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Tooth Size Variation in Assemblages of Tremacyllus (Hegetotheriidae, Notoungulata): Insights into Geographical Gradients, Systematics, and Sexual Dimorphism

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Abstract

Tooth size variation within fossil assemblages can be associated with intra- or interspecific variation, functional, developmental, and geographical factors, and/or sexual dimorphism. Understanding these sources of variation is necessary to develop diagnoses for fossil mammals, where teeth are usually the most frequent remains. Tremacyllus (Ameghino, 1891) (Hegetotheriidae, Notoungulata) is a genus of small-sized herbivorous mammals abundant in late Miocene to Pliocene outcrops of southern South America. Its simplified, euhypsodont dentition and size variability have hampered systematics studies and led, for instance, to an overestimation of the number of species. I analyzed tooth size variations within assemblages of Tremacyllus in a quantitative framework to test three hypotheses: (1) magnitudes of size variation are different among tooth loci and assemblages; (2) tooth size follows a geographical pattern within the analyzed sample (Bergmann’s rule), but is also associated with taxonomy; and (3) there is a correlation between size variation and sexual dimorphism reflected in distinguishable subgroups. Results indicate that patterns of variation might be associated with eruption time and/or functional position. Northwestern forms are larger than southwestern-Pampean ones, not conforming to Bergmann’s rule but revealing a strong influence of latitude. Size differences between assemblages agree with dental features that distinguish T. incipiens and T. impressus, allowing expanded species diagnoses. Two size subgroups might reflect sexual dimorphism in the absence of biostratigraphic or morphological differences between them. This interpretation indicates that northwestern specimens referred to T. diminutus should be referred to T. incipiens.

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References

  • Ameijeiras-Alonso J, Crujeiras RM, Rodríguez-Casal A (2019) Mode testing, critical bandwidth and excess mass. Test 28(3):900–919

    Google Scholar 

  • Ameijeiras-Alonso J, Crujeiras RM, Rodriguez-Casal A (2021) multimode: An R Package for Mode Assessment. J of Statistical Softw 97(1):1–32

    Google Scholar 

  • Ameghino F (1885) Nuevos restos de mamíferos fósiles oligocenos recogidos por el Profesor Pedro Scalabrini y pertenecientes al Museo Provincial de la ciudad de Paraná. Bol Acad Nac Cien Córdoba 8:5–207

    Google Scholar 

  • Ameghino F (1891) Mamíferos y aves fósiles argentinos. Especies nuevas, adiciones y correcciones. Rev Arg Hist Nat 1:240–259

    Google Scholar 

  • Ameghino F (1908) Las formaciones sedimentarias de la región litoral de Mar del Plata y Chapalmalán. An Mus Nac Buenos Aires 3:343–428

    Google Scholar 

  • Andersson M (1994) Sexual Selection. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Armella MA (2019) Sistemática, bioestratigrafía y paleobiogeografía de los notoungulados del Neógeno del Noroeste Argentino. Dissertation, Universidad Nacional de Tucumán

  • Armella MA, Domínguez L, Georgieff SM, Esteban GI, Sabater S (2020) First radioisotopic age and sedimentary analysis of the Las Cañas Formation in Termas de Río Hondo, Santiago del Estero (Northwestern Argentina). J South Am Earth Sci 104:102868

  • Armella MA, Ercoli MD, Bonini RA, García-López DA (in press) Detecting morphological gaps in teeth outlines of a Pachyrukhinae (Hegetotheriidae, Notoungulata) lineage: systematic and palaeobiogeographical significance of the records from Northwestern Argentina. Comptes Rendus – Palevol

  • Armella MA, García-López DA, Esteban GI (2015) Nuevo registro y revisión del género Tremacyllus (Pachyrukhinae, Hegetotheriidae, Notoungulata) del Mioceno tardío de la Provincia de Catamarca. Ameghiniana 52(4):R6

    Google Scholar 

  • Armella MA, García-López DA, Esteban GI (2019) Paleobiogeografía del Orden Notoungulata en el Neógeno del Noroeste Argentino: análisis integral de los registros de la región. Act Res V Simp Mio-Pleist Centro y Norte Arg:165–168

  • Armella MA, Madozzo Jaén C, Nasif NL, García-López DA, Esteban GI, Ortiz PE, González R, Babot J, Georgieff S (2016) Vertebrados de la Formación Andalhuala en la localidad de Encalilla, Tucumán, Argentina. Ameghiniana 53(1):R4

