Evolutionary Trends of Protypotherium (Interatheriidae, Notoungulata) Lineage throughout the Miocene of South America

Abstract

Protypotherium (Mammalia, Notoungulata, lnteratheriinae) is a well-known and very diverse genus of extinct native ungulates of South America, widely distributed from southern to middle latitudes of Argentina, Chile, and Bolivia. This genus exhibits distinctive species throughout the Miocene to the beginning of the Pliocene that display an interesting size pattern. The large sample of specimens studied during several years of research allows us to analyze the shape and size of upper and lower molars for nine species of Protypotherium, in order to test the hypothesis of reduction of size ranges preserving a general tooth morphology as a response to climate deterioration, documented in South America by a marked reduction of temperature that occurred during Miocene times. Elliptic Fourier analyses were used to capture the shape of the occlusal morphology and the centroid size was also retained for subsequent analyses. Our results demonstrate that: 1) a similar morphological tooth pattern is observed among all species; 2) tooth shape variation is not associated with a change in size; and 3) there is a tendency to increase the size and decrease the number of species. This striking pattern could be correlated with a global trend to lower temperatures, which indicates a deterioration of paleoenvironmental conditions. A conservative tooth pattern, together with an increase of size and a reduction in number of species were the main evolutionary and ecological tendencies accounted in Protypotherium from the early to late Miocene-beginning of the Pliocene, which were accompanied by a latitudinal displacement from Patagonia to northern areas at the end of the Miocene.

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Data Availability

The datasets generated and/or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Adams DC, Collyer M L (2007) Analysis of character divergence along environmental gradients and other covariates. Evolution 3(61):510–515

    Article  Google Scholar 

  2. Adams DC, Collyer ML (2009) A general framework for the analysis of phenotypic trajectories in evolutionary studies. Evolution 5(63):1143–1154

    Article  Google Scholar 

  3. Adams DC, Collyer ML (2016) On the comparison of the strength of morphological integration across morphometric datasets. Evolution 11(70):2623–2631

    Article  Google Scholar 

  4. Adams DC, Otarola-Castillo, E (2013) Geomorph: an R package for the collection and analysis of geometric morphometric shape data. Meth Ecol Evol 4(4):393–399

    Article  Google Scholar 

  5. Ameghino F (1885) Nuevos restos de mamíferos fósiles oligocenos, recogidos por el profesor Pedro Scalabrini y pertenecientes al Museo Provincial de la Ciudad del Paraná. Bol Acad Nac Cienc Córdoba 8:85–207

    Google Scholar 

  6. Ameghino F (1887a) Enumeración sistemática de las especies de mamíferos fósiles coleccionados por Carlos Ameghino en terrenos eocenos de la Patagonia austral y depositados en el Museo La Plata. Bol Mus La Plata 1:1–26

    Google Scholar 

  7. Ameghino F (1887b) Observaciones generales sobre el orden de mamíferos extinguidos sud-americanos llamados toxodontes (Toxodontia) y sinopsis de los géneros y especies hasta ahora conocidos. An Mus La Plata 1(1):1–66

    Google Scholar 

  8. Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecol 1(26)32–46

    Google Scholar 

  9. Aragón E, Goin FJ, Aguilera Y, Woodburne MO, Carlini AA, Roggiero MF (2011) Palaeogeography and palaeoenvironments of northern Patagonia from the Late Cretaceous to the Miocene: the Palaeogene Andean gap and the rise of the North Patagonian High Plateau. Biol J Linnean Soc 103:305–315

    Article  Google Scholar 

  10. Armella M, Bonini RA (2020) Biostratigraphic signifcance of the presence of Protypotherium cf. P. antiquum Ameghino 1885 (Interatheriidae, Notoungulata) in the late Miocene of northwestern Argentina. J S Am Earth Sci. https://doi.org/10.1016/j.jsames.2020.102676

  11. Barreda V, Palazzesi L (2007) Patagonian vegetation turnovers during the Paleogene-Early Neogene: origin of arid-adapted floras. Bot Rev 73:31–50

    Article  Google Scholar 

  12. Billet G (2011) Phylogeny of the Notoungulata (Mammalia) based on cranial and dental characters. J Syst Palaeontol 4(9):481–497

