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The origin of placental mammal life histories

Abstract

After the end-Cretaceous extinction, placental mammals quickly diversified1, occupied key ecological niches2,3 and increased in size4,5, but this last was not true of other therians6. The uniquely extended gestation of placental young7 may have factored into their success and size increase8, but reproduction style in early placentals remains unknown. Here we present the earliest record of a placental life history using palaeohistology and geochemistry, in a 62 million-year-old pantodont, the clade including the first mammals to achieve truly large body sizes. We extend the application of dental trace element mapping9,10 by 60 million years, identifying chemical markers of birth and weaning, and calibrate these to a daily record of growth in the dentition. A long gestation (approximately 7 months), rapid dental development and short suckling interval (approximately 30–75 days) show that Pantolambda bathmodon was highly precocial, unlike non-placental mammals and known Mesozoic precursors. These results demonstrate that P. bathmodon reproduced like a placental and lived at a fast pace for its body size. Assuming that P. bathmodon reflects close placental relatives, our findings suggest that the ability to produce well-developed, precocial young was established early in placental evolution, and that larger neonate sizes were a possible mechanism for rapid size increase in early placentals.

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Fig. 1: Palaeohistology of P. bathmodon.
Fig. 2: Trace element distributions in the enamel of the first and second lower molars (NMMNH P-19541).
Fig. 3: Comparison of the reconstructed life history of P. bathmodon to extant mammals using the PanTHERIA dataset50.

Data availability

Fossil specimens in this study are housed at the NMMNH, and the palaeohistological thin sections underlying the analyses are accessioned at the University of Edinburgh but will be returned to the NMMNH for permanent curation upon completion of our research. The living mammal datasets are available from Jones et al.50 (https://doi.org/10.6084/m9.figshare.c.3301274.v1) and Newham et al.34 (https://www.nature.com/articles/s41467-020-18898-4#Sec18). Overview images of palaeohistological slides and LA–ICP–MS data are deposited at Figshare (https://doi.org/10.6084/m9.figshare.20272737). Source data are provided with this paper.

Code availability

No custom code or software was used in the study.

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Acknowledgements

We thank N. Volden for facilitating specimen access, J. Craven for access to microscopy facilities and A. Reynolds for discussion of captive lifespan. Funding was provided by the University of Edinburgh, the Royal Society (grant NIF\R1\191527), National Science Foundation (grants DEB 1654949 and EAR 1654952), European Research Council (ERC) starting grants (nos. 756226 and 805246) under the European Union’s Horizon 2020 Research and Innovation Programme, a Philip Leverhulme Prize and a SNSF Mobility Fellowship (grant P2EZP2_199923).

Author information

Authors and Affiliations

Authors

Contributions

G.F.F. designed the study, made the thin sections, conducted the histological, life history and statistical analyses, prepared the figures and wrote the manuscript. P.E.d. contributed to the study design, identification of the material, morphological analyses and drafting the manuscript. J.T.S. and M.D. conducted the LA–ICP–MS analyses at STAiG and contributed to figures and drafting the manuscript. S.L.S. created the skeletal reconstruction of P. bathmodon and contributed to discussion and drafting the manuscript. L.E.P. conducted the LA–ICP–MS analyses at the University of Edinburgh and contributed to drafting the manuscript. N.J.C. conducted the scanning electron microscopy analyses. J.R.W. contributed to drafting the manuscript. T.E.W. oversaw the collection and curation of the material, provided stratigraphic data and contributed to drafting the manuscript. J.W.B.R. supervised the LA–ICP–MS analyses. S.L.B. coordinated the project and contributed to study design and drafting the manuscript.

Corresponding authors

Correspondence to Gregory F. Funston or Stephen L. Brusatte.

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The authors declare no competing interests.

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Nature thanks Renaud Joannes-Boyau, Tanya Smith and the other, anonymous, reviewer(s) for their contribution to the peer review of this work. Peer reviewer reports are available.

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Extended data figures and tables

Extended Data Fig. 1 Incremental features of the teeth of Pantolambda bathmodon.

