Barium distributions in teeth reveal early-life dietary transitions in primates

Abstract

Early-life dietary transitions reflect fundamental aspects of primate evolution and are important determinants of health in contemporary human populations. Weaning is critical to developmental and reproductive rates; early weaning can have detrimental health effects but enables shorter inter-birth intervals, which influences population growth. Uncovering early-life dietary history in fossils is hampered by the absence of prospectively validated biomarkers that are not modified during fossilization. Here we show that large dietary shifts in early life manifest as compositional variations in dental tissues. Teeth from human children and captive macaques, with prospectively recorded diet histories, demonstrate that barium (Ba) distributions accurately reflect dietary transitions from the introduction of mother's milk through the weaning process. We also document dietary transitions in a Middle Palaeolithic juvenile Neanderthal, which shows a pattern of exclusive breastfeeding for seven months, followed by seven months of supplementation. After this point, Ba levels in enamel returned to baseline prenatal levels, indicating an abrupt cessation of breastfeeding at 1.2 years of age. Integration of Ba spatial distributions and histological mapping of tooth formation enables novel studies of the evolution of human life history, dietary ontogeny in wild primates, and human health investigations through accurate reconstructions of breastfeeding history.

Figure 1. Barium distribution in human deciduous teeth

(a) Ba/Ca map of incisor. Dentine horn indicated by arrowhead. (b) Area highlighted in a and polarized light micrograph. In dentine (D), Ba/Ca levels show marked increase coinciding with the neonatal line (white arrowheads). Neonatal line in enamel (E) is indicated by black arrowheads and EDJ by arrows. (c) Ba/Ca measured adjacent to EDJ from dentine horn to cervix of a, which rose at birth and with introduction of infant formula (21–24 d). X-axis shows days since birth (B). (d–f) Three diet patterns: (d) breastfeeding for 3 months (dotted white line) followed by exclusive formula-feeding (solid black line), (e) formula introduced within 1 week of birth (solid black line), and (f) exclusive breastfeeding (dotted white line). Neonatal line indicated by dashed white line. Intensity indices are Ba/Ca × 10⁻⁴. High Ba/Ca adjacent to pulp (red zone) are in secondary dentine, a later-forming region not relevant to the current study (see Kohn et al.).

Figure 2. Barium distribution reveals natural and truncated weaning

(a) Macaque 515: natural weaning after 296 d. (b) Macaque 152: weaned slightly early due to maternal separation at 257 d. (c) Macaque 401: markedly truncated weaning due to maternal separation at 166 d. This individual’s weight fluctuated during final seven months of life due to illness; post-weaning enrichment may be due to release from skeletal stores. Diet transitions: prenatal regions (arrowhead), exclusive mothers’ milk (MM), transitional (T) periods, and post-weaning regions delineated in enamel (dotted lines) and dentine (black arrows). EDJ indicated with dashed line. Y-axis shows enamel Ba/Ca adjacent to EDJ. X-axis shows days since birth (B) and weaning (red line). Elemental maps of dentine and enamel were rendered on different scales to clearly show Ba/Ca transitions. The colour scale only reflects Ba/Ca variations within the dentine or enamel of a tooth.

Figure 3. Dietary transitions in a Neanderthal permanent first molar

(a) Developmental time (in days from birth) of stress lines in enamel (dark blue lines) was determined from daily growth increments (following dotted blue lines). Scale bar = 1 mm. (b) Ba/Ca map shows marked variations in enamel at birth, 227 and 435 d, which resemble human and macaque transition from exclusive maternal milk (MM) consumption to supplementation. (c) Ba/Ca in enamel adjacent to EDJ. X-axis shows days from birth (B) to proposed exclusive MM, transitional diet (T) periods and hypothesized weaning event (red line). Elevated Ba/Ca levels at the very beginning and end of crown formation are likely due to subtle diagenetic modification.