    Article  Google Scholar 

  13. Boehme M, Winklhofer M (2008) A continental Miocene thermal maximum predates the Miocene climate optimum in central Europe. Geophys Res Abstr 10:EGU2008-A-08574

  14. Bond M (1986) Los ungulados fósiles de Argentina: evolución y paleoambientes. Actas IV Congr Arg Paleontol Bioestrat 2:173–185

    Google Scholar 

  15. Bonhomme V, Picq S, Gaucherel C, Claude J (2014) Momocs: outline analysis using R. J Stat Soft 13(56):1–24

    Google Scholar 

  16. Bonhomme V, Prasad S, Gaucherel C (2013) Intraspecific variability of pollen morphology as revealed by elliptic Fourier analysis. Plant Syst Evol 299:811–816

    Article  Google Scholar 

  17. Brea M, Zucol AF, Iglesias A (2012) Fossil plant studies from late early Miocene of Santa Cruz Formation: paleoecology and paleoclimatology at the passive margin of Patagonia, Argentina. In: Vizcaíno SF, Kay RF, Bargo MS (eds) Early Miocene Paleobiology in Patagonia: High-latitude Paleocommunities of the Santa Cruz Formation. Cambridge University Press, Cambridge, pp 104–128

  18. Cabrera A, Kraglievich L (1931) Diagnosis previas de los ungulados fósiles del Arroyo Chasicó. Notas Prelim Mus La Plata 1:107–113

    Google Scholar 

  19. Cassini GH, Hernández Del Pino S, Muñoz NA, Acosta MVW, Fernández F, Bargo MS, Vizcaíno SF (2017) Teeth complexity, hypsodonty and body mass in Santacrucian (early Miocene) notoungulates (Mammalia). Earth Environ Sci Trans R Soc Edinb 106: 303-313

    Google Scholar 

  20. Cassini GH, Vizcaíno SF, Bargo MS (2012) Body mass estimation in early Miocene native South American ungulates: a predictive equation based on 3D landmarks. J Zool 287:53–64

    Article  Google Scholar 

  21. Cerling TE, Harris JM, MacFadden BJ, Leakey MG, Quade J, Eisenmann V, Ehleringer JR (1997) Global vegetation change through the Miocene/Pliocene boundary. Nature 389:153–158

    CAS  Article  Google Scholar 

  22. Cione AL, Azpelicueta MM, Bond M, Carlini AA, Casciotta JR, Cozzuol MA, de la Fuente M, Gasparini Z, Goin FJ, Noriega J (2000) Miocene Vertebrates from Entre Ríos Province, eastern Argentina. In: Aceñolaza FG, Herbst R (eds) El Neógeno de Argentina. Serie Correlación Geológica 14:191–237

    Google Scholar 

  23. Claude J (2008) Morphometrics with R. Springer Science and Business Media, Berlin

    Google Scholar 

  24. Cohen KM, Finney SC, Gibbard PL, Fan J-X (2013) The ICS International Chronostratigraphic Chart. Episodes 36:199–204

    Article  Google Scholar 

  25. Collyer ML, Adams DC (2007) Analysis of two-state multivariate phenotypic change in ecological studies. Ecology 3(88):683–692

    Article  Google Scholar 

  26. Collyer ML, Adams DC (2013) Phenotypic trajectory analysis: comparison of shape change patterns in evolution and ecology. Hystrix 1(24):75–83

    Google Scholar 

  27. Collyer ML, Sekora DJ, Adams DC (2015) A method for analysis of phenotypic change for phenotypes described by high-dimensional data. Heredity 4(115):357–365

    Article  Google Scholar 

  28. Collyer ML, Stockwell CA, Adams DC, Reiser MH (2007) Phenotypic plasticity and contemporary evolution in introduced populations: evidence from translocated populations of white sands pupfish (Cyrpinodon tularosa). Ecol Res 6(22):902–910

    Article  Google Scholar 

  29. Croft DA (2001) Cenozoic environmental change in South America as indicated by mammalian body size distributions (cenograms). Divers Distrib 7:271–287

    Article  Google Scholar 

  30. Croft DA, Anaya F (2006) A new middle Miocene hegetotheriid (Notoungulata: Typotheria) and a phylogeny of the Hegetotheriidae. J Vertebr Paleontol 26: 387–399

