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Jurassic fossil juvenile reveals prolonged life history in early mammals

Nature volume 632, pages 815–822 (2024)Cite this article

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Abstract

Living mammal groups exhibit rapid juvenile growth with a cessation of growth in adulthood1. Understanding the emergence of this pattern in the earliest mammaliaforms (mammals and their closest extinct relatives) is hindered by a paucity of fossils representing juvenile individuals. We report exceptionally complete juvenile and adult specimens of the Middle Jurassic docodontan Krusatodon, providing anatomical data and insights into the life history of early diverging mammaliaforms. We used synchrotron X-ray micro-computed tomography imaging of cementum growth increments in the teeth2,3,4 to provide evidence of pace of life in a Mesozoic mammaliaform. The adult was about 7 years and the juvenile 7 to 24 months of age at death and in the process of replacing its deciduous dentition with its final, adult generation. When analysed against a dataset of life history parameters for extant mammals5, the relative sequence of adult tooth eruption was already established in Krusatodon and in the range observed in extant mammals but this development was prolonged, taking place during a longer period as part of a significantly longer maximum lifespan than extant mammals of comparable adult body mass (156 g or less). Our findings suggest that early diverging mammaliaforms did not experience the same life histories as extant small-bodied mammals and the fundamental shift to faster growth over a shorter lifespan may not have taken place in mammaliaforms until during or after the Middle Jurassic.

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Fig. 1: New specimens of K. kirtlingtonensis.
Fig. 2: Juvenile specimen of K. kirtlingtonensis, NMS G.2023.8.1.
Fig. 3: Juvenile and adult skulls of K. kirtlingtonensis, overview of phylogeny and cementum for adult.
Fig. 4: Reconstructed skull and cementum chronology for juvenile K. kirtlingtonensis, NMS G.2023.8.1.
Fig. 5: Analyses of body size and mass against tooth eruption and weaning time.

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Data availability

The CT and PPC-SRµCT datasets generated and analysed in this study are available in the MorphoSource repository: www.morphosource.org/projects/00000C428. Further data including the cementum increments (images and histograms) and data for body mass scaling relationships are outlined in the Supplementary Information and available at Figshare (https://doi.org/10.6084/m9.figshare.25341508)74.

Code availability

We use Supplementary R code in R studio for our analyses, adapting existing packages and code. No new packages were developed for this study. Supplementary R code scripts are included and available at Figshare (https://doi.org/10.6084/m9.figshare.25341508)74.

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Acknowledgements

E.P. was funded by the Leverhulme Trust, the University of Oxford’s John Fell Fund and Linacre College’s EPA Cephalosporin Fellowship. Some of the scans of NMS G.1992.47.124 and NMS G.1992.47.122.1 were undertaken while E.P. was funded by the Natural Environment Research Council (NE/L002558/1). We thank K. Smithson and T. Davies for assistance with CT scanning and E. Griffiths, A.-M. Serra and S. Wright for segmenting scan data of extant mammal limb bones. We also thank R. Asher, Y. Candela, M. Day and Z. Timmons for loan of specimens and T. Davies, N. M. Morales García, P. Gill and J. Schultz for their assistance obtaining scan data. We acknowledge the European Synchrotron Radiation Facility (ESRF) and the Swiss Light Source at the Paul Scherrer Institute for provision of synchrotron radiation facilities and we would like to thank the beamline staff for assistance and support in using beamline ID19 (ESRF proposal ES587) and TOMCAT (proposal 20182126). We are grateful to N. Brocklehurst for assistance with R coding. We would like to thank NatureScot and the John Muir Trust for permission to work on the Elgol Coast SSSI and NCO and the fieldwork teams for their work. All fieldwork has been carried out in adherence to The Scottish Fossil Code.

Author information

Authors and Affiliations

  1. Natural Sciences Department, National Museums Scotland, Edinburgh, UK

    Elsa Panciroli, Nicholas C. Fraser & Stig Walsh

  2. University of Oxford Museum of Natural History, Oxford, UK

    Elsa Panciroli

  3. American Museum of Natural History, New York, NY, USA

    Roger B. J. Benson

  4. European Synchrotron Radiation Facility, Grenoble, France

    Vincent Fernandez

  5. Northern Rogue Studios, Inverness, UK

    Matt Humpage

  6. University of Chicago, Chicago, IL, USA

    Zhe-Xi Luo

  7. School of Engineering and Material Science, Queen Mary University of London, London, UK

    Elis Newham

  8. Section Palaeontology, Institute of Geosciences, Rheinische Friedrich-Wilhelms-Universität Bonn, Bonn, Germany

    Elis Newham

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  1. Elsa Panciroli
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Contributions

