Advertisement

International Journal of Primatology

, Volume 37, Issue 1, pp 69–88 | Cite as

Niche Divergence in a Brown Lemur (Eulemur spp.) Hybrid Zone: Using Ecological Niche Models to Test Models of Stability

  • Steig E. Johnson
  • Kira E. Delmore
  • Kerry A. Brown
  • Tracy M. Wyman
  • Edward E. LouisJr.
Article

Abstract

Endogenous selection is often implicated in the maintenance of stability of natural hybrid zones. Environmental conditions often vary across these zones, suggesting that local adaptation to ecological conditions could also play a role in this process. We used niche modeling to investigate these alternatives in a hybrid zone between two species of brown lemur (Eulemur rufifrons and E. cinereiceps) in southeastern Madagascar. We produced ecological niche models (ENMs) for parental and hybrid populations and compared values of niche overlap to null expectations using identity and background tests. All three taxonomic groups had nonequivalent ENMs with limited spatial overlap, supporting a role for niche divergence and local adaptation in the maintenance of this zone. However, values of niche overlap between ENMs were not greater than null expectations controlling for background environmental differences. These results could suggest that taxa in this hybrid zone inhabit portions of their environments that are more similar to their backgrounds, i.e., niche conservatism. Nevertheless, we did find evidence of niche divergence when using background tests that examined environmental variables separately. Although we could not rule out models indicating selection against hybrids, most lines of evidence were consistent with predictions for the bounded superiority model of hybrid zone stability. This study thus provides support that exogenous, environmental selection may be responsible for maintaining the hybrid zone, and may be implicated in the evolutionary divergence of these taxa.

Keywords

Bounded superiority Ecological niche models Geographical selection-gradient Hybrid zone Tension zone 

Notes

Acknowledgments

The authors express their appreciation to Giuseppe Donati for the invitation to contribute to this special issue. The authors also thank the government of Madagascar for permission to conduct the original research reanalyzed here. The authors are grateful for the funding that contributed to the original field research: Primate Action Fund, Primate Conservation, Inc., American Society of Primatologists, National Science and Engineering Research Council of Canada, Omaha’s Henry Doorly Zoo and Aquarium, and University of Calgary. Omaha’s Henry Doorly Zoo and Aquarium Center for Conservation and Research, Madagascar Biodiversity Partnership and Madagascar Institut pour la Conservation des Ecosystèmes Tropicaux facilitated the fieldwork. The authors also thank Alison Porter for assistance with analyses. Finally, we thank three anonymous reviewers and the editor-in-chief for their helpful suggestions to improve the manuscript.

Supplementary material

10764_2015_9872_MOESM1_ESM.r (2 kb)
ESM 1 (R 2 kb)

