Hostname: page-component-848d4c4894-xfwgj Total loading time: 0 Render date: 2024-06-22T17:15:42.888Z Has data issue: false hasContentIssue false

Ecological correlates of ghost lineages in ruminants

Published online by Cambridge University Press:  08 April 2016

Juan L. Cantalapiedra
Departamento de Paleobiología, Museo Nacional de Ciencias Naturales, UCM-CSIC, Pinar 25, 28006 Madrid, Spain. E-mail:
Manuel Hernández Fernández
Departamento de Paleontología, Facultad de Ciencias Geológicas, Universidad Complutense de Madrid y Departamento de Cambio Medioambiental, Instituto de Geociencias, Consejo Superior de Investigaciones Científicas, José Antonio Novais 2, 28040 Madrid, Spain
Gema M. Alcalde
Departamento de Paleobiología, Museo Nacional de Ciencias Naturales, UCM-CSIC, Pinar 25, 28006 Madrid, Spain. E-mail:
Beatriz Azanza
Departamento de Ciencias de la Tierra, Facultad de Ciencias and Instituto de Ciencias de Aragón, Universidad de Zaragoza, Pedro Cerbuna 12, 50009 Zaragoza, Spain
Daniel DeMiguel
Departament de Faunes del Neogen i Quaternari, Institut Català de Paleontologia, Edifici ICP, Universitat Autònoma de Barcelona, 08193 Cerdanyola del Vallès, Spain
Jorge Morales
Departamento de Paleobiología, Museo Nacional de Ciencias Naturales, UCM-CSIC, Pinar 25, 28006 Madrid, Spain. E-mail:


Integration between phylogenetic systematics and paleontological data has proved to be an effective method for identifying periods that lack fossil evidence in the evolutionary history of clades. In this study we aim to analyze whether there is any correlation between various ecomorphological variables and the duration of these underrepresented portions of lineages, which we call ghost lineages for simplicity, in ruminants. Analyses within phylogenetic (Generalized Estimating Equations) and non-phylogenetic (ANOVAs and Pearson correlations) frameworks were performed on the whole phylogeny of this suborder of Cetartiodactyla (Mammalia). This is the first time ghost lineages are focused in this way. To test the robustness of our data, we compared the magnitude of ghost lineages among different continents and among phylogenies pruned at different ages (4, 8, 12, 16, and 20 Ma). Differences in mean ghost lineage were not significantly related to either geographic or temporal factors. Our results indicate that the proportion of the known fossil record in ruminants appears to be influenced by the preservation potential of the bone remains in different environments. Furthermore, large geographical ranges of species increase the likelihood of preservation.

Copyright © The Paleontological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)