E.P. was principle investigator. E.P., R.B., S.W., N.F. and Z.-X.L. contributed to the conception and design of the overall project. E.P., R.B. and E.N. contributed to design of methodology. S.W. and N.F. provided access to specimens and logistical support. E.P., R.B. and S.W. carried out fieldwork. E.P., R.B., V.F., E.N. and S.W. collected micro-CT and synchrotron CT data. E.P. carried out digital segmentation, data collection and histological analysis and life history calculations. E.N. carried out further cementum analysis. R.B. carried out body mass calculations. E.P. and M.H. carried out digital reconstruction, visualization and figure preparation. E.P. led manuscript preparation and writing and all authors contributed to editing the manuscript.

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Correspondence to Elsa Panciroli.

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Extended data figures and tables

Extended Data Fig. 1 Molar morphology in Krusatodon kirtlingtonensis.

All digital renderings except for diagrammatic outlines and g (photograph). a-f, holotype lower right molar NHMUK PV M.46526 in: a, lingual; b, labial; c, occlusal; d, diagrammatic occlusal; e, posterior; f, anterior view. g-h NHMUK PV M.46437 upper left molar (M3) in: g, occlusal; h diagrammatic occlusal views. i-k, adult NMS. G.1992.47.122.1: I, lower m2 in lingual view; j and occlusal view; k, upper molar row occlusal view. l-n, juvenile NMS G.2023.8.1: l, lower left molar tooth row plus dp5 occlusal view; m and lingual view. n, upper right molar tooth row plus dP5 in occlusal view. o-p, mirrored versions of D and H to facilitate comparison. q, results of phylogenetic analysis for Docodonta including new scores for Krusatodon. a-f same scale, g-h same scale, i-k same scale, l-n same scale. All scale bars = 1 mm.

Extended Data Fig. 2 Reconstructed skull of Krusatodon kirtlingtonensis.

a-d, NMS. G.1992.47.122.1; e-f, NMS G.2023.8.1. a and e, left lateral view of digitally rendered skull elements, placed in anatomically correct positions. b-d and f, diagrammatic reconstructions of skull in: b and f, left lateral; c, anterior/rostral; d, posterior/caudal views. g, anterior portion of skull showing extent of elements with dotted lines. h, simplified diagram of teeth showing replacement stage in NMS G.2023.8.1. Scale bar same for a-f = 10 mm. Scale bar for g = 5 mm.

Extended Data Fig. 3 Dentaries and maxillae of adult Krusatodon kirtlingtonensis NMS. G.1992.47.122.1.

a, left dentary in medial view; b, left dentary of juvenile NMS G.2023.8.1 in medial view for comparison; c, left dentary in lateral view; d, location of dental cementum data for i1-c in specimen NMS G.1992.47.124, locations marked with yellow boxes, numbers correspond to Supplementary Table 8 and Supplementary Files; e, right dentary in lateral view; f, partially reconstructed dentaries in occlusal view; g, left maxilla in lateral view; h, right maxilla in lateral; i and medial views; j, partial reconstruction of the maxillae in occlusal view. Scale same for a-f and for g-j. All scale bars = 10 mm.

Extended Data Fig. 4 Dentaries of juvenile Krusatodon kirtlingtonensis NMS G.2023.8.1.

a-c, left dentary and teeth: a, lower tooth row in medial view showing deciduous (orange) and permanent generations; b, medial; c, lateral views. d-f, right dentary and teeth: d, lateral; e, medial views; f, lower tooth row in medial view showing deciduous (orange) and permanent generations. g, partially reconstructed dentaries in occlusal view. h, diagrammatic reconstruction of postdentary bones. Arrows indicate anterior direction. Scale bar same for b-e and g = 10 mm. Scale bar for a and f = 5 mm.

Extended Data Fig. 5 Maxillae and premaxillae of juvenile Krusatodon kirtlingtonensis NMS G.2023.8.1.

a-c, left maxilla and premaxilla: a, upper tooth row in lateral view showing deciduous (orange) and permanent generations; b, lateral; c and occlusal views. d-f, right maxilla and premaxilla: d, occlusal; e and lateral views; f, upper tooth row in lateral view showing deciduous (orange) and permanent generations. g, partial reconstruction of maxillae and premaxillae in occlusal view. Arrows indicate anterior direction. Scale bar same in b-e and g = 10 mm. Scale bars in a and f = 5 mm.