References

  1. Agarwal, D. K., Silander, J. A., Gelfand, A. E., Dewar, R. E., & Mickelson, J. G. (2005). Tropical deforestation in Madagascar: analysis using hierarchical spatially explicit, Bayesian regression models. Ecological Modelling, 185, 105–131.CrossRefGoogle Scholar
  2. Alexandrino, J., Baird, S. J. E., Lawson, L., Macey, J. R., Moritz, C., & Wake, D. B. (2005). Strong selection against hybrids at a hybrid zone in the Ensatina ring species complex and its evolutionary implications. Evolution, 59, 1334–1347.Google Scholar
  3. Allnutt, T. F., Ferrier, S., Manion, G., Powell, G. V. N., Ricketts, T. H., Fisher, B. L., Harper, G. J., Irwin, M. E., Kremen, C., Labat, J. N., Lees, D. C., Pearce, T. A., & Rakotondrainibe, F. (2008). A method for quantifying biodiversity loss and its application to a 50-year record of deforestation across Madagascar. Conservation Letters, 1, 173–181.CrossRefGoogle Scholar
  4. Anderson, E. (1949). Introgressive hybridization. New York: John Wiley & Sons.CrossRefGoogle Scholar
  5. Anderson, R. P., Peterson, A. T., & Gomez-Laverde, M. (2002). Using niche-based GIS modeling to test geographic predictions of competitive exclusion and competitive release in South American pocket mice. Oikos, 98, 3–16.Google Scholar
  6. Arnold, M. L. (1992). Natural hybridization as an evolutionary process. Annual Review of Ecology and Systematics, 12, 237–261.CrossRefGoogle Scholar
  7. Barton, N. H., & Hewitt, G. M. (1985). Analysis of hybrid zones. Annual Review of Ecology and Systematics, 16, 113–148.CrossRefGoogle Scholar
  8. Bigelow, R. S. (1965). Hybrid zones and reproductive isolation. Evolution, 19, 449–458.Google Scholar
  9. Blair, M. E., Sterling, E. J., Dusch, M., Raxworthy, C. J., & Pearson, R. G. (2013). Ecological divergence and speciation between lemur (Eulemur) sister species in Madagascar. Journal of Evolutionary Biology, 26, 1790–1801.CrossRefPubMedGoogle Scholar
  10. Brenneman, R. A., Johnson, S. E., Bailey, C. A., Ingraldi, C., Delmore, K. E., Wyman, T. M., Andriamaharoa, H. E., Ralainasolo, F. R., Ratsimbazafy, J. H., & Louis, E. E. (2012). Population genetics and abundance of gray-headed lemurs (Eulemur cinereiceps): potential consequences of fragmentation and cyclones in an endangered primate. Oryx, 462, 298–307.CrossRefGoogle Scholar
  11. Bronson, C. L., Grubb, T. C., & Braun, M. J. (2003). A test of the endogenous and exogenous selection hypotheses for the maintenance of a narrow avian hybrid zone. Evolution, 57, 630–637.CrossRefPubMedGoogle Scholar
  12. Delmore, K. E., Louis, E. E., & Johnson, S. E. (2011). Morphological characterization of a brown lemur hybrid zone (Eulemur rufifrons × E. cinereiceps). American Journal of Physical Anthropology, 145, 55–66.CrossRefPubMedGoogle Scholar
  13. Delmore, K. E., Brenneman, R. A., Lei, R., Bailey, C. A., Brelsford, A., Louis, E. E., & Johnson, S. E. (2013). Clinal variation in a brown lemur (Eulemur spp.) hybrid zone: combining morphological, genetic and climatic data to examine stability. Journal of Evolutionary Biology, 26, 1677–1690.CrossRefPubMedGoogle Scholar
  14. 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.CrossRefGoogle Scholar
  15. Elith, J., & Leathwick, J. R. (2009). Species distribution models: ecological explanation and prediction across space and time. Annual Review of Ecology, Evolution, and Systematics, 40, 677–697.CrossRefGoogle Scholar
  16. Elith, J., Graham, C. H., Anderson, R. P., Dudik, M., Ferrier, S., Guisan, A., Hijmans, R. J., Huettmann, F., Leathwick, J. R., Lehmann, A., Li, J., Lohmann, L. G., Loiselle, B. A., Manion, G., Moritz, C., Nakamura, M., Nakazawa, Y., Overton, J. M., Peterson, A. T., Phillips, S. J., Richardson, K., Scachetti-Pereira, R., Schapire, R. E., Soberon, J., Williams, S., Wisz, M. S., & Zimmermann, N. E. (2006). Novel methods improve prediction of species' distributions from occurrence data. Ecography, 29, 129–151.CrossRefGoogle Scholar
  17. Elith, J., Phillips, S. J., Hastie, T., Dudik, M., Chee, Y. E., & Yates, C. J. (2011). A statistical explanation of MaxEnt for ecologists. Diversity and Distributions, 17, 43–57.CrossRefGoogle Scholar
  18. Endler, J. A. (1977). Geographic variation, speciation and clines, vol. 10. Princeton: Princeton University Press.Google Scholar
  19. ESRI. (2012). ArcGIS desktop: Release 10.1. Redlands: Environmental Systems Research Institute.Google Scholar
