Hostname: page-component-745bb68f8f-lrblm Total loading time: 0 Render date: 2025-01-12T23:23:35.574Z Has data issue: false hasContentIssue false
  • English
  • Français

Diversity patterns of nonmammalian cynodonts (Synapsida, Therapsida) and the impact of taxonomic practice and research history on diversity estimates

Published online by Cambridge University Press:  05 December 2018

Marcus Lukic-Walther ,
Neil Brocklehurst ,
Christian F. Kammerer  and
Jörg Fröbisch
Marcus Lukic-Walther
Affiliation:
Erst-Reuter-Gesellschaft, Freie Universität Berlin, Kaiserswerther Strasse 16–18, 14195 Berlin, Germany. E-mail: [email protected]
Neil Brocklehurst
Affiliation:
Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstraße 43, D-10115 Berlin, Germany.
Christian F. Kammerer
Affiliation:
North Carolina Museum of Natural Sciences, 11 West Jones Street, Raleigh, North Carolina 27601-1029, U.S.A. E-mail: [email protected]
Jörg Fröbisch
Affiliation:
Museum für Naturkunde, Leibniz-Institut für Evolutions- und Biodiversitätsforschung, Invalidenstraße 43, and Institut für Biologie, Humboldt Universität zu Berlin, Invalidenstraße 42, D-10115 Berlin, Germany. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Nonmammalian cynodonts represent a speciose and ecologically diverse group with a fossil record stretching from the late Permian until the Cretaceous. Because of their role as major components of Triassic terrestrial ecosystems and as the direct ancestors of mammals, cynodonts are an important group for understanding Mesozoic tetrapod diversity. We examine patterns of nonmammalian cynodont species richness and the quality of their fossil record. A supertree of cynodonts is constructed from recently published trees and time calibrated using a Bayesian approach. While this approach pushes the root of Cynodontia back to the earliest Guadalupian, the origins of Cynognathia and Probainognathia are close to their first appearance in the fossil record. Taxic, subsampled, and phylogenetic diversity estimates support a major cynodont radiation following the end-Permian mass extinction, but conflicting signals are observed at the end of the Triassic. The taxic diversity estimate shows high diversity in the Rhaetian and a drop across the Triassic/Jurassic boundary, while the phylogenetic diversity indicates an earlier extinction between the Norian and Rhaetian. The difference is attributed to the prevalence of taxa based solely on teeth in the Rhaetian, which are not included in the phylogenetic diversity estimate. Examining the completeness of cynodont specimens through geological time does not support a decrease in preservation potential; although the median completeness score decreases in the Late Triassic, the range of values remains consistent. Instead, the poor completeness scores are attributed to a shift in sampling and taxonomic practices: an increased prevalence in microvertebrate sampling and the naming of fragmentary material.

Type
Articles
Information
Paleobiology , Volume 45 , Issue 1 , February 2019 , pp. 56 - 69
Copyright
Copyright © 2018 The Paleontological Society. All rights reserved 

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.)

Footnotes

*

Present address: Department of Earth Sciences, University of Oxford, South Parks Road, Oxford, UK, OX1 3AN. E-mail: [email protected]