    Article  Google Scholar 

  31. Croft DA, Anaya F, Auerbach D, Garzione C, MacFadden BJ (2009) New data on Miocene Neotropical provinciality from Cerdas, Bolivia. J Mammal Evol 16:175–198

    Article  Google Scholar 

  32. Croft DA, Carlini AA, Ciancio MR, Brandoni D, Drew NE, Engelman RK, Anaya F (2016) New mammal faunal data from Cerdas, Bolivia, a middle-latitude neotropical site that chronicles the end of the middle Miocene climatic optimum in South America. J Vertebr Paleontol 36:e1163574

    Article  Google Scholar 

  33. Croft DA, Gelfo JN, López GM (2020) Splendid Innovation: the extinct South American native ungulates. Annu Rev Earth Planet Sci 48:259–290

    CAS  Article  Google Scholar 

  34. Cuitiño JI, Fernicola JC, Kohn MJ, Trayler R, Naipauer M, Bargo MS, Kay RF, Vizcaíno SF (2016) U-Pb geochronology of the Santa Cruz Formation (early Miocene) at the Río Bote and Río Santa Cruz (southernmost Patagonia, Argentina): implications for the correlation of fossil vertebrate localities. J S Am Earth Sci 70:198–210

    Article  CAS  Google Scholar 

  35. Domingo L, Tomassini RL, Montalvo CI, Sanz-Pérez D, Alberdi MT (2020) The Great American Biotic interchange revisited: a new perspective from the stable isotope record of Argentine pampas fossil mammals. Sci Rep 10:1–10

    Article  CAS  Google Scholar 

  36. du Plessis KL, Martin RO, Hockey PAR, Cunningham SJ, Ridley AR (2012) The costs of keeping cool in a warming world: implications of high temperatures for foraging, thermoregulation and body condition of an arid-zone bird. Glob Change Biol 10(18):3063–3070

    Article  Google Scholar 

  37. Fernández M, Fernicola JC, Cerdeño ME, Reguero MA (2018) Identification of type materials of the species of Protypotherium Ameghino, 1885 and Patriarchus Ameghino, 1889 (Notoungulata: Interatheriidae) erected by Florentino Ameghino. Zootaxa 4387(3):473–498

    PubMed  Article  Google Scholar 

  38. Flower BP, Kennett JP (1993) Middle Miocene ocean-climate transition: high-resolution oxygen and carbon isotopic records from deep sea drilling project site 588A, southwest Pacific. Paleoceanograph Paleoclimatol 8(6):811–843

    Article  Google Scholar 

  39. Flower BP, Kennett JP (1994) The middle Miocene climatic transition: East Antarctic ice sheet development, deep ocean circulation and global carbon cycling. Palaeogeogr Palaeoclimatol Palaeoecol 108:537–555

    Article  Google Scholar 

  40. Gardner JL, Peters A, Kearney MR, Joseph L, Heinsohn R (2011) Declining body size: a third universal response to warming? Trends Ecol Evol 6(26):285–291

    Article  Google Scholar 

  41. Illius AW, Gordon IJ (1992) Modelling the nutritional ecology of ungulate herbivores: evolution of body size and competitive interactions. Oecologia 89:428–434

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  42. Janis CM (1993) Tertiary mammal evolution in the context of changing climates, vegetation, and tectonic events. Annu Rev Ecol Syst 1993. 24:467–500

    Article  Google Scholar 

  43. Kay RF, Vizcaino SF, Bargo MS (2012) A review of the paleoenvironment and paleoecology of the Miocene Santa Cruz Formation. In: Vizcaino SF, Kay RF, Bargo MS (eds) Early Miocene Paleobiology in Patagonia: High-latitude Paleocommunities of the Santa Cruz Formation. Cambridge University Press, Cambridge, pp 331–365

  44. Kramarz AG, Bond M, Arnal M (2015) Systematic description of three new mammals (Notoungulata and Rodentia) from the early Miocene Cerro Bandera Formation, northern Patagonia, Argentina. Ameghiniana 52:585–597