  20. Fielding, A. H., & Bell, J. F. (1997). A review of methods for the assessment of prediction errors in conservation presence/absence models. Environmental Conservation, 21, 38–49.CrossRefGoogle Scholar
  21. Flockhart, D. T. T., & Wiebe, K. L. (2009). Absence of reproductive consequences of hybridization in the northern flicker (Colaptes auratus) hybrid zone. The Auk, 126, 351–358.CrossRefGoogle Scholar
  22. Fourcade, Y., Engler, J. O., Rödder, D., & Secondi, J. (2014). Mapping species distributions with MAXENT using a geographically biased sample of presence data: a performance assessment of methods for correcting sampling bias. PLoS ONE, 9, e97122.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Franklin, J. (2009). Mapping species distributions. Cambridge: Cambridge University Press.Google Scholar
  24. Gligor, M., Ganzhorn, J. U., Rakotondravony, D., Ramalijaona, O. R., Razafimahatratra, E., Zischler, H., & Hapke, A. (2009). Hybridization between mouse lemurs in an ecological transition zone. Molecular Ecology, 18, 520–533.CrossRefPubMedGoogle Scholar
  25. Godsoe, W. (2010). Regional variation exaggerates ecological divergence in niche models. Systematic Biology, 59, 298–306.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Good, T. P., Ellis, J. C., Annett, C. A., & Pierotti, R. (2000). Bounded hybrid superiority in an avian hybrid zone: effects of mate, diet, and habitat choice. Evolution, 54, 1774–1783.CrossRefPubMedGoogle Scholar
  27. Goodman, S. M., & Lewis, B. A. (1996). Description of the Réserve Naturelle Intégrale d'Andringitra, Madagascar. Fieldiana: Zoology, 85, 7–19.Google Scholar
  28. Grinand, C., Rakotomalala, F., Gond, V., Vaudry, R., Bernoux, M., & Vieilledent, G. (2013). Estimating deforestation in tropical humid and dry forests in Madagascar from 2000–2010 using multi-date Landsat satellite images and the random forests classifier. Remote Sensing of Environment, 139, 68–80.CrossRefGoogle Scholar
  29. Hapke, A., Gligor, M., Rakotondranary, S. J., Rosenkranz, D., & Zupke, O. (2011). Hybridization of mouse lemurs: different patterns under different ecological conditions. BMC Evolutionary Biology, 11, 297.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Harper, G. J., Steininger, M. K., Tucker, C. J., Juhn, D., & Hawkins, F. (2007). Fifty years of deforestation and forest fragmentation in Madagascar. Environmental Conservation, 34, 1–9.CrossRefGoogle Scholar
  31. Hewitt, G. (1988). Hybrid zones—natural laboratories for evolutionary studies. Trends in Ecology and Evolution, 3, 158–167.CrossRefPubMedGoogle Scholar
  32. Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P., & Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25, 1965–1978.CrossRefGoogle Scholar
  33. Hosmer, D. W., & Lemeshow, S. (2000). Applied logistic regression (2nd ed.). New York: John Wiley & Sons.CrossRefGoogle Scholar
  34. Ingraldi, C. (2010). Forest fragmentation and edge effects on eight sympatric lemur species in southeast Madagascar. Master's thesis, University of Calgary.Google Scholar
  35. Ingram, J. C., & Dawson, T. P. (2005). Inter-annual analysis of deforestation hotspots in Madagascar from high temporal resolution satellite observations. International Journal of Remote Sensing, 26, 1447–1461.CrossRefGoogle Scholar
  36. Irwin, M. T., Johnson, S. E., & Wright, P. C. (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.CrossRefGoogle Scholar
  37. IUCN. (2015). The IUCN red list of threatened species. Retrieved from http://www.iucnredlist.org. Accessed 6 Jan 2014.
  38. Johnson, S. E. (2002). Ecology and speciation in brown lemurs: White-collared lemurs (Eulemur albocollaris) and hybrids (Eulemur albocollaris × Eulemur fulvus rufus) in southeastern Madagascar. Unpublished Ph.D. dissertation, University of Texas at Austin, Austin, TX.Google Scholar
  39. Johnson, S. E. (2007). Evolutionary divergence in the brown lemur species complex. In L. Gould & M. L. Sauther (Eds.), Lemurs: Ecology and adaptation (pp. 187–210). New York: Springer Science+Business Media.Google Scholar
  40. Johnson, S. E., Lei, R., Martin, S. K., Irwin, M. T., & Louis, E. E. (2008). Does Eulemur cinereiceps exist? Preliminary evidence from genetics and ground surveys in southeastern Madagascar. American Journal of Primatology, 70, 372–385.CrossRefPubMedGoogle Scholar