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.6jk8416

References

Literature Cited

Abdala, F., and Ribeiro, A. M.. 2010. Distribution and diversity patterns of Triassic cynodonts (Therapsida, Cynodontia) in Gondwana. Palaeogeography, Palaeoclimatology, Palaeoecology 286:202–217.Google Scholar
Abdala, F., Mocke, H. S., and Hancox, P. J.. 2007. Lower Triassic postcanine teeth with allotherian-like crowns. South African Journal of Science 103:245–247.Google Scholar
Abdala, F., Rubidge, B. S., and van den Heever, J.. 2008. The oldest therocephalians (Therapsida: Eutheriodontia) and the early diversification of Therapsida. Palaeontology 51:1011–1024.Google Scholar
Abdala, F., Jashashvili, T., Rubidge, B. S., and van den Heever, J.. 2014. New material of Microgomphodon oligocynus (Eutherapsida, Therocephalia) and the taxonomy of southern African Bauriidae. Pp. 209–231 in Kammerer, C. F., Angielczyk, K. D., and Fröbisch, J., eds. Early evolutionary history of the Synapsida. Springer, Dordrecht, Netherlands.Google Scholar
Alroy, J. 2010. Geographical, environmental and intrinsic biotic controls on Phanerozoic marine diversification. Palaeontology 53:1121–1235.Google Scholar
Alroy, J. n.d. Shareholder quorum subsampling R function. https://bio.mq.edu.au/~jalroy/SQS.html, accessed July 2018.Google Scholar
Barrett, P. M., McGowan, A. J., and Page, V.. 2009. Dinosaur diversity and the rock record. Proceedings of the Royal Society of London B 276:2667–2674.Google Scholar
Baum, B. R. 1992. Combining trees as a way of combining data sets for phylogenetic inference, and the desirability of combining gene trees. Taxon 41:1–10.Google Scholar
Bell, M., Upchurch, P., Mannion, P. D., and Lloyd, G. T.. 2013. Using the character completeness metric to examine completeness of Mesozoic dinosaurs: a Maastrichtian high and a paleoequatorial low. Journal of Vertebrate Palaeontology Program and Abstracts 84.Google Scholar
Benson, R., Butler, R. J., Lindgren, J., and Smith, A. S.. 2011. Palaeodiversity of Mesozoic marine reptiles: mass extinctions and temporal heterogeneity in geologic megabiases affecting vertebrates. Proceedings of the Royal Society of London B 277:829–234.Google Scholar
Benton, M. J., and Clark, J. M.. 1988. Archosaur phylogeny and the relationships of the Crocodylia. Pp. 295–338 in Benton, M. J., ed. The phylogeny and classification of the tetrapods, Vol. 1. Clarendon, Oxford.Google Scholar
Benton, M. J., Ruta, M., Dunhill, A. M., and Sakamoto, M.. 2013. The first half of tetrapod evolution, sampling proxies, and fossil record quality. Palaeogeography, Palaeoclimatology, Palaeoecology 372:18–41.Google Scholar
Botha, J., Abdala, F., and Smith, R.. 2007. The oldest cynodont: new clues on the origin and early diversification of the Cynodontia. Zoological Journal of the Linnean Society 149:477–492.Google Scholar
Brocklehurst, N. 2015. A simulation-based examination of residual diversity estimates as a method of correcting for sampling bias. Palaeontologia Electronica 18(3):1–15.Google Scholar
Brocklehurst, N., and Fröbisch, J.. 2014. Current and historical perspectives on the completeness of the fossil record of pelycosaurian-grade synapsids. Palaeogeography, Palaeoclimatology, Palaeoecology 399:114–126.Google Scholar
Brocklehurst, N., Upchurch, P., Mannion, P. D., and O'Connor, J.. 2012. The completeness of the fossil record of Mesozoic birds: implications for early avian evolution. PLoS ONE 7:e39056.Google Scholar
Brocklehurst, N., Kammerer, C. F., and Fröbisch, J.. 2013. The early evolution of synapsids and the influence of sampling on their fossil record. Paleobiology 39:470–490.Google Scholar