    Google Scholar 

  • Barreda V, Anzótegui M, Prieto A, Aceñolaza PM, Bianchi M, Borromei AM, Brea M, Caccavari M, Cuadrado GA, Garralla S, Grill S, Guerstein GR, Lutz A, Mancini MV, Mautino LR, Ottone EG, Quattrocchio M, Romero EJ, Zamaloa MC, Zucol A (2007) Diversificación y cambios de las angiospermas durante el Neógeno en Argentina. Ameghiniana 11:173–191

    Google Scholar 

  • Benaglia T, Chauveau D, Hunter D, Young D (2009) mixtools: An R package for analyzing finite mixture models. J of Statistical Softw, 32(6):1–29

    Google Scholar 

  • Bergmann KGLC (1847) Über die Verhältnisse der wärmeokönomie der Thiere zu ihrer Grösse. Göttinger Studien 3:595–708

    Google Scholar 

  • Biernacki C, Celeux G, Govaert G (2000) Assessing a mixture model for clustering with the integrated completed likelihood. IEEE Trans Pattern Anal Mach Intell 22(7):719–725

    Google Scholar 

  • Billet G, Bardin, J (2021) Segmental series and size: clade-wide investigation of molar proportions reveals a major evolutionary allometry in the dentition of placental mammals. Syst Biol. https://doi.org/10.1093/sysbio/syab007

    Article  PubMed  Google Scholar 

  • Blackburn TM, Gaston KJ, Loder N (1999) Geographic gradients in body size: a clarification of Bergmann’s rule. Div and Dist 5:165–174

    Google Scholar 

  • Bonhomme V, Picq S, Gaucherel C, Claude J (2014) Momocs: outline analysis using R. J of Statistical Softw 56:1–24

    Google Scholar 

  • Bonini R (2014) Bioestratigrafía y diversidad de los mamíferos del Neógeno de San Fernando y Puerta de Corral Quemado (Catamarca, Argentina). Dissertation, Universidad Nacional de La Plata

  • Burmeister CV (1888) Relación de un viaje a la Gobernación de Chubut. An Mus Nac Buenos Aires 3:175–222

    Google Scholar 

  • Cerdeño E, Bond M (1998) Taxonomic Revision and Phylogeny of Paedotherium and Tremacyllus (Pachyrukhinae, Hegetotheriidae, Notoungulata) from the late Miocene to the Pleistocene of Argentina. J Vertebr Paleontol 18:799–811

    Google Scholar 

  • Cerdeño E, Reguero M (2015) The Hegetotheriidae (Mammalia, Notoungulata) assemblage from the late Oligocene of Mendoza, central-western Argentina. J Vertebr Paleontol 35:e907173

    Google Scholar 

  • Cerdeño E, Montalvo CI, Sostillo R (2017) Deciduous dentition and eruption pattern in Paedotherium (Pachyrukhinae, Hegetotheriidae, Notoungulata) from Late Miocene of La Pampa Province, Argentina. Hist Biol 29:359–375

    Google Scholar 

  • Cheng MY, Hall P (1998) Calibrating the excess mass and dip tests of modality. J R Statist Soc: Series B (Statistical Methodology) 60(3):579–589

    Google Scholar 

  • Conover WJ, Iman RL (1981) Rank transformations as a bridge between parametric and nonparametric statistics. Am Statistician 35(3):124–129

    Google Scholar 

  • Copes LE, Schwartz GT (2010) The scale of it all: postcanine tooth size, the taxon-level effect, and the universality of Gould’s scaling law. Paleobiol 36(2):188–203

    Google Scholar 

  • Creighton GK (1980) Static allometry of mammalian teeth and the correlation of tooth size and body size in contemporary mammals. J Zool 191(4):435–443

    Google Scholar 

  • 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

    Google Scholar 

  • Elissamburu A, Dondas A, De Santis L (2011) Morfometría de las paleocuevas de la “Fm”. Chapadmalal y su asignación a Actenomys (Rodentia), Paedotherium (Notoungulata) y otros mamíferos fósiles hospedantes. Mastozool Neotrop 18(2):227–238

    Google Scholar 

  • Ercoli MD, Candela AM, Rasia LL, Ramírez MA (2017) Dental shape variation of Neogene Pachyrukhinae (Mammalia, Notoungulata, Hegetotheriidae): systematics and evolutionary implications for the late Miocene Paedotherium species. J Syst Palaeontol 16(13):1073–1095

    Google Scholar 

  • Fairbairn DJ, Blanckenhorn WU, Székely T (2007) Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press. Oxford

  • Fox J, Weisberg S (2019) An R Companion to Applied Regression, Third Edition. Thousand Oaks CA: Sage. https://socialsciences.mcmaster.ca/jfox/Books/Companion/