Literature Cited

Adkins, R. M., Gelke, E. L., Rowe, D., and Honeycutt, R. L. 2001. Molecular phylogeny and divergence time estimates for major rodent groups: evidence from multiple genes. Molecular Biology and Evolution 18:777791.Google Scholar
Alberdi, M., Alonso, M., Azanza, B., Hoyos, M., and Morales, J. 2001. Vertebrate taphonomy in circum-lake environments: three cases in the Guadalix-Baza Basin (Granada, Spain). Palaeogeography, Palaeoclimatology, Palaeoecology 161:126.Google Scholar
Alcalde, G., Alberdi, M. T., Azanza, B., and Hernández Fernández, M. 2006. Inferencias ambientales a partir del estudio de la locomoción en comunidades de ruminantes. Pp. 1315 in Fernández Martínez, E., ed. XXII Jornadas de las Sociedad Española de Paleontología. León University, León.Google Scholar
Alroy, J., Marshall, C. R., Bambach, R. K., Bezusko, K., Foote, M., Fürsich, F. T., Hansen, T. A., Holland, S. M., Ivany, L. C., Jablonski, D., Jacobs, D. K., Jones, D. C., Kosnik, M. A., Lidgard, S., Low, S., Miller, A. I., Novack-Gottshall, P. M., Olszewski, T. D., Patzkowsky, M. E., Raup, D. M., Roy, K., Sepkoski, J. J. Jr, Sommes, M. G., Wagner, P. J., and Webber, A. 2001. Effects of sampling standardization on estimates of Phanerozoic marine diversification. Proceedings of the National Academy of Sciences U.S.A. 98:62616266.Google Scholar
Answell, W. F. H. 1971. Order Artiodactyla. Pp. 184 in Meester, J.and Setzer, H. W., eds. The mammals of Africa: an identification manual. Smithsonian Institution Press, Washington, D.C.Google Scholar
Behrensmeyer, A. K. 1976. Fossil assemblages in relation to sedimentary environments in the East Rudolf succession. Pp. 383401 in Coppens, Y., Howell, F. C., Isaac, G. L., and Leakey, E. F., eds. Earliest man and environment in the Lake Rudolf Basin: stratigraphy, paleoecology, and evolution. University of Chicago Press, Chicago.Google Scholar
Benton, M. J., Wills, M. A., and Hitchin, R. 2000. Quality of the fossil record through time. Nature 403:534537.Google Scholar
Bininda-Emonds, O. R. P., Cardillo, M., Jones, K. E., MacPhee, R. D. E., Beck, R. M. D., Grenyer, R., Price, S. A., Vos, R. A., Gittleman, J. L., and Purvis, A. 2007. The delayed rise of present-day mammals. Nature 446:507512.Google Scholar
Brown, J. H. 1984. On the relationship between abundance and distribution of species. American Naturalist 124:255279.Google Scholar
Brown, J. H. 1995. Macroecology. University of Chicago Press, Chicago.Google Scholar
Brown, J. H., and Maurer, B. A. 1987. Evolution of species assemblages: effects of energetic constraints and species dynamics on the diversification of the North American avifauna. American Naturalist 130:117.Google Scholar
Brown, J. H., and Maurer, B. A. 1989. Macroecology: the division of food and space among species on continents. Science 243:11451150.Google Scholar
Cavin, L., and Forey, P. L. 2007. Using ghost lineages to identify diversification events in the fossil record. Biology Letters 3:201204.Google Scholar
Cerling, T. E., Wang, Y., and Quade, J. 1993. Expansion of C4 ecosystems as indicator of global ecological change in the late Miocene. Nature 361:344345.Google Scholar
Corbet, G. B. 1978. The mammals of the Palaearctic region: a taxonomic review. Cornell University Press, Ithaca, N.Y.Google Scholar
Corbet, G. B., and Hill, J. E. 1992. The mammals of the Indomalayan Region: a systematic review. Oxford University Press, Oxford.Google Scholar
Crampton, J. S., Beu, A. G., Cooper, R. A., Jones, C. M., Marshall, B., and Maxwell, P. A. 2003. Estimating the rock volume bias in paleobiodiversity studies. Science 301:358360.Google Scholar
DeGusta, D., and Vrba, E. S. 2003. A method for inferring paleohabitats from the functional morphology of bovid astragali. Journal of Archaeological Science 30:10091022.Google Scholar
DeMiguel, D., Fortelius, M., Azanza, B., and Morales, J. 2008. Ancestral feeding state of ruminants reconsidered: earliest grazing adaptation claims a mixed condition for Cervidae. BMC Evolutionary Biology 8(13). doi:10.1186/1471-2148-8-13Google Scholar
Eisenberg, H. J. F. 1989. Mammals of the Neotropics, Vol. 1. The northern Neotropics. University of Chicago Press, Chicago.Google Scholar
Eisenberg, H. J. F.and Redford, K. 2000. Mammals of the Neotropics, Vol. 3. The central Neotropics. University of Chicago Press, Chicago.Google Scholar
Gaston, K. J., and Blackburn, T. M. 1996a. Conservation implications of geographic range size–body size relationships. Conservation Biology 10:638646.Google Scholar
Gaston, K. J., and Blackburn, T. M. 1996b. Range size–body size relationships: evidence of scale dependence. Oikos 75:479485.Google Scholar
Glazier, D. S. 1980. Ecological shifts and the evolution of geographically restricted species of North American Peromyscus (mice). Journal of Biogeography 7:6383.Google Scholar