Brocklehurst, N., Ruta, M., Müller, J., and Fröbisch, J.. 2015. Elevated extinction rates as a trigger for diversification rate shifts. Scientific Reports 5:17104.Google Scholar
Chao, A., and Jost, L.. 2012. Coverage-based rarefaction and extrapolation: standardising samples by completeness rather than size. Ecology 93: 2533–2547.Google Scholar
Clifford, P., Richarson, S., and Hemon, D.. 1989. Assessing the significance of the correlation between two spatial processes. Biometrics 45:123–134.Google Scholar
Close, R. A., Friedman, M., Lloyd, G. T., and Benson, R.. 2015. Evidence for a mid-Jurassic adaptive radiation of mammals. Current Biology 25:2137–2142.Google Scholar
Close, R. A., Evers, S. W., Alroy, J., and Butler, R. J.. 2018. How should we estimate diversity in the fossil record? Testing richness estimators using sampling-standardised discovery curves. Methods in Ecology and Evolution 9:1386–1400.Google Scholar
Dean, C. D., Mannion, P. D, and Butler, R. J.. 2016. Preservational bias controls the fossil record of pterosaurs. Palaeontology 59:225–247.Google Scholar
Deenen, M. H., Ruhl, M., Bonis, N. R., Krijgsman, W., Kuerschner, W. M., Reitsma, M., and Van Bergen, M. J.. 2010. A new chronology for the end-Triassic mass extinction. Earth and Planetary Scientific Letters 291:112–125.Google Scholar
de Oliveira, T. V., Soares, M. B., and Schultz, C. L.. 2010. Trucidocynodon riograndensis gen. nov. et sp. Nov. (Eucynodontia), a new cynodont from the Brazilian Upper Triassic (Santa Maria Formation). Zootaxa 2382:1–71.Google Scholar
Dos Reis, M., Donoghue, P. C. J., and Yang, Z.. 2016. Bayesian molecular clock dating of species divergences in the genomics era. Nature Reviews Genetics 17:71–80.Google Scholar
Felsenstein, J. 1985. Phylogenies and the comparative method. American Naturalist 125:1–15.Google Scholar
Fröbisch, J. 2008. Global taxonomic diversity of anomodonts (Tetrapoda, Therapsida) and the terrestrial rock record across the Permian–Triassic boundary. PLoS ONE 3:e3733.Google Scholar
Fröbisch, J. 2014. Synapsid diversity and the rock record in the Permian–Triassic Beaufort Group (Karoo Supergroup), South Africa. Pp. 305–319 in Kammerer, C. F., Angielczyk, K. D., and Fröbisch, J., eds. Early evolutionary history of the Synapsida. Springer, Dordrecht, Netherlands.Google Scholar
Gaetano, L. C., Mocke, K., Abdala, F., and Hancox, P. J.. 2012. Complex multicusped postcanine teeth from the lower Triassic of South Africa. Journal of Vertebrate Paleontology 32:1411–1420.Google Scholar
Hallam, A. 1990. The end-Triassic mass extinction event. Geological Society of America Special Paper 247:577–584.Google Scholar
Heckert, A. B. 2004. Late Triassic microvertebrates from the lower Chinle group (Otischalkian-Adamanian:Carnian), southwestern USA. Bulletin of the New Mexico Museum of Natural History and Science 27:1–170.Google Scholar
Hedman, M. M. 2010. Constraints on clade ages from fossil outgroups. Paleobiology 36:16–31.Google Scholar
Huttenlocker, A.K. 2014. Body size reductions in nonmammalian eutheriodont therapsids (Synapsida) during the end-Permian mass extinction. PLoS ONE 9:e87553.Google Scholar
Huttenlocker, A. K., and Smith, R. M.. 2017. New whaitsioids (Therapsida: Therocephalia) from the Teekloof Formation of South Africa and therocephalian diversity during the end-Guadalupian extinction. PeerJ 5:e3868.Google Scholar
Jones, M. E. H., Anderson, C. L., Hipsley, C. A., Müller, J., Evans, S. E., and Schoch, R. R.. 2013. Integration of molecules and new fossils supports a Triassic origin of Lepidosauria (lizards, snakes and tuatara). BMC Evolutionary Biology 13:208.Google Scholar
Kammerer, C. F. 2016. A new taxon of cynodont from the Tropidstoma Assemblage Zone (Upper Permian) of South Africa, and the early evolution of Cynodontia. Papers in Paleontology 2:387–397.Google Scholar