    Article  Google Scholar 

  45. Kuhl FP, Giardina CR (1982) Elliptic Fourier features of a closed contour. Comp Graph Imag Proc 3(18):236–258

    Article  Google Scholar 

  46. MacFadden BJ (1986) Fossil horses from ‘Eohippus’ (Hyracotherium) to Equus: scaling, Cope’s Law, and the evolution of body size. Paleobiology 12:355–369

    Article  Google Scholar 

  47. MacFadden BJ, Wang Y, Cerling TE, Anaya F (1994) South American fossil mammals and carbon isotopes: a 25 million-year sequence from the Bolivian Andes. Palaeogeogr Palaeoclimatol Palaeoecol 107:257–268

    Article  Google Scholar 

  48. Mendoza M, Palmqvist P (2008) Hypsodonty in ungulates: an adaptation for grass consumption or for foraging in open habitat?. J Zool 274 (2):134–142

  49. Montalvo C, Tomassini RL, Sostillo R, Cerdeño E, Verzi DH, Folguera A, Schmidt GI (2019) A Chasicoan (late Miocene) vertebrate assemblage from Cerro Azul Formation, central Argentina. Geomorphological and biochronological considerations. J S Am Earth Sci https://doi.org/10.1016/j.jsames.2019.102218

  50. Ortíz-Jaureguizar E, Alberdi MT (2003) El patrón de cambios en la masa corporal de los Hipparionini (Perissodactyla, Equidae) de la península ibérica durante el Mioceno Superior-Plioceno Superior. Coloq Paleontol 1:499–509

    Google Scholar 

  51. Palazzesi L, Barreda V, Prieto A (2003) Análisis evolutivo de la vegetación cenozoica en las provincias de Chubut y Santa Cruz (Argentina) con especial atención en las comunidades herbáceos-arbustivas. Rev Mus Arg Cien Nat 5(2):151–161

    Article  Google Scholar 

  52. Pascual R (1984) La sucesión de las edades-mamífero, de los climas y del diastrofismo sudamericano durante el Cenozoico: fenómenos concurrentes. Anales de la Academia Nacional de Ciencias Exactas, Físicas y Naturales, 36:15–37

    Google Scholar 

  53. Pascual R, Odreman Rivas OE (1971) Evolución de las comunidades de los vertebrados del Terciario argentino. Los aspectos paleozoogeográficos y paleoclimáticos relacionados. Ameghiniana 7:372–412

    Google Scholar 

  54. Pascual R, Ortíz-Jaureguizar E (1990) Evolving climates and mammal faunas in Cenozoic South America. J Human Evol 19:23–60

    Article  Google Scholar 

  55. Perkins ME, Fleagle JG, Heizler MT, Nash B, Bown TM, Tauber AA, Dozo MT (2012) Tephrochronology of the Miocene Santa Cruz and Pinturas formations, Argentina. In: Vizcaíno SF, Kay RF, Bargo MS (eds.) Early Miocene Paleobiology in Patagonia: High-latitude Paleocommunities of the Santa Cruz Formation. Cambridge University Press, Cambridge, pp 23–40

  56. R Development Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3–900051-07-0. Retrieved from http://www.Rproject.org

  57. Rabassa J (2008) Late Cenozoic glaciations in Patagonia and Tierra del Fuego. Developments in Quaternary Sciences 11:151–204

    Article  Google Scholar 

  58. Reguero MA, Prevosti FJ (2010) Rodent-like notoungulates (Typotheria) from Gran Barranca, Chubut Province, Argentina: phylogeny and systematics. In: Madden RH, Carlini AA, Vucetich MG, Kay RF (eds) The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, Cambridge, pp 148–165

    Google Scholar 

  59. Roff DA (2005) Variation and life-history evolution. In: Hallgrímsson BK, Hall B (eds) Variation: A Central Concept in Biology, 1st ed. Academic Press, Cambridge, pp 333–357

    Google Scholar 

  60. Rohlf RJ (2008) TPSDIG, Version 2.12. Stony Brook, NY: Department of Ecology and Evolution, State University of New York. Retrieved from http://life.bio.sunysb.edu/morph/

    Google Scholar 

  61. Roth S (1899) Apuntes sobre la geología y la paleontología de los territorios del Río Negro y Neuquén. Rev Mus La Plata 9:1–56