  • Garrido AC, Turazzini GF, Bond M, Aguirrezabala G, Forasiepi AM (2014) Estratigrafía, vertebrados fósiles y evolución tectosedimentaria de los depósitos neógenos del Bloque de San Rafael (Mioceno-Plioceno), Mendoza, Argentina. Act Geol Lilloana 26:133–164

    Google Scholar 

  • Georgieff SM, Muruaga CM, Ibañez LM, Spagnuolo C, Bonini R, Esteban G, Nasif N, Del Pero MA (2017) Estilos de deformación, cronoestratigrafía y evolución paleoambiental de las unidades neógenas de las Sierras Pampeanas Noroccidentales de Catamarca y Tucumán, Argentina. In: Muruaga CM, Grosse P (eds) Ciencias de la Tierra y Recursos Naturales del NOA, Relatorio del XX Congreso Geológico Argentino. San Miguel de Tucumán, pp 254–268

  • Gingerich PD (1974) Size variability of the teeth in living mammals and the diagnosis of closely related sympatric fossil species. J Paleont 48(5):895–903

    Google Scholar 

  • Godfrey LR, Lyon SK, Sutherland MR (1993) Sexual dimorphism in large-bodied primates: the case of the subfossil lemurs. Am J Phys Anth 90(3):315–334

    CAS  Google Scholar 

  • Gomes Rodrigues H, Lefebvre R, Fernández-Monescillo M, Mamani Quispe B, Billet G (2017) Ontogenetic variations and structural adjustments in mammals evolving prolonged to continuous dental growth. R Soc Open Sci 4(7):170494

    PubMed  PubMed Central  Google Scholar 

  • Gould SJ (1975) On the scaling of tooth size in mammals. Am Zoologist 15(2):353–362

    Google Scholar 

  • Greenwood PJ, Wheeler P (1985) The evolution of sexual size dimorphism in bird and mammals: a “hot blooded” hypothesis. In: Greenwood PJ, Harvey PH, Stalkin M (eds) Evolution. Essays in Honour of John Maynard Smith. Cambridge University Press, Cambridge, pp 287–299

    Google Scholar 

  • Hall P, York M (2001) On the calibration of Silverman’s test for multimodality. Stat Sinica 11:515–536

    Google Scholar 

  • Hartigan JA, Hartigan PM (1985) The dip test of unimodality. Ann Stat 13:70–84

  • Hervé M (2021) RVAideMemoire: Testing and Plotting Procedures for Biostatistics. R package version 0.9–79. https://CRAN.Rproject.org/package=RVAideMemoire

  • Hijmans RJ (2020) raster: Geographic Data Analysis and Modeling. R package version 3.4-5. https://CRAN.R-project.org/package=raster

  • Isaac JL (2005) Potential causes and life-history consequences of sexual size dimorphism in mammals. Mamm Rev 35(1):101–115

    Google Scholar 

  • Janis CM (1990) Correlation of cranial and dental variables with dietary preferences in mammals: a comparison of macropodoids and ungulates. Mem Queensland Mus 28(1):349–366

    Google Scholar 

  • Kaiser TM, Fickel J, Streich, WJ, Hummel J, Clauss M (2010) Enamel ridge alignment in upper molars of ruminants in relation to their natural diet. J Zool 281(1):12–25.

    Google Scholar 

  • Kaiser TM, Fortelius M (2003) Differential mesowear in occluding upper and lower molars: opening mesowear analysis for lower molars and premolars in hypsodont horses. J Morph 258(1):67–83

    PubMed  Google Scholar 

  • Kuhl FP, Giardina CR (1982) Elliptic Fourier features of a closed contour. Comput Graph Imag Proc18(3):236–258

    Google Scholar 

  • Lindenfors P, Gittleman JL, Jones KE (2007) Sexual size dimorphism in mammals. In: Fairbairn DJ, Blanckenhorn WU, Szekely T (eds) Sex, Size, and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism, Oxford University Press, pp 16–26

  • Loison A, Gaillard JM, Pélabon C, Yoccoz NG (1999) What factors shape sexual size dimorphism in ungulates? Evolut Ecol Res 1(5):611–633

    Google Scholar 

  • Loomis EB (1914) The Deseado Formation of Patagonia. Runford Press, Concord

    Google Scholar 

  • Makowski D, Ben-Shachar MS, Lüdecke D (2019) bayestestR: Describing effects and their uncertainty, existence and significance within the Bayesian framework. J Open Sour Softw 4(40):1541