Kangas, A. T., Evans, A. R., Thesleff, I., and Jukka, J.. 2004. Nonindependence of mammalian dental characters. Nature 432:211–214.Google Scholar
Kemp, T. S. 2005. The origin and evolution of mammals. Oxford University Press, Oxford.Google Scholar
Kielan-Jaworowska, Z., Cifelli, R. L., and Luo, Z.-X.. 2004. Mammals from the age of dinosaurs: origins, evolution and structure. Columbia University Press, New York.Google Scholar
Kunin, W. E. 2008. On comparative analyses involving non-heritable traits: why half a load is sometimes worse than none. Evolutionary Ecology Research 10:787–796.Google Scholar
Lane, A., Janis, C. M., and Sepkoski, J. J. Jr. 2005. Estimating palaeodiversities: a test of the taxic and phylogenetic methods. Paleobiology 31:21–34.Google Scholar
Liu, J., Rubidge, B. S., and Li, J.. 2009. New basal synapsid supports Laurasian origin for therapsids. Acta Palaeontologica Polonica 54:393–400.Google Scholar
Lloyd, G. T., Bapst, D. W., Friedman, M., and Davis, K. E., K.E. 2016. Probabilistic divergence time estimation without branch lengths: dating the origins of dinosaurs, avian flight and crown birds. Biology Letters 12:20160609.Google Scholar
Lopatin, A. V., and Agadjanian, A. K.. 2007. A tritylodont (Tritylodontidae, Synapsida) from the Mesozoic of Yakutia. Doklady Biological Sciences 419:107–110.Google Scholar
Luo, Z.-X. 2007. Transformation and diversification in early mammal evolution. Nature 450:1011–1019.Google Scholar
Mannion, P. D., and Upchurch, P.. 2010. Completeness metrics and the quality of the sauropodomorph fossil record through geological and historical time. Paleobiology 36:283–302.Google Scholar
Mannion, P. D., Upchurch, P., Carrano, W. T., and Barrett, P. M.. 2011. Testing the effect of the rock record on diversity: a multidisciplinary approach to elucidating the generic richness of sauropodomorph dinosaurs through time. Biological Reviews 86:157–181.Google Scholar
Martinelli, A. G., and Rougier, G. W.. 2007. On Chaliminia musteloides (Eucynodontia, Trithelodontidae) from the Late Triassic of Argentina, and a phylogeny of Ictidosauria. Journal of Vertebrae Paleontology 17:442–460.Google Scholar
Martinelli, A. G., Eltink, E., Da-Rosa, A. A. S., and Langer, M. C.. 2017a. A new cynodont from the Santa Maria Formation, south Brazil, improves Late Triassic probainognathian diversity. Papers in Palaeontology 3:401–423.Google Scholar
Martinelli, A. G., Kammerer, C. F., Melo, T. P., Paes Neto, P. D., Ribeiro, A. M., Da-Rosa, A. A. S., Schultz, C. L., and Soares, M. B.. 2017b. The African cynodont Aleodon (Cynodontia, Probainognathia) in the Triassic of southern Brazil and its biostratigraphic significance. PLoS ONE 12:e0177948.Google Scholar
Martinelli, A. G., Soares, M. B., de Oliveira, T. V., Rodrigues, P. G., and Schultz, C. L.. 2017c. The Triassic eucynodont Candelariodon barberenai revisited and the early diversity of stem prozostrodontians. Acta Palaeontologia Polonica 62:527–542.Google Scholar
McKinney, M. L. 1990. Classifying and analysing evolutionary trends. Pp. 28–58 in McNamara, K. J., ed. Evolutionary trends. Belhaven, London.Google Scholar
Melo, T., Martinelli, A. G., Soares, M. B.. 2017. A new gomphodont cynodont (Traversodontidae) from the Middle–Late Triassic Dinodontosaurus Assemblage Zone of the Santa Maria Supersequence, Brazil. Palaeontology 60:571–582.Google Scholar
Newham, E., Benson, R., and Upchurch, P.. 2014. Mesozoic mammaliaform diversity: the effect of sampling correction on reconstructions of evolutionary dynamics. Palaeogeography, Palaeoclimatology, Palaeoecology 412:32–44.Google Scholar