    Google Scholar 

  62. Scarano AC, Carlini AA, Illius AW (2011) Interatheriidae (Typotheria; Notoungulata), body size and paleoecology characterization. Mammal Biol 76:109–114

    Article  Google Scholar 

  63. Scarano AC, Vera B (2018) Age related change in molar shape variation of low-crowned Notoungulata (Mammalia), using geometric morphometric analysis: a proxy for systematic inferences. J Morphol 279(2):216–227

    PubMed  Article  PubMed Central  Google Scholar 

  64. Sinclair WJ (1909) Typotheria of the Santa Cruz beds. In: Scott WB (ed) Reports of the Princeton University Expedition to Patagonia 1896–1899 6:1–110

  65. Sostillo R, Montalvo C, Cerdeño E, Schmidt GI, Folguera A, Cardonatto MC (2020) Updated knowledge on the Notoungulata (Mammalia) from the late Miocene Cerro Azul Formation, La Pampa Province, Argentina. Hist Biol. https://doi.org/10.1080/08912963.2019.1689239

  66. Tauber A (1996) Los representantes del género Protypotherium (Mammalia, Notoungulata, Interatheriidae) del Mioceno Temprano del sudeste de la Provincia de Santa Cruz, República Argentina. Misc Acad Nac Cienc Córdoba 95:1–29

    Google Scholar 

  67. Vera B, Reguero M, González-Ruiz L (2017) The Interatheriinae notoungulates from the middle Miocene Collón Curá Formation in Argentina. Acta Palaeontol Pol 62(4):845–863

    Google Scholar 

  68. Vera B, Scarano A (2019) Evolutionary trends of Protypotherium lineage throughout the Miocene-Pliocene of South America. 79th Annual Meeting of the Society of Vertebrate Paleontology. Abstracts:211

  69. Vincent E, Berger WH (1985) Carbon dioxide and polar cooling in the Miocene: the Monterey hypothesis. In: Sundquist ET, Broecker WS (eds) The Carbon Cycle and Atmospheric CO2: Natural Variations Archean to Present. American Geophysical Union, Washington, D.C., pp 455–468

    Google Scholar 

  70. Westerhold T, Bickert T, Röhl U (2005) Middle to late Miocene oxygen isotope stratigraphy of ODP site 1085 (SE Atlantic): new constrains on Miocene climate variability and sea-level fluctuations. Palaeogeogr Palaeoclimatol Palaeoecol 217:205–222

    Article  Google Scholar 

  71. Williams SH, Kay RF (2001) A comparative test of adaptive explanations for hypsodonty in ungulates and rodents. J Mammal Evol 8(3):207–229

    Article  Google Scholar 

  72. Zachos J, Pagani M, Sloan L, Thomas E, Billups K (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292:686–693

    CAS  PubMed  Article  PubMed Central  Google Scholar 

  73. Zárate MA, Schultz PH, Blasi A, Heil C, King J, Hames W (2007) Geology and geochronology of type Chasicoan (late Miocene) mammal-bearing deposits of Buenos Aires (Argentina). J S Am Earth Sci 23:81–90

    Article  Google Scholar 

  74. Zimicz N, Payrola P, del Papa C (2018) New late Miocene mammalian assemblage from the Palo Pintado Formation (northwestern Argentina). J S Am Earth Sci 81:31–44

    Article  Google Scholar 

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Acknowledgements

We are grateful to the following institutions and people who provided access to the collections under their care: K.C. Beard (KUVP), Ari Iglesias and Nicolás Ferreiro (MAPBAR), A. Kramarz (MACN), J. Cundiff (MCZ), G. Billet (MNHN), and E. Robert (UCBL-FSL). We thank Matías A. Armella and one anonymous reviewer for their helpful comments. Also, we thank John Wible for his helpful comments in the review process.

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Correspondence to Alejo C. Scarano.

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Scarano, A.C., Vera, B. & Reguero, M. Evolutionary Trends of Protypotherium (Interatheriidae, Notoungulata) Lineage throughout the Miocene of South America. J Mammal Evol (2021). https://doi.org/10.1007/s10914-020-09534-5

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Keywords

  • Interatheriidae
  • Typotheria
  • Tooth morphology
  • Size variation
  • Elliptic Fourier analysis