Grubb, P. 1993. Order Artiodactyla. Pp. 377414 in Wilson, D. E.and Reeder, D. M., eds. Mammal Species of the World: a taxonomic and geographic reference. Smithsonian Institution Press, Washington, D.C.Google Scholar
Hall, E. R. 1981. The mammals of North America. Wiley, New York.Google Scholar
Hartenberger, J. 1998. Description de la radiation des Rodentia (Mammalia) du Paléocène supérieur au Miocène; incidences phylogénétiques. Comptes Rendus de l'Académie des Sciences 326:439444.Google Scholar
Hernandez Fernández, M. 2001. Bioclimatic discriminant capacity of terrestrial mammal faunas. Global Ecology and Biogeography 10:189204.Google Scholar
Hernández Fernández, M., and Vrba, E. S. 2005a. A complete estimate of the phylogenetic relationships in Ruminantia: a dated species-level supertree of the extant ruminants. Biological Reviews 80:269302.Google Scholar
Hernández Fernández, M., and Vrba, E. S. 2005b. Macroevolutionary processes and biomic specialization: testing the resource-use hypothesis. Evolutionary Ecology 19:199219.Google Scholar
Hernández Fernández, M., and Vrba, E. S. 2005c. Rapoport effect and biomic specialization in African mammals: revisiting the climatic variability hypothesis. Journal of Biogeography 32:903918.Google Scholar
Hernández Fernández, M., and Vrba, E. S. 2006. Plio-Pleistocene climatic change in the Turkana Basin (East Africa): evidence from large mammal faunas. Journal of Human Evolution 50:595626.Google Scholar
Hernández Fernández, M., Alcalde, G. M., DeMiguel, D., García-Yelo, B., and Azanza, B. 2009. Functional groups in ruminants as environmental proxies. Journal of Vertebrate Paleontology 29(Suppl. to No. 3):113.Google Scholar
Huchon, D., Madsen, O., Sibbald, M. J., Ament, K., Stanhope, M. J., Catzeflis, F., de Jong, W. W., and Douzery, E. J. 2002. Rodent phylogeny and a timescale for the evolution of glires: evidence from an extensive taxon sampling using three nuclear genes. Molecular Biology and Evolution 19: 1053–65.Google Scholar
Jackson, J. B. C. 1974. Biogeographic consequences of eurytopy and stenotopy among marine bivalves and their evolutionary significance. American Naturalist 108:541560.Google Scholar
Johnson, W. E., Eizirik, E., Pecon-Slattery, J., Murphy, W. J., Antunes, A., Teeling, E., and O'Brien, S. J. 2006. The late radiation of modern Felidae: a genetic assessment. Science 311:7377.Google Scholar
Kerbis, J. C., Wrangham, R. W., Carter, M. L., and Hauser, H. D. 1993. A contribution to tropical rain-forest taphonomy: retrieval and documentation of chimpanzee remains from Kibale Forest, Uganda. Journal of Human Evolution 25:485514.Google Scholar
Kingdon, J. 1997. The Kingdon field guide to African mammals. Academic Press, London.Google Scholar
Köhler, M. 1993. Skeleton and habitat of Recent and fossil ruminants. Friedrich Pfeil, Munich.Google Scholar
Lane, A., Janis, C. M., and Sepkoski, J. J. Jr. 2005. Estimating paleodiversities: a test of the taxic and phylogenetic methods. Paleobiology 31:2134.Google Scholar
Liu, F. R., Miyamoto, M. M., Freire, N. P., Ong, P. Q., Tennant, M. R., Young, T. S., and Gugel, K. F. 2001. Molecular and morphological supertrees for eutherian (placental) mammals. Science 291:17861789.Google Scholar
Lyman, R. L. 1994. Vertebrate taphonomy. Cambridge University Press, Cambridge.Google Scholar
MacArthur, R. H. 1972. Geographical ecology: patterns in the distribution of species. Harper and Row, New York.Google Scholar
Maddison, W., and Maddison, D. 2007. Mesquite: a modular system for evolutionary analysis, Version 2.0. http://mesquiteproject.orgGoogle Scholar
Mayr, E. 1963. Animal species and evolution. Belknap Press of Harvard University Press, Cambridge.Google Scholar
McKenna, M. C., and Bell, S. K. 1997. Classification of mammals above the species level. Columbia University Press, New York.Google Scholar
Mitchell-Jones, A. J., Amori, G., Bogdanowic, W., Krystufek, B., and Reijnders, P. 1999. The atlas of European mammals. Poyser, London.Google Scholar
Moreno Bofarull, A., Arias Royo, A., Hernández Fernández, M., Ortiz-Jaurequizar, E., and Morales, J. 2008. Influence of continental history on the ecological specialization and macroevolutionary processes in the mammalian assemblage of South America: Differences between small and large mammals. BMC Evolutionary Biology 8(97). doi:10.1186/1471-2148-8-97Google Scholar
Norell, M. A. 1992. Taxic origin and temporal diversity: the effect of phylogeny. Pp. 89118 in Novacek, M. J.and Wheeler, Q. D., eds. Extinction and phylogeny. Columbia University Press, New York.Google Scholar
Norell, M. A. 1993. Tree-based approaches to understanding history: comments on ranks, rules, and the quality of fossil record. American Journal of Science 293-A:407417.Google Scholar
Norell, M. A. 1996. Ghost taxa, ancestors, and assumptions: a comment on Wagner. Paleobiology 22:453455.Google Scholar