Pálfy, J., Mortensen, J. K., Carter, E. S., Smith, P. L., Friedman, R. M., and Tipper, H. W.. 2000. Timing the end-Triassic mass extinction: first on land, then in the sea? Geology 28:39–42.Google Scholar
Panciroli, E., Walsh, S., Fraser, N. C., Brusatte, S. L., and Corfe, I.. 2017. A reassessment of the postcanine dentition and systematics of the tritylodontid Stereognathus (Cynodontia, Tritylodontidae, Mammaliamorpha), from the Middle Jurassic of the United Kingdom. Journal of Vertebrate Paleontology 37:e1351448.Google Scholar
Paradis, E., Claude, J., and Strimmer, K.. 2004. APE: analyses of phylogenetics and evolution in R language. Bioinformatics 20:289–290.Google Scholar
Ragan, M. A. 1992. Phylogentic inference based on matrix representation of trees. Molecular Phylogenetics and Evolution 1:53–58.Google Scholar
R Core Team. 2016. R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Rheindt, F. E., Grafe, T. U., and Abouheif, E.. 2004. Rapidly evolving traits and the comparative method: how important is testing for phylogenetic signal. Evolutionary Ecology Research 6:377–396.Google Scholar
Ruta, M., Cisneros, J. C., Liebrecht, T., Tsuji, L. A., and Müller, J.. 2011. Amniotes through major biological crises: faunal turnover among parareptiles and the end-Permian mass extinction. Palaeontology 54:1117–1137.Google Scholar
Ruta, M., Botha-Brink, J., Mitchell, S. A., and Benton, M. J.. 2013. The radiation of cynodonts and the ground plan of mammalian morphological diversity. Proceedings of the Royal Society of London B 280:20131865.Google Scholar
Sansom, R., Wills, M. A., and Williams, T.. 2017. Dental data perform relatively poorly in reconstructing mammal phylogenies: morphological partition evaluated with molecular benchmarks. Systematic Biology 66:813–822.Google Scholar
Schoch, R. R., and Sues, H.-D.. 2015. A Middle Triassic stem-turtle and the evolution of the turtle body plan. Nature 523:584–587.Google Scholar
Sidor, C. A. 2003. Evolutionary trends and the origin of the mammalian lower jaw. Paleobiology 29:605–640.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 24:254–273.Google Scholar
Sigogneau-Russell, D., and Hahn, G.. 1994. Late Triassic microvertebrates from central Europe. Pp. 197–213 in Fraser, N. and Sues, H.-D., eds. In the shadow of the dinosaurs: early Mesozoic tetrapods. Cambridge University Press, Cambridge.Google Scholar
Sookias, R. B., Butler, R. J., and Benson, R. B. J.. 2012. Rise of the dinosaurs reveals major body-size transitions are driven by passive processes of trait evolution. Proceedings of the Royal Society of London B 279:2180–2187.Google Scholar
Tatarinov, L. P., and Maschenko, E. N.. 1999. A find of an aberrant tritylodont in the Lower Cretaceous of Mongolia. Paleontological Journal 33:430–437.Google Scholar
Upchurch, P., and Barrett, P. M.. 2005. Phylogenetic and taxic perspectives on sauropod diversity. Pp. 104–124 in Rogers, K. C. and Wilson, J. A, eds. The sauropods: evolution and palaeobiology. University of California Press, Berkeley.Google Scholar
van den Berg, T., Whiteside, D. I., Viegas, P., Schouten, R., and Benton, M. J.. 2012. The Late Triassic microvertebrate fauna of Tytherington, UK. Proceedings of the Geological Association 123:638–648.Google Scholar
Verrière, A., Brocklehurst, N., and Fröbisch, J.. 2016. Assessing the completeness of the fossil record: comparison of different methods applied to parareptilian tetrapods (Vertebrata: Sauropsida). Paleobiology 42:680–695.Google Scholar
Walther, M., and Fröbisch, J.. 2013. The quality of the fossil record of anomodonts. Comptes Rendus Palevol 12:495–504.Google Scholar
Watabe, M., Tsubamoto, T., and Tsogtbaatar, K.. 2007. A new tritylodontid synapsid from Mongolia. Acta Palaeontologia Polonica 52:263–274.Google Scholar