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A Cretaceous eutriconodont and integument evolution in early mammals

Nature volume 526, pages 380–384 (2015)Cite this article

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Abstract

The Mesozoic era (252–66 million years ago), known as the domain of dinosaurs, witnessed a remarkable ecomorphological diversity of early mammals. The key mammalian characteristics originated during this period and were prerequisite for their evolutionary success after extinction of the non-avian dinosaurs 66 million years ago. Many ecomorphotypes familiar to modern mammal fauna evolved independently early in mammalian evolutionary history. Here we report a 125-million-year-old eutriconodontan mammal from Spain with extraordinary preservation of skin and pelage that extends the record of key mammalian integumentary features into the Mesozoic era. The new mammalian specimen exhibits such typical mammalian features as pelage, mane, pinna, and a variety of skin structures: keratinous dermal scutes, protospines composed of hair-like tubules, and compound follicles with primary and secondary hairs. The skin structures of this new Mesozoic mammal encompass the same combination of integumentary features as those evolved independently in other crown Mammalia, with similarly broad structural variations as in extant mammals. Soft tissues in the thorax and abdomen (alveolar lungs and liver) suggest the presence of a muscular diaphragm. The eutriconodont has molariform tooth replacement, ossified Meckel’s cartilage of the middle ear, and specialized xenarthrous articulations of posterior dorsal vertebrae, convergent with extant xenarthran mammals, which strengthened the vertebral column for locomotion.

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Figure 1: New Early Cretaceous gobiconodontid Spinolestes xenarthrosus.
Figure 2: New gobiconodontid S. xenarthrosus, holotype counter slab (MCCMLH30000B) and integumentary structures.

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Acknowledgements

Research funds were provided by Spanish MINECO, Project CGL-2013-42643 P and Junta de Comunidades de Castilla-La Mancha. We thank J. L. Sañudo for finding the specimen, M. Llandres and O. Dülfer for preparation, D. Kranz for artwork, O. Sanisidro for the lifelike reconstruction of S. xenarthrosus, G. Oleschinski for photography, M. Furió and A. Valera for SEM, K. Jäger for three-dimensional reconstructions, and T. McCann for improving the English. R. L. Cifelli is thanked for review and B. Mähler for discussion on actuo-taphonomical experiments on rat carcasses.

Author information

Authors and Affiliations

  1. Steinmann-Institut für Geologie, Mineralogie und Paläontologie, Universität Bonn, Nussallee 8, Bonn, 53115, Germany

    Thomas Martin

  2. Departamento de Biología, Unidad de Paleontología, Facultad Ciencias, Universidad Autónoma de Madrid, C/Darwin 2, Madrid, 28049, Spain

    Jesús Marugán-Lobón, Hugo Martín-Abad & Angela D. Buscalioni

  3. Dinosaur Institute, Natural History Museum of Los Angeles County, 900 Exposition Boulevard, Los Angeles, 90007, California, USA

    Jesús Marugán-Lobón

  4. Géosciences Rennes, UMR CNRS 6118, Université de Rennes 1, Campus de Beaulieu, bâtiment 15, 263 avenue du Général Leclerc, CS 74205, Rennes, 35042, France

    Romain Vullo

  5. Department of Organismal Biology and Anatomy, The University of Chicago, 1027 East 57th Street, Chicago, 60637, Illinois, USA

    Zhe-Xi Luo

Authors
  1. Thomas Martin
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Contributions

A.D.B. designed the Las Hoyas research project; J.M.-L., R.V., H.M.-A., and A.D.B. participated in the fieldwork; T.M., J.M.-L., R.V., H.M.-A., Z.-X.L., and A.D.B. organized and conducted the research (preparation, computed tomography scan, light microscopy, and SEM imaging) and analysed data; Z.-X.L. performed phylogenetic analyses; and T.M., J.M.-L., R.V., Z.-X.L., and A.D.B. wrote the manuscript.

Corresponding authors

Correspondence to Thomas Martin, Zhe-Xi Luo or Angela D. Buscalioni.

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The authors declare no competing financial interests.

Extended data figures and tables

Extended Data Figure 1 New gobiconodontid S. xenarthrosus, holotype transferred slab MCCMLH30000A.

Skull exposed in ventral aspect. Inset: left calcaneus in dorsal view on the same slab somewhat apart from the skeleton. Arrow points to skin patch preserving hair bundles between dorsal vertebrae 11 and 14.

Extended Data Figure 2 Dentition and xenarthrous vertebrae of Spinolestes.

a, SEM images (stereo pair) of right lower mandible and right upper maxilla with molariforms. b, SEM image of anterior portion of skull and mandibles with dentition. c, SEM image of penultimate (m3) and ultimate (m4) right lower molariforms in lingual view. Abbreviations: C/c, upper/lower canine; I/i, incisor; M/m, molariform; P/p, premolar; D/d, deciduous tooth; R/r, replacing tooth. d, SEM images (stereo pair) of dorsal vertebrae D 12 to D 19 in lateral aspect with ribs.