  • McKenna MC, Bell S (1997) Classification of Mammals Above the Species Level. Columbia University Press, New York

    Google Scholar 

  • McNab BK (1971) On the ecological significance of Bergmann’s rule. Ecology 52(5):845–854

    Google Scholar 

  • Meiri S (2011) Bergmann’s Rule–what’s in a name? Glob Ecol Biogeogr 20(1):203–207

    Google Scholar 

  • Meiri S, Dayan T (2003) On the validity of Bergmann’s rule. J Biogeogr 30:331–351

    Google Scholar 

  • Meiri S, Yom-Tov Y, Geffen E (2007) What determines conformity to Bergmann’s rule? Glob Ecol Biogeogr 16(6):788–794

    Google Scholar 

  • Müller DW, Sawitzki G (1991) Excess mass estimates and tests for multimodality. J Am Statistic Assoc 86(415):738–746

    Google Scholar 

  • Nakazawa M (2019) fmsb: Functions for Medical Statistics Book with some Demographic Data. R package version 0.7.0. https://CRAN.R-project.org/package=fmsb

  • Oxnard CE (1987) Fossils, Teeth and Sex. University of Washington Press, Seattle

    Google Scholar 

  • Pearson K (1896) Mathematical contributions to the theory of evolution. III. Regression, heredity and panmixia. Phil Trans R Soc A 187:253–318

    Google Scholar 

  • Plavcan JM (1994) Comparison of four simple methods for estimating sexual dimorphism in fossils. Am J Phys Anth 94(4):465–476

    CAS  Google Scholar 

  • Prado JL, Chiesa J, Tognelli G, Cerdeño E, Strasser E (1998) Los mamíferos de la Formación Río Quinto (Plioceno), provincia de San Luis. Aspectos paleoambientales y bioestratigráficos. Est Geol 54:153–160

    Google Scholar 

  • Quin DG, Smith AP, Norton TW (1996) Eco-geographic variation in size and sexual dimorphism in sugar gliders and squirrel gliders (Marsupialia: Petauridae). Austr J Zool 44(1):19–45

    Google Scholar 

  • R Core Team (2017, 2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.r-project.org/

  • Reguero MA, Candela AM, Alonso RN (2007) Biochronology and biostratigraphy of the “Uquian” mammals (Pliocene-Early Pleistocene, NW of Argentina) and their significance in the Great American Biotic Interchange. J South Am Earth Sci 23:1–16

    Google Scholar 

  • Reguero MA, Candela, AM, Cassini G 2010. Hypsodonty and body size in rodent-like notoungulates. In: Madden R, Carlini AA, Vucetich MG, Kay R (eds) The Paleontology of Gran Barranca: Evolution and Environmental Change through the Middle Cenozoic of Patagonia. Cambridge University Press, New York, pp 362–371

    Google Scholar 

  • Reuter DM, Hopkins SS, Davis EB (2021) Carnivoran intraspecific tooth-size variation shows heterogeneity along the tooth row and among species. J Mamm 102(1):236–249

    Google Scholar 

  • Riggs ES, Patterson B (1939) Stratigraphy of the Late-Miocene and Pliocene deposits of the Province of Catamarca (Argentina) with notes on the faunae. Physis 14:143–162

    Google Scholar 

  • Rovereto, C. 1914. Los estratos araucanos y sus fósiles. An Mus Nac Hist Nat 25:1–247.

    Google Scholar 

  • Schwarz G (1978) Estimating the dimension of a model. Ann Stat 6(2):461–464

    Google Scholar 

  • Shelomi M, Zeuss D (2017) Bergmann’s and Allen’s rules in native European and Mediterranean Phasmatodea. Front Ecol Evol 5:25

  • Scrucca L, Fop M, Murphy TB, Raftery AE (2016) mclust 5: clustering, classification and density estimation using Gaussian finite mixture models. The R J 8(1):289

    PubMed  Google Scholar 

  • Scherrer B (1984) Biostatistique. Gaëtan Morin Editeur, Montréal

    Google Scholar 

  • Simpson GG (1945) The principles of classification and a classification of mammals. Bull. Am. Mus Nat Hist 85:1–350

    Google Scholar 

  • Simpson GG (1948) The beginning of the age of mammals in South America. Part I. Bull Am Mus Nat Hist 91:1–232

    Google Scholar 

  • Silverman BW (1981) Using kernel density estimates to investigate multimodality. J R Statist Soc: Series B (Methodological) 43(1):97–99

    Google Scholar 

  • Sostillo R, Cerdeño E, Montalvo CI (2018) Taxonomic implications of a large sample of Tremacyllus (Hegetotheriidae: Pachyrukhinae) from the late Miocene Cerro Azul Formation of la Pampa, Argentina. Ameghiniana 55:407–422