  41. Kamilar, J. M., & Tecot, S. (2016). Anthropogenic and climatic effects on the distribution of Eulemur species: An ecological niche modeling approach. International Journal of Primatology, 37.Google Scholar
  42. Kamilar, J. M., Blanco, M., & Muldoon, K. M. (2015). Ecological niche modeling of mouse lemurs (Microcebus spp.) and its implications for their species diversity and biogeography. In S. M. Lehman, U. Radespiel, & E. Zimmerman (Eds.), Dwarf and mouse lemurs of Madagascar: Biology, behavior and conservation biogeography of the Cheirogaleidae. Cambridge: Cambridge University Press (in press)Google Scholar
  43. Kawakami, T., Butlin, R. K., Adams, M., Paull, D., & Cooper, S. J. B. (2008). Genetic analysis of a chromosomal hybrid zone in the Australian morabine grasshoppers (Vandiemenella, viatica species group). Evolution, 63, 139–152.CrossRefPubMedGoogle Scholar
  44. Key, K. H. L. (1968). The concept of stasipatric speciation. Systematic Biology, 17, 14–22.CrossRefGoogle Scholar
  45. Kozak, K. H., Graham, C. H., & Wiens, J. J. (2008). Integrating GIS-based environmental data into evolutionary biology. Trends in Ecology & Evolution, 23, 141–148.Google Scholar
  46. Lehman, S. M., & Wright, P. C. (2000). Preliminary study of the conservation status of lemur communities Betsakafandrika region of eastern Madagascar. Lemur News, 5, 23–25.Google Scholar
  47. Losos, J. B. (2008). Phylogenetic niche conservatism, phylogenetic signal and the relationship between phylogenetic relatedness and ecological similarity among species. Ecological Letters, 11, 995–1003.Google Scholar
  48. Losos, J. B., & Glor, R. E. (2003). Phylogenetic comparative methods and the geography of speciation. Trends in Ecology and Evolution, 18, 220–227.CrossRefGoogle Scholar
  49. Mallet, J. (2007). Hybrid speciation. Nature, 446, 279–283.CrossRefPubMedGoogle Scholar
  50. Markolf, M., & Kappeler, P. M. (2013). Phylogeographic analysis of the true lemurs (genus Eulemur) underlines the role of river catchments for the evolution of micro-endemism in Madagascar. Frontiers in Zoology, 10, 70.CrossRefPubMedPubMedCentralGoogle Scholar
  51. McConnell, W. J., & Kull, C. A. (2014). Deforestation in Madagascar: Debates over the island’s forest cover and challenges of measuring forest change. In I. R. Scales (Ed.), Conservation and environmental management in Madagascar (pp. 67–104). London: Routledge.Google Scholar
  52. McCormack, J. E., Zellmer, A. J., & Knowles, L. L. (2010). Does niche divergence accompany allopatric divergence in Aphelocoma jays as predicted under ecological speciation? Insights from tests with niche models. Evolution, 64, 1231–1244.PubMedGoogle Scholar
  53. Mittermeier, R. A., Konstant, W. R., Hawkins, F., Louis, E. E., Langrand, O., Ratsimbazafy, J., Rasoloarison, R., Ganzhorn, J. U., Rajaobelina, S., Tattersall, I., & Meyers, D. M. (2006). Lemurs of Madagascar (2nd ed.). Washington, DC: Conservation International.Google Scholar
  54. Mittermeier, R. A., Ganzhorn, J. U., Konstant, W. R., Glander, K., Tattersall, I., Groves, C. P., Rylands, A. B., Hapke, A., Ratsimbazafy, J., Mayor, M. I., Louis, E. E., Rumpler, Y., Schwitzer, C., & Rasoloarison, R. M. (2008). Lemur diversity in Madagascar. International Journal of Primatology, 29, 1607–1656.CrossRefGoogle Scholar
  55. Moore, W. S. (1977). An evaluation of narrow hybrid zones in vertebrates. The Quarterly Review of Biology, 52, 263–277.CrossRefGoogle Scholar
  56. Moore, W. S., & Price, J. T. (1993). Nature of selection in the northern flicker hybrid zone and its implications for speciation theory. In R. G. Harrison (Ed.), Hybrid zones and the evolutionary process (pp. 196–225). New York: Oxford University Press.Google Scholar
  57. Nosil, P. (2012). Ecological speciation. Oxford: Oxford University Press.CrossRefGoogle Scholar
  58. Overdorff, D. J. (1993). Similarities, differences, and seasonal patterns in the diets of Eulemur rubriventer and Eulemur fulvus rufus in the Ranomafana National Park, Madagascar. International Journal of Primatology, 14, 721–753.CrossRefGoogle Scholar