Extended Data Figure 3 Phylogenetic relationships of Spinolestes and patterns of mammalian integumentary structure in early mammalian evolution.

a, Position of Spinolestes within Eutriconodonta (Bremer index/bootstrap values on the key clades of this study). b, Evolution of mammalian integumentary structures (simplified tree). Data sets and full analyses are presented in Supplementary Information.

Extended Data Figure 4 Skin structures of S. xenarthrosus.

a, SEM image of skin surface showing compound hair follicles (FO), epidermal cells (keratinocytes), and pores (P). b, Schematic drawings of scale-like skin folds (SCF) with compound hair follicles (FO) of the dog with primary (PH) and secondary (SH) hairs of three ontogenetic stages (redrawn from ref. 38). c, Skin surface of Spinolestes with scale-like wrinkles. d, Schematic diagram of scale-like wrinkled skin folds with hair follicles of a dog (redrawn from ref. 38). e, SEM image of epidermal cells (keratinocytes) of a hair follicle. f, SEM images of skin surface with polygonal epidermal cells (keratinocytes) and pores. g, Detail of the keratinocytes.

Extended Data Figure 5 SEM images and interpretative line drawings of cuticular scale patterns.

a–c, Primary (a, b) and secondary (b, c) hairs.

Extended Data Figure 6 Hair structures of S. xenarthrosus.

a, c, d, Patch of skin located between dorsal vertebrae 11 and 14 (arrow in Fig. 1 and Extended Data Fig. 1) on slab MCCMLH30000A under translucent light. b, SEM image of an orifice of a compound follicle (FO) with primary hair (PH) and three broken secondary hairs (SH). e, SEM image of a fraying hair of S. xenarthrosus showing fusiform cortical cells (FCC). f, Schematic diagram of human hair bulb (B) with cuticular scales (CU) and fusi (F) of the hair shaft (HS). g, Schematic diagram of a human head hair with fusiform cortical cells (FCC) and fusi. f, g, Redrawn from ref. 40. Abbreviations: C, cuticula; HB, hair bulb.

Extended Data Figure 7 External pinna of S. xenarthrosus.

a, b, Comparison with pinna and scalp of decaying rat (Rattus norvegicus): a, on transferred slab MCCMLH30000A; b, on counter slab MCCMLH30000B on original limestone rock matrix. c, d, Pinna and scalp of decaying rat (Rattus norvegicus) for comparison. c, Head of decaying rat after 274 days in water at room temperature. The skull is detached from the scalp and has fallen to the bottom. Scalp and right pinna are still intact and connected to the torso of the floating carcass. d, Detail of c with well-preserved right pinna in original position at the scalp. The mandible is displaced and loosely hanging down from the skin.

Extended Data Figure 8 Keratinous dermal scutes (SC) of S. xenarthrosus.

a, Oval dermal scutes dorsally of dorsal vertebra 20. b, Oval dermal scute dorsally of left ischium (ISC-L). c, Oval dermal scute from dorsal region with tubules (T) merging to homogeneous keratinous matrix.

Extended Data Figure 9 Visceral cavities of S. xenarthrosus with internal organs.

a, Detail of the visceral cavities of MCCMLH30000B with separation of the anterior thoracic cavity (TC) containing the lungs (LU), and the posterior abdominal cavity (AC) containing the liver (LI). Dashed line represents the diaphragm. SE, sternal elements. b, Lung tissue in the anterior part of the thoracic cavity. c, Peripheral conducting and acinar airways of the lungs with typical dichotomous structure of the bronchial tree. d, Peripheral conducting and acinar airways of the lungs from transferred slab MCCMLH30000A under translucent light. e, f, Details of the peripheral conducting airway dichotomies (DI) and acinar structures (ACI) of the lungs.

Extended Data Figure 10 Lifelike reconstruction of S. xenarthrosus.

Supplementary information

Supplementary Information

This file contains Supplementary Text and Data, see contents page for details. (PDF 2988 kb)

CT reconstruction of right maxilla of Spinolestes xenarthrosus with heavily worn DM3 and DM4 still in place labially of replacing M3 and M4.

CT reconstruction of right maxilla of Spinolestes xenarthrosus with heavily worn DM3 and DM4 still in place labially of replacing M3 and M4. (MP4 12294 kb)

CT reconstruction of right mandible of Spinolestes xenarthrosus with wide Meckel´s groove (ossified Meckel´s cartilage fallen off).

CT reconstruction of right mandible of Spinolestes xenarthrosus with wide Meckel´s groove (ossified Meckel´s cartilage fallen off). (MP4 12361 kb)

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Martin, T., Marugán-Lobón, J., Vullo, R. et al. A Cretaceous eutriconodont and integument evolution in early mammals. Nature 526, 380–384 (2015). https://doi.org/10.1038/nature14905

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