Norell, M. A., and Novacek, M. J. 1992a. The fossil record and evolution: comparing cladistic and paleontological evidence for vertebrate history. Science 255:16901693.Google Scholar
Norell, M. A., and Novacek, M. J. 1992b. Congruence between superpositional and phylogenetic patterns: comparing cladistic patterns with fossil record. Cladistics 8:319337.Google Scholar
O'Keefe, F. R., and Sander, P. M. 1999. Paleontological paradigms and inferences of phylogenetic pattern: a case study. Paleobiology 25:518533.Google Scholar
Ortolani, A. 1999. Spots, stripes, tail tips and dark eyes: predicting the function of carnivore colour patterns using the comparative method. Biological Journal of the Linnean Society 67:433476.Google Scholar
Ortolani, A., and Caro, T. M. 1996. The adaptive significance of color patterns in carnivores: phylogenetic tests of classic hypotheses. Pp. 132188 in Gittleman, J. L., ed. Carnivore behavior, ecology, and evolution. Cornell University Press, Ithaca, N.Y.Google Scholar
Paradis, E. 2006. Analysis of phylogenetics and evolution with R. Springer, New York.Google Scholar
Paradis, E., and Claude, J. 2002. Analysis of comparative data using generalized estimating equations. Journal of Theoretical Biology 218:175185.Google Scholar
Paul, C. R. C. 1982. The adequacy of the fossil record. Pp. 75117 in Donovan, S.and Paul, C. R. C., eds. The adequacy of the fossil record. Wiley, Chichester, U.K.Google Scholar
Pol, D., and Norell, M. A. 2006. Uncertainty in the age of fossils and the stratigraphic fit to phylogenies. Systematic Biology 55:512521.Google Scholar
Polonio, I., and López Martínez, N. 2000. Análisis tafonómico de los yacimientos de Somosaguas (Mioceno Medio, Madrid). Coloquios de Paleontología 51:235266.Google Scholar
Potts, R., and Behrensmeyer, A. K. 1992. Late Cenozoic terrestrial ecosystems. Pp. 419541 in Behrensmeyer, A. K., Damuth, J. D., DiMichele, W. A., Sues, H. D., Potts, R., and Wing, S. L., eds. Terrestrial ecosystems trough time. University of Chicago Press, Chicago.Google Scholar
Redford, K., and Eisenberg, H. J. F. 1992. Mammals of the Neotropics, Vol. 2. The Southern Cone. University of Chicago Press, Chicago.Google Scholar
Ruta, M., and Benton, M. J. 2008. Calibrated diversity, tree topology and the mother of mass extinctions: the lesson of temnospondyls. Paleobiology 51:12611288.Google Scholar
Sidor, C. A., and Hopson, J. A. 1998. Ghost lineages and “mammalness”: assessing the temporal pattern of character acquisition in the Synapsida. Paleobiology 24:254273.Google Scholar
Smith, A. B. 1994. Systematics and the fossil record. Blackwell Scientific, Oxford.Google Scholar
Smith, J. M., and Savage, R. J. G. 1956. Some locomotory adaptations in mammals. Zoological Journal of the Linnean Society 42:603622.Google Scholar
Teeling, E. C., Springer, M. S., Madsen, O., Bates, P., O'Brien, S. J., and Murphy, W. J. 2005. A molecular phylogeny for bats illuminates biogeography and the fossil record. Science 307:580584.Google Scholar
Thompson, K., Hodgson, J. G., and Gaston, K. J. 1998. Abundance-range size relationships in the herbaceous flora of central England. Journal of Ecology 86:439448.Google Scholar
Vrba, E. S. 1987. Ecology in relation to speciation rates: some case histories of Miocene-Recent mammal clades. Evolutionary Ecology 1:283300.Google Scholar
Vrba, E. S., and Schaller, G. B. 2000. Introduction. Pp. 18 in Vrba, E. S.and Schaller, G. B., eds. Antelopes, deer, and relatives: fossil record, behavioral ecology, systematics and conservation. Yale University Press, New Haven, Conn.Google Scholar
Wagner, P. J. 1995. Stratigraphic tests of cladistic hypotheses. Paleobiology 21:153178.Google Scholar
Wagner, P. J. 2000a. Phylogenetic analyses and the fossil record: tests and inferences, hypotheses and models. In Erwin, D. H.and Wing, S. L., eds. Deep time: Paleobiology's perspective. Paleobiology 26(Suppl. to No. 4):341371.Google Scholar
Wagner, P. J. 2000b. The quality of the fossil record and the accuracy of phylogenetic inferences about sampling diversity. Systematic Biology 49:6586.Google Scholar
Walter, H. 1970. Vegetationszonen und Klima. Eugen Ulmer, Stuttgart.Google Scholar
Weishampel, D. B. 1996. Fossils, phylogeny, and discovery: a cladistic study of history of tree topologies and ghost lineages durations. Journal of Vertebrate Paleontology 16:191197.Google Scholar
Wills, M. A. 2002. The tree of life and the rock of ages: are we getting better at estimating phylogeny? BioEssays 24:203207.Google Scholar
Worthy, T. H., Tennyson, A. J., Archer, M., Musser, A. M., Hand, S. J., Jones, C., Douglas, B. J., McNamara, J. A., and Beck, R. M. 2006. Miocene mammal reveals a Mesozoic ghost lineage on insular New Zealand, southwest Pacific. Proceedings of the National Academy of Sciences U.S.A. 103:1941919423.Google Scholar