Extended Data Fig. 6 Postcranial skeleton of Krusatodon kirtlingtonensis.

a-b, e-f, g, i-j, l, n and p, adult NMS. G.1992.47.122.1. c-d, h, k and m, juvenile NMS G.2023.8.1. a, right clavicle; b, manubria; c, sacrum in dorsal view; d, sacrum in ventral view; e, left femur in posterior view; f, left femur in lateral view. g-h, left humeri in anterior view; i, left radius; j-k, left ulnae in anterior view; l, right pelvic girdle in lateral view; m, posterior of the right ilium in lateral view; n, left tibia in medial view; o, distal tibia in Eucosmodon adapted from Yuan et al. (2013); p, distal tibia showing condyles. Scale same for i-k. Scale bars a-d and l-k = 5 mm. All other scale bars = 10 mm.

Extended Data Fig. 7 Manus and pes of Krusatodon kirtlingtonensis NMS. G.1992.47.122.1.

a, speculative reconstruction using preserved elements of right manus; b, speculative reconstruction using preserved elements of right pes, mirrored calcaneus in paler green. Only named elements have confident identifications, so all placements for other elements are speculative. c-f, left calcaneus in: c, dorsal; d, lateral; e, ventral; f and medial views. g, example of ungual (position unknown); h-i, os calcaris; j, os calcaris in Gobiconodon, adapted from Hurum et al (2006). k-m, right astragalus in: k, dorsal; l, lateral; m and ventral views. Scale same for a-b = 10 mm. Scale same for c-g and k-l = 5 mm. Scale in h-i = 5 mm. Scale in j = 10 mm.

Extended Data Fig. 8 Evolution of the mammaliaform procoracoid.

a, the addition of information from Krusatodon suggests two independent losses of the procoracoid: once in Docodonta and later in stem therians; b, an alternative hypothesis for shoulder evolution requires three homoplasies; c, incomplete scapulacoracoid of juvenile Krusatodon NMS G.2023.8.1; d, scapulacoracoid in adult Krusatodon NMS. G.1992.47.122.1; e, diagrammatic reconstruction of the pectoral girdle.

Extended Data Fig. 9 Location of histological sections in the left tooth rows of juvenile Krusatodon NMS G.2023.8.1, indicated by yellow rectangles.

a, left upper tooth row with loci labelled; b, left upper tooth row with locations of histological sections; c, left lower tooth row with locations of histological sections; d, left lower tooth row with loci labelled. Names of sections correspond to Supplementary Files. See Figs. 3–4 in main paper and Supplementary Table 8 for cementum increment pair counts.

Extended Data Fig. 10 Location of histological sections in the right tooth rows of juvenile Krusatodon NMS G.2023.8.1, indicated by yellow rectangles.

a, right upper tooth row with loci labelled; b, right upper tooth row with locations of histological sections; c, right lower tooth row with locations of histological sections; d, right lower tooth row with loci labelled. Sections obtained using synchrotron tomographic imaging. Names of sections correspond to Supplementary Files. See Figs. 3–4 in main paper and Supplementary Table 8 for cementum increment pair counts.

Supplementary information

Supplementary Information

Details of the methods used for body mass estimations for K. kirtlingtonensis, using dataset of 158 species, spanning 4.0 g to 130 kg adult body mass. Systematic section, including updated referred material and diagnosis for K. kirtlingtonensis. Full anatomical description of the crania and postcrania of Krusatodon. Updated phylogenetic analysis based on ref. 47, incorporating character scores for K. kirtlingtonensis. Summary of changes to existing character scores in the matrix. Details of new information on the loss of the procoracoid in Mammaliaformes based on its presence in NMS G.2023.8.1 and NMS G.1992.47.122.1. Explanation of the methods used to determine the annual cementum deposition in the dentition of NMS G.2023.8.1 and NMS G.1992.47.122.1, using PPC-SRµCT. Code used in analyses of body size against postcanine dentition, percentage of postcanine eruption at weaning, body mass against age and birth, weaning and adult mass and body mass scaling relationships. Also available on Figshare: https://doi.org/10.6084/m9.figshare.25341508. This file also contains Supplementary Tables 3–8 and references.

Reporting Summary

Supplementary Table 1

Supplementary Table 2

R code

Codes used in analyses; adapted from existing packages.

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Panciroli, E., Benson, R.B.J., Fernandez, V. et al. Jurassic fossil juvenile reveals prolonged life history in early mammals. Nature 632, 815–822 (2024). https://doi.org/10.1038/s41586-024-07733-1

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