(a) Overview of coronal section of deciduous ultimate upper premolar of NMMNH P-27844 under plane-polarized light (left) and cross-polarized light with a lambda filter (right), showing locations of inset images. (b,c) Photomontages of the protocone exposed for the enamel (b) and the dentine (c), showing excellent preservation of incremental features, neonatal line (dashed line), and locations of close-up images. (d) Contrast-enhanced close-up of lines of von Ebner preserved in the dentine (arrows), extending parallel to the dentinoenamel junction and perpendicular to dentine tubules, and neonatal line (large arrow). (e) Contrast-enhanced close-up of enamel cross-striations and daily laminations (arrows) in the enamel, extending sub-parallel to the dentinoenamel junction and perpendicular to the enamel prisms. Images in b–e are under cross-polarized light. Abbreviations: NNL, neonatal line. Scale bars: 1 mm (a), 200 µm (b, c), 100 µm (d, e).

Extended Data Fig. 2 Zn-enrichment of the neonatal line in the enamel of lower second molar of NMMNH P-19541.

(a, c) coronal sections of enamel of paraconid (a) and protoconid (c) under cross-polarized light. Insets show location on coronal sections of entire tooth. (b, d), LA-ICP-MS trace element maps, showing higher concentrations of Zn in discrete areas corresponding to the neonatal line (white arrows). Abbreviations: DEJ, dentinoenamel junction; NNL, neonatal line; OES, outer enamel surface. Scale bars: 1 mm (insets), 100 µm (a–d).

Extended Data Fig. 3 Microwear on the dentition of NMMNH P-27844.

(a) Right maxilla with three deciduous premolars and adult first molar in occlusal view, showing location of scanning electron microscopy (SEM) scan. (b) Overview secondary electron (SE) image of protocone of adult first molar, showing development of mesowear and location of close-up image. (c) Close-up SE image of scratches and gouges attributable to abrasive microwear; black arrows highlight curved scratches resulting from chewing motion. White arrows in (a) and (b) indicate lingual direction. Abbreviations: d, deciduous; M, upper molar; P, upper premolar.

Extended Data Fig. 4 Changes in zinc associated with birth in the deciduous upper premolars of NMMNH P-27844.

Postnatal dentine is enriched in Zn in the deciduous upper ultimate premolar (a, b) and the deciduous upper second premolar (c, d). (a) Overview of thin section showing location of close-up image. (b) Mosaic image showing protocone in cross-polarized light, with trace element map overlain, showing change at histologically-inferred neonatal line (dashed line; NNL). (c) Overview image of embedded block showing location of trace element map. (d) Trace element map showing increased postnatal Zn. Scale bars: 1 mm (a, c), 500 µm (b, d). Abbreviations: NNL, neonatal line.

Extended Data Fig. 5 Dental wear, cementum annulations, and maximum lifespan in the oldest sampled individuals.

(a) Right first upper molar of NMMNH P-19625, showing extensive wear and erosion of enamel in most areas of the crown. (b) Anterior root of lower molar (tooth position unknown) from another individual of NMMNH P-19625, showing the location of the thin sections. (c) Overview transverse section of cervical root area, showing clear demarcation of cementum and dentine, and location of close-up. (d) Close-up of acellular extrinsic-fiber cementum in transverse section, showing six pairs of dark and bright bands comprising annual growth layer groups and alteration of external cementum; bright bands indicated with blue arrows. (e) longitudinal section of the same tooth, showing thick external layer of cementum, continuity of growth layer groups, and location of close-up. (f) close-up image of acellular extrinsic-fiber cementum in longitudinal section, showings six annual growth layer groups and alteration of external cementum; bright bands indicated with orange arrows. Images c–f under cross-polarized light. Scale bars: 1 mm (a–c, e), 200 µm (d, f).

Extended Data Fig. 6 Weaning transition recorded in the postcranial bones of NMMNH P-27844.