    Google Scholar 

  • Szuma E (2000) Variation and correlation patterns in the dentition of the red fox from Poland. Annales Zoologici Fennici 37:113–127

    Google Scholar 

  • Tauber AA (2005) Mamíferos fósiles y edad de la Formación Salicas (Mioceno tardío) de la sierra de Velasco, La Rioja, Argentina. Ameghiniana 42:443–460

    Google Scholar 

  • Tauber AA, Krapovickas JM, Marengo H, Haro A (2014) Paleontología del Cenozoico. In: Martino RD, Guereschi AB (eds) Relatorio de la Geología y Recursos Naturales de la Provincia de Córdoba, 19º Congreso Geológico Argentino. Córdoba, Argentina, pp 591–621

    Google Scholar 

  • Tomassini RL (2012) Estudio tafonómico y bioestratigráfico de los vertebrados de la Formación Monte Hermoso (Plioceno) en su localidad tipo, provincia de Buenos Aires. Dissertation, Universidad Nacional del Sur

  • Tomassini RL, Montalvo CI, Deschamps CM, Manera T (2013) Biostratigraphy and biochronology of the Monte Hermoso Formation (early Pliocene) at its type locality, Buenos Aires Province, Argentina. J South Am Earth Sci 48:31–42

    Google Scholar 

  • van Hinsbergen DJ, De Groot LV, van Schaik SJ, Spakman W, Bijl PK, Sluijs A, Langereis CG, Brinkhuis H (2015) A paleolatitude calculator for paleoclimate studies. PloS one 10(6): e0126946

    PubMed  PubMed Central  Google Scholar 

  • van Valkenburgh B, Sacco T (2002) Sexual dimorphism, social behavior, and intrasexual competition in large Pleistocene carnivorans. J Vertebr Paleontol 22:164–169

    Google Scholar 

  • Vera B (2016) Phylogenetic revision of the South American notopithecines (Mammalia: Notoungulata). J Syst Palaeontol 14(6):461–480

    Google Scholar 

  • Vera B, Ercoli MD (2018) Systematic and morphogeometric analyses of Pachyrukhinae (Mammalia, Hegetotheriidae) from the Huayquerías, Mendoza (Argentina): biostratigraphic and evolutionary implications. J Vertebr Paleontol 38(3):e1473410

    Google Scholar 

  • Vitzthum VJ (1990) Odontometric variation within and between taxonomic levels of cercopithecidae: Implications for interpetations of fossil samples. Hum Evol 5(4):359

    Google Scholar 

  • Zetti J (1972) Los mamíferos fósiles de edad huayqueriense (Plioceno medio) de la región pampeana. Dissertation, Universidad de La Plata

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Acknowledgments

I thank D. Croft, the associate editor, J. Tejada, and two anonymous reviewers for their useful comments and suggestions that improve this study. Also, I thank D.A. García-López for his helpful comments on the first version of this manuscript. The following curators and collection managers kindly allowed access to specimens in their care: P. Ortiz (Colección Paleontología Vertebrados Lillo, San Miguel de Tucumán, Tucumán, Argentina); S. Sabater (Museo Municipal ‘Rincón de Atacama’, Termas de Río Hondo, Santiago del Estero, Argentina); C. Montalvo (Facultad de Ciencias Exactas y Naturales, Universidad Nacional de La Pampa, Santa Rosa, La Pampa, Argentina); A. Kramarz (Museo Argentino de Ciencias Naturales ‘Bernardino Rivadavia’, Buenos Aires, Argentina); and M. Reguero (Museo de La Plata, La Plata, Buenos Aires, Argentina). I acknowledge G. Esteban, N. Nasif, and R. Bonini for their comments on the paleontological context of the findings. I also thank to M. Ercoli for sharing specimen photographs (FMNH) and M.C. Gallo for dispelling doubts on statistical approaches.

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Asociación Paleontológica Argentina, Argentina (APA-Bunge & Born Grants 2017; awarded to M.A. Armella); and Secretaría de Ciencia, Arte e Innovación Tecnológica, Universidad Nacional de Tucumán, Argentina (PIUNT 2018 G-626).

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Armella, M.A. Tooth Size Variation in Assemblages of Tremacyllus (Hegetotheriidae, Notoungulata): Insights into Geographical Gradients, Systematics, and Sexual Dimorphism. J Mammal Evol 29, 113–128 (2022). https://doi.org/10.1007/s10914-021-09575-4

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