingdon J, editors. A primate radiation: evolutionary biology of the African guenons. Cambridge: Cambridge University Press. p 477-497.
72. Tattersall I,. 1982. The primates of Madagascar. New York: Columbia University Press.
73. Tosi AJ, Morales JC, Melnich DJ,. 2000. Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Mol Phylogenet Evol 17: 133-144.
74. Tung J, Charpentier JE, Garfield DA, Altmann J, Alberts SC,. 2008. Genetic evidence reveals temporal change in hybridization patterns in a wild baboon population. Mol Ecol 17: 1998-2011. (Pubitemid 351521516)
75. Vick LG, Conley JM,. 1976. An ethogram for Lemur fulvus. Primates 17: 125-144.
76. Wilmé L, Goodman SM, Ganzhorn JU,. 2006. Biogeographic evolution of Madagascar's microendemic biota. Science 312: 1063-1065.
77. Woodruff DS,. 1973. Natural hybridization and hybrid zones. Syst Zool 22: 213-218.
78. Wyner Y,. 2000. Species boundaries and conservation units in two species in the family Lemuridae. Ph.D. dissertation. New York: New York University.
79. Wyner Y, Absher R, Amato G, Sterling E, Stumpf R, Rumpler Y, DeSalle R,. 1999. Species concepts and the determination of historic gene flow patterns in the Eulemur fulvus (brown lemur) complex. Biol J Linn Soc Lond 66: 39-56. (Pubitemid 29096727)
80. Wyner YM, Johnson SE, Stumpf RM, DeSalle R,. 2002. Genetic assessment of a white-collared × red-fronted lemur hybrid zone at Andringitra. Madagascar. Am J Primatol 67: 51-66. (Pubitemid 34788809)