(a) Transverse section of right humerus diaphysis under cross-polarized light, showing arrangement of tissues and large medullary cavity and location of close-up image. (b) Close-up of cortex of right humerus under cross-polarized light, showing increase in proportion of parallel-fibered bone (brighter tissues) later in growth (arrow), indicative of a decrease in growth rate. (c) Transverse section of right tibia diaphysis under plane polarized light, showing location of close-up image. (d) Close-up of cortex of right tibia under cross-polarized light with a lambda filter, showing transition (arrow) from highly-vascularized fibrolamellar bone with a high proportion of woven-fibered matrix (upper right) to more slowly-growing parallel-fibered bone with reduced vascularity (lower left). (e) Transverse section of right radius diaphysis under cross-polarized light, showing location of close-up image. (f) Close-up image of cortex of right radius under cross-polarized light with a lambda filter, showing annulus of parallel-fibered bone (arrow) separating region of highly-vascularized fibrolamellar bone (lower right) from region of less-vascularized fibrolamellar bone with a higher proportion of parallel-fibered bone (upper left). Scale bars: 1 mm (a, c, e), 500 µm (b, d, f).

Extended Data Fig. 7 Transition to slower growth likely reflecting sexual maturity.

(a) Coronal section of posterior dentary of NMMNH P-22012 under cross-polarized light with a lambda filter, showing locations of close-up images. Dark regions have been diagenetically altered by the deposition of opaque minerals. (b, c) Close-up of transition (dashed line) between faster-growing fibrolamellar bone (flb) and slower-growing lamellar bone (lb), indicative of sexual maturity, under cross-polarized light (b) and cross-polarized light with a lambda filter (c). Arrows indicate first line of arrested growth, deposited after the transition to slower growth. Scale bars: 1 mm (a), 200 µm (b, c).

Extended Data Fig. 8 Life history of P. bathmodon compared to living mammals.

(a, b) principal components analyses using the PanTHERIA dataset (placentals, green; marsupials, blue; monotremes, purple) incorporating suckling interval, gestation period, maximum lifespan, and age at sexual maturity, with adult body mass excluded (a) or included (b) as a variable; close living analogues to P. bathmodon indicated by silhouettes. (c–f) regressions of life history variables in placental mammals with 95% confidence intervals (thin black lines) centred on the generalized linear model regression trendline for suckling interval (c), gestation period (d), maximum lifespan (e), and age at sexual maturity (f), showing that P. bathmodon is within the 95% confidence interval of placentals in all parameters. Silhouette of Pantolambda bathmodon created by SLS. Silhouettes of Orycteropus and Priodontes adapted from Phylopic images (CC0 1.0 https://creativecommons.org/publicdomain/zero/1.0/), silhouette of Leptonychotes is original artwork by GFF, silhouette of Phoca was generated from a photograph taken by GFF, and all others were generated from public domain images (CC0 1.0 https://creativecommons.org/publicdomain/zero/1.0/).

Extended Data Fig. 9 Relationship between neonate mass and adult body mass in extant mammals.

(a) Generalized linear model regression of neonate body mass against adult body mass for all species in the PanTheria dataset, showing clear separation of placental mammals (green, p-value < 2.2x10−16) from non-placental mammals (p-value: 4.07x10−6); 95% confidence interval for regression slope shown as shaded envelope. (b) Neonate body mass plotted against adult body mass for placental species, showing tight correlations of neonate mass and adult mass (p values both < 2.2x10−16); 95% confidence interval for generalized linear model regression slope shown as shaded envelope. (c) Gestation period plotted against neonate body mass; 95% confidence interval for generalized linear regression slope shown as shaded envelope. (d) Relative importance of multiple regression of adult body mass against neonate weight, gestation period, maximum lifespan, time to sexual maturity, and suckling period, showing relative contribution of factors to adult body mass; confidence intervals derived from 1000 replicates of bootstrapping.

Extended Data Table 1 Quantitative dental histological data for Pantolambda bathmodon

Supplementary information

Supplementary Information

This file contains supplemental text including methodological details, results and discussion. It includes two Tables and eight Figures. The tables show specimen cataloguing information and geochemical analysis parameters. The figures show the trace element maps for each sample and an idealized diagram of expected barium distributions in mammalian enamel.

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Funston, G.F., dePolo, P.E., Sliwinski, J.T. et al. The origin of placental mammal life histories. Nature 610, 107–111 (2022). https://doi.org/10.1038/s41586-022-05150-w

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