  59. Pastorini, J., Zaramody, A., Curtis, D. J., Nievergelt, C. M., & Mundy, N. I. (2009). Genetic analysis of hybridization and introgression between wild mongoose and brown lemurs. BMC Evolutionary Biology, 9, 32.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Pearson, R. G., Raxworthy, C. J., Nakamura, M., & Peterson, A. T. (2007). Predicting species distributions from small numbers of occurrence records: a test case using cryptic geckos in Madagascar. Journal of Biogeography, 34, 102–117.CrossRefGoogle Scholar
  61. Peterson, A. T., Soberón, J., Pearson, R. G., Anderson, R. P., Martínez-Meyer, E., Nakamura, M., & Araújo, M. B. (2011). Ecological niches and geographic distribution. Princeton: Princeton University Press.Google Scholar
  62. Phillips, S. J., Anderson, R. P., & Schapire, R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling, 190, 231–259.CrossRefGoogle Scholar
  63. R Development Core Team. (2014). R: A language and environment for statistical computing. (Version 3.03). Vienna, Austria.Google Scholar
  64. Radosavljevic, A., & Anderson, R. P. (2014). Making better Maxent models of species distributions: complexity, overfitting and evaluation. Journal of Biogeography, 41, 629–643.Google Scholar
  65. Rakotondranary, S. J., & Ganzhorn, J. U. (2011). Habitat separation of sympatric Microcebus spp. in the dry spiny forest of south-eastern Madagascar. Folia Primatologica, 82, 212–223.CrossRefGoogle Scholar
  66. Schluter, D. (2001). Ecology and the origin of species. Trends in Ecology and Evolution, 18, 372–380.CrossRefGoogle Scholar
  67. Schluter, D. (2009). Evidence for ecological speciation and its alternative. Science, 323, 737–741.CrossRefPubMedGoogle Scholar
  68. Schwitzer, C., Mittermeier, R. A., Johnson, S. E., Donati, G., Irwin, M., Peacock, H., Ratsimbazafy, J., Razafindramanana, J., Louis, E. E., Jr., Chikhi, L., Colquhoun, I. C., Tinsman, J., Dolch, R., LaFleur, M., Nash, S., Patel, E., Randrianambinina, B., Rasolofoharivelo, T., & Wright, P. C. (2014). Averting lemur extinctions amid Madagascar's political crisis. Science, 343, 842–843.CrossRefPubMedGoogle Scholar
  69. Swenson, N. G. (2006). Gis-based niche models reveal unifying climatic mechanisms that maintain the location of avian hybrid zones in a North American suture zone. Journal of Evolutionary Biology, 19, 717–725.Google Scholar
  70. Swenson, N. G. (2008). The past and future influence of geographic information systems on hybrid zone, phylogeographic and speciation research. Journal of Evolutionary Biology, 21, 421–434.Google Scholar
  71. Syfert, M. M., Smith, M. J., & Coomes, D. A. (2013). The effects of sampling bias and model complexity on the predictive performance of MaxEnt species distribution models. PLoS ONE, 8, e55158.CrossRefPubMedPubMedCentralGoogle Scholar
  72. Tattersall, I., Sussman, R., & Sussman, R. (1998). 'Little brown lemurs' of northern Madagascar. Folia Primatologica, 69(Supplement 1), 379–388.CrossRefGoogle Scholar
  73. USGS. (2012). Global 30 Arc-Second Elevation (GTOPO30). Retrieved from https://lta.cr.usgs.gov/GTOPO30. Accessed 8 Nov 2014.
  74. Warren, D. L. (2012). In defense of ‘niche modeling.’. Trends in Ecology & Evolution, 27, 497–500.CrossRefGoogle Scholar
  75. Warren, D. L., Glor, R. E., & Turelli, M. (2008). Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution, 62, 2868–2883.CrossRefPubMedGoogle Scholar
  76. Warren, D. L., Glor, R. E., & Turelli, M. (2010). ENMTools: a toolbox for comparative studies of environmental niche models. Ecography, 33, 607–611.CrossRefGoogle Scholar
  77. Wiens, J. J. (2004). Speciation and ecology revisited: phylogenetic niche conservatism and the origin of species. Evolution, 58, 193–197.CrossRefPubMedGoogle Scholar
  78. Wyner, Y. M., Johnson, S. E., Stumpf, R. M., & DeSalle, R. (2002). Genetic assessment of a white-collared × red-fronted lemur hybrid zone at Andringitra, Madagascar. American Journal of Primatology, 57, 51–66.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Steig E. Johnson
    • 1
  • Kira E. Delmore
    • 2
  • Kerry A. Brown
    • 3
  • Tracy M. Wyman
    • 1
  • Edward E. LouisJr.
    • 4
  1. 1.Department of Anthropology and ArchaeologyUniversity of CalgaryCalgaryCanada
  2. 2.Department of ZoologyUniversity of British ColumbiaVancouverCanada
  3. 3.School of Geography, Geology and the Environment, Centre for Earth and Environmental Science Research (CEESR)Kingston UniversitySurreyUK
  4. 4.Center for Conservation and ResearchOmaha’s Henry Doorly Zoo and AquariumOmahaUSA

Personalised recommendations