Developmental stress in South African hominins: Comparison of recurrent enamel hypoplasias in Australopithecus africanus and Homo naledi

Abstract

Discovery of a new hominin (Homo naledi) in the same geographical area as Australopithecus africanus creates the opportunity to compare developmental dental stress in higher latitude hominins with low that in latitude apes, among whom repetitive linear enamel hypoplasia (rLEH) recurs seasonally at about 6 or 12 months. In contrast to equatorial Africa, a single rainy/dry cycle occurs annually in non-coastal southern Africa. It is predicted that LEH will recur annually but not differ in duration between ancient and more recent hominins. Data were collected from epoxy casts of anterior teeth attributed to H. naledi (18 incisors, 13 canines) and A. africanus (29 incisors, 8 canines) using a digital microscope, surface scanner and scanning electron microscope. The location, number, width, depth and distance between defects (including perikymata counts and spatial measurements) of 136 LEH events were compared among crown moieties (deciles 4-6 and 7-9), tooth types and taxa. Enamel defects are concentrated in the cervical half of anterior crowns, and in similar numbers in each taxon. Contrary to expectations, H. naledi show bimodal LEH durations reconstructed at about 2 and 8 weeks compared to just 4 weeks in A. africanus. Both taxa show bimodally recurrent episodes of LEH centring on 2 and, more commonly and severely, 6 months. A combination of two independent annual stressor types, one disease and one seasonal, could explain the observations. These estimations of duration and recurrence of developmental stress require evaluation using actual perikymata periodicity for H. naledi and more refined understanding of palaeoenvironments for both taxa. Significance:• Seasonal stress is a central concern in the biological and health sciences. Because of the innate way that enamel is deposited, the timing of stress in the childhood of apes, modern humans and their fossil ancestors can be measured with a precision of about 1 week.• Application of this method to South African Pliocene Australopithecus africanus and Mid-Pleistocene Homo naledi reveals that, unexpectedly, both forms show semi-annual stress -a finding that is tentatively attributed to two independent annual stressors, possibly disease and malnutrition.

3D enamel profilometry reveals faster growth but similar stress severity in Neanderthal versus Homo sapiens teeth

“…When compared with published defect depths from nonhuman great apes and hominins, the H. sapiens sample has the highest median depths (47.5 µm in mandibular canines), perhaps as a result of their slower average extension rates, larger striae of Retzius angles, and thicker enamel compared to apes 18 . The Neanderthal specimens, in contrast, have a median defect depth (30.3 µm) that is more similar to earlier hominins Australopithecus africanus (26.0 µm) and H. naledi (26.9 µm) as reported by Skinner 21 , as well as nonhuman apes (23.6 µm in mountain gorillas). However, the A. africanus and H. naledi depths 21 were collected from leveled DEMs and therefore likely underestimate the true depth, based on our comparisons of leveled vs. raw data (Fig.…”

“…The Neanderthal specimens, in contrast, have a median defect depth (30.3 µm) that is more similar to earlier hominins Australopithecus africanus (26.0 µm) and H. naledi (26.9 µm) as reported by Skinner 21 , as well as nonhuman apes (23.6 µm in mountain gorillas). However, the A. africanus and H. naledi depths 21 were collected from leveled DEMs and therefore likely underestimate the true depth, based on our comparisons of leveled vs. raw data (Fig. S2 ).…”

“…Previous work hypothesized that the relationship between enamel growth rates and defect depth exists among hominins as well 20 , with differences in depth, and thus perceptibility via qualitative observation, influencing estimates of LEH prevalence. However, no defect depths are published for Homo sapiens , and only one study currently exists on fossil hominins comparing Australopithecus africanus and H. naledi 21 . Therefore, very little is known about how defect depth might relate to enamel growth and life history patterns in our own species and extinct relatives.…”

“…Researchers have long hypothesized that defect depth provides information about the severity of the stressor that disrupted growth in hominoids 16 , 21 , 27 , just as location and width of the defects tell us something about their timing and duration, respectively. Evidence from great ape studies supports this, with several wild-captured individuals exhibiting particularly deep defects that might reflect major stress events 17 .…”

“…Further, flanged orangutans, which exhibit higher levels of the stress hormone cortisol throughout development, have defects that are more than twice as deep as unflanged or developmentally arrested males with either the same or lower cortisol levels 28 . The duration of the disruption is also likely to affect classic furrow-form defect dimensions, as is usually approximated by counting the number of perikymata involved in the defect, with each additional perikyma carving more deeply into the enamel wall 20 , 21 . At the cellular level, the number of affected enamel-secreting cells, as well as the relative timing of the growth disruption in relation to the life of the cells, affects the depth of the defect at the outer enamel surface 24 , 25 .…”