Teeth, prenatal growth rates, and the evolution of human-like pregnancy in later Homo

Abstract

Evidence of how gestational parameters evolved is essential to understanding this fundamental stage of human life. Until now, these data seemed elusive given the skeletal bias of the fossil record. We demonstrate that dentition provides a window into the life of neonates. Teeth begin to form in utero and are intimately associated with gestational development. We measured the molar dentition for 608 catarrhine primates and collected data on prenatal growth rate (PGR) and endocranial volume (ECV) for 19 primate genera from the literature. We found that PGR and ECV are highly correlated (R² = 0.93, P < 0.001). Additionally, we demonstrated that molar proportions are significantly correlated with PGR (P = 0.004) and log-transformed ECV (P = 0.001). From these correlations, we developed two methods for reconstructing PGR in the fossil record, one using ECV and one using molar proportions. Dental proportions reconstruct hominid ECV (R² = 0.81, P < 0.001), a result that can be extrapolated to PGR. As teeth dominate fossil assemblages, our findings greatly expand our ability to investigate life history in the fossil record. Fossil ECVs and dental measurements from 13 hominid species both support significantly increasing PGR throughout the terminal Miocene and Plio-Pleistocene, reflecting known evolutionary changes. Together with pelvic and endocranial morphology, reconstructed PGRs indicate the need for increasing maternal energetics during pregnancy over the last 6 million years, reaching a human-like PGR (i.e., more similar to humans than to other extant apes) and ECV in later Homo less than 1 million years ago.

Keywords: dentition; endocranial volume; hominid fossil record; maternal energetics; prenatal growth.

Fig. 1.

(A) PGR (g/day) is significantly correlated with log-transformed ECV in extant catarrhines (R² = 0.93, P < 0.001). (B) PGRs of fossil hominids, reconstructed from fossil ECV measurements, are plotted alongside extant catarrhines. Values were reconstructed via a linear regression model developed from extant data (Table 1). Homo sapiens are labeled with an asterisk, extant cercopithecids are labeled with a circle, extant nonhuman apes are labeled with a triangle, Ardipithecus is marked with a crossed circle, Australopithecus are marked with a crossed diamond, and nonhuman fossil Homo species are marked with a crossed square. Homo sapiens (North Africa) and (South Africa) are fossil samples. See SI Appendix, Figs. S3 and S4 for mandibular MMC results. See SI Appendix text for notes on morphospace clustering.

Fig. 2.

(A) PGRs (R² = 0.50, P < 0.004) and (B) log-transformed ECVs (R² = 0.57, P = 0.001) are significantly correlated with maxillary MMC in extant catarrhines. (C) PGRs of fossil hominids, reconstructed from molar proportions, are plotted alongside extant catarrhines. Values were reconstructed via a linear regression model developed from extant data (Table 1). (D) Figurative illustration of MMC in apes. Dashed red line on the third molar (M3) indicates where molar mesiodistal length is measured. Distal is to the Left, and mesial is to the Right. Homo sapiens are labeled with an asterisk, extant cercopithecids are labeled with a circle, extant nonhuman apes are labeled with a triangle, Ardipithecus is marked with a crossed circle, Australopithecus are marked with a crossed diamond, and nonhuman fossil Homo species are marked with a crossed square. Homo sapiens (North Africa) and (South Africa) are fossil samples. SI Appendix, Figs. S3 and S4 include mandibular MMC results.

Fig. 3.

Timeline of morphological, behavioral, and ecological changes in the hominid fossil record from terminal Miocene to present. The x-axis is geologic time in millions of years (Ma). The y-axes are parsed by variable. From Top to Bottom: (A) Predicted PGR, predicted via the linear regression model (for ECV) developed as part of the method published in this article. (B) ECV (in cubic centimeters) reconstructed from cranial fossil specimens [data from (77)]. (C) Maxillary MMC. (D) Soil carbonate δ¹³C (‰ Vienna Pee Dee Belemnite), sampled from paleosols in eastern African hominid-bearing areas. Stable isotope data (D) were obtained from (101); temporal shifts toward more positive (enriched) isotopic values on the y-axis indicate ecological transitions from C₃ to C₄ vegetation coinciding with climatological increases in aridity. Fossil species are plotted as averages with error bars to represent currently known first and last appearance dates (77, 97, 116, 117). Evolutionary changes in pelvic shape, ECV, and MMC are visualized through extremes (A–C, respectively). PGR is represented by fossil pelves from Australopithecus afarensis AL 288-1 and recent Homo sapiens [images adapted from (118)]. ECV is represented by Australopithecus anamensis MRD-VP-1/1 [image adapted from (116)] and Homo sapiens Skhul V [image adapted from (119)]. MMC is represented by a figurative visualization of dental proportions. Major changes in behavior are plotted on the x-axis at the top of the figure using illustrative images, representing the evolution of obligate bipedalism, use of Oldowan tools, and use of Acheulean tools [images and dates are adapted from (75)]. Figure legend includes fossil taxa and extant Homo sapiens. Fossil Homo sapiens are demarcated as North Africa and South Africa. Location refers to the sites where the soil carbonate isotopes were sampled. SI Appendix, Fig. S8 includes expanded figure that includes PGR predicted from MMC, and additional stable isotope data.