Diet and the evolution of the earliest human ancestors
Over the past decade, discussions of the evolution of the earliest human ancestors have focused on the locomotion of the australopithecines. Recent discoveries in a broad range of disciplines have raised important questions about the influence of ecological factors in early human evolution. Here we trace the cranial and dental traits of the early australopithecines through time, to show that between 4.4 million and 2.3 million years ago, the dietary capabilities of the earliest hominids changed dramatically, leaving them well suited for life in a variety of habitats and able to cope with significant changes in resource availability associated with long-term and short-term climatic fluctuations.
Impact of meat and Lower Palaeolithic food processing techniques on chewing in humans
The origins of the genus Homo are murky, but by H. erectus, bigger brains and bodies had evolved that, along with larger foraging ranges, would have increased the daily energetic requirements of hominins1,2. Yet H. erectus differs from earlier hominins in having relatively smaller teeth, reduced chewing muscles, weaker maximum bite force capabilities, and a relatively smaller gut3,4,5. This paradoxical combination of increased energy demands along with decreased masticatory and digestive capacities is hypothesized to have been made possible by adding meat to the diet6,7,8, by mechanically processing food using stone tools7,9,10, or by cooking11,12. Cooking, however, was apparently uncommon until 500,000 years ago13,14, and the effects of carnivory and Palaeolithic processing techniques on mastication are unknown. Here we report experiments that tested how Lower Palaeolithic processing technologies affect chewing force production and efficacy in humans consuming meat and underground storage organs (USOs). We find that if meat comprised one-third of the diet, the number of chewing cycles per year would have declined by nearly 2 million (a 13% reduction) and total masticatory force required would have declined by 15%. Furthermore, by simply slicing meat and pounding USOs, hominins would have improved their ability to chew meat into smaller particles by 41%, reduced the number of chews per year by another 5%, and decreased masticatory force requirements by an additional 12%. Although cooking has important benefits, it appears that selection for smaller masticatory features in Homo would have been initially made possible by the combination of using stone tools and eating meat.
Eating of meat allowed reduction of size in teeth, jawbone, and chewing muscles.
The australopithecines exhibited a complex of morphological features related to diet that are unique compared with living hominoids or Miocene apes. These early hominids all had small- to moderate-sized incisors; large, flat molars with little shear potential; a ratio of first to third molar area that was low compared with those of extant apes, but generally higher than those of Miocene apes; thick tooth enamel; and thick mandibular corpora. This suite of traits is distinctive of australopithecines and suggests a dietary shift at or near the stem of hominid evolution. Their thickenameled, flattened molars would have had great difficulty propagating cracks through tough foods, suggesting that the australopithecines were not well suited for eating tough fruits, leaves, or meat. The dental microwear data agree with this conclusion, as the australopithecine patterns documented to date are most similar to those of modern-day seed predators and soft fruit eaters. Furthermore, given their comparatively small incisors, these hominids probably did not specialize in large, husked fruits or those requiring extensive incisal preparation. Instead, the australopithecines would have easily been able to break down hard, brittle foods. Their large flat molars would have served well for crushing, and their thick enamel would have withstood abrasion and fracture. Their mandibular corpora would probably have conferred an advantage for resisting failure, given high occlusal loads. In essence, for much of their history, the australopithecines had an adaptive package that allowed them ready access to hard objects, plus soft foods that were not particularly tough. The early hominids could also have eaten both abrasive and nonabrasive foods. This ability to eat both hard and soft foods, plus abrasive and nonabrasive foods, would have left the early hominids particularly well suited for life in a variety of habitats, ranging from gallery forest to open savanna. Fig. 5. Mandibular corpus shape (data from refs. 75, 76, and 85 and M. Leakey, personal communication).
Does this mean we can talk of a characteristic ‘‘australopithecine’’ dietary pattern? Perhaps to some extent, but although the australopithecines shared many features in common, they also differed from one another, suggesting a change in diet through time. Such morphological changes occurred as a mosaic, much as that seen for locomotor anatomy. Much of the evidence for Ardipithecus ramidus is not yet available, but despite its thin molar enamel and absolutely smaller teeth than those of later hominids, it shows molar size proportions that may hint at dietary changes to come. A. anamensis shows the first indications of thicker molar enamel in a hominid, and its molar teeth were equivalent in size to those of A. afarensis. Still, its mandibular corpus is intermediate in robusticity between those of living great apes and later australopithecines. This combination of features suggests that A. anamensis might have been the first hominid to be able to effectively withstand the functional demands of hard and perhaps abrasive objects in its diet, whether or not such items were frequently eaten or were only an important occasional food source. A. afarensis was similar to A. anamensis in relative tooth sizes and probably enamel thickness, yet it did show a large increase in mandibular robusticity. This increase may be due to changes in peak force magnitude or degree of repetitive loading in mastication. Either way, hard and perhaps abrasive foods may have become even more important components of the diet of A. afarensis. A. africanus shows yet another increase in postcanine tooth size, which by itself would suggest an increase in the sizes and abrasiveness of foods. However, its molar microwear does not show the degree of pitting one might expect from a classic hard-object feeder. Thus, even A. africanus has evidently not begun to specialize in hard objects, but rather has emphasized dietary breadth. In contrast, subsequent ‘‘robust’’ australopithecines do show hard-object microwear and craniodental specializations, suggesting a substantial departure in feeding adaptive strategies early in the Pleistocene. In sum, diet was probably an important factor in the origin and early evolution of our family. The earliest australopithecines show a unique suite of diet-related features unlike those of Miocene apes or living hominoids. Such features suggest that the earliest hominids may have begun to experiment with harder, more brittle foods at the expense of softer, tougher ones early on. This does not mean that all of the australopithecines were specialized hard-object feeders. It merely means that, through time, they acquired the ability to feed on hard objects. Many modern primates need to consume critical ‘‘fall-back foods’’ at certain times of the year (6), and it may well be that the earliest australopithecines resorted to the consumption of hard objects only in such situations, whereas the robust australopithecines relied on them far more regularly. Another important aspect of early hominid trophic adaptations is evident from data presented here—the dietary shift from apes to early hominids did not involve an increase in the consumption of tough foods, and so the australopithecines were not preadapted for eating meat. This conclusion runs counter to (i) recent isotope work suggesting that the australopithecines did in fact consume significant amounts of meat (7) and (ii) nutritional work suggesting that meat may have provided critical nutrients for both young and old hominids (77–79). There would seem to be three different ways to reconcile these perspectives. First, the present study has reviewed only craniodental features related to diet. If the australopithecines used other means for ingesting and processing meat (e.g., tools), they might have been able to process meat more efficiently than the craniodental evidence suggests (80, 81). Second, the heavy C3 signature found in A. africanus (7) may reflect the consumption of underground storage organs of C3 plants rather than meat (82). Third, the functional analyses of the teeth assume that all meat has the same degree of toughness. This may not be the case. Studies of the physical properties of food have thus far focused on plant remains, with only brief mention of the toughness of materials like skin (40, 46). Variations in toughness between animal tissues might well be due to variations in the arrangement and density of collagen matrix. Furthermore, the physical effects of decomposition might render meat less tough and more readily processed by hominids. If this is so, it could be further evidence in support of scavenging as part of the early hominid way of life. Investigators have tried to relate patterns of hominid evolution to patterns of climatic change for some time (3, 4). The focus of much of the recent work has been on the origin of the genus Homo. Can the dietary shifts in the earliest hominids also be tied to such changes? Whereas there is some evidence of large-scale climatic changes around the Mediterranean (83) and unusual faunal turnover in parts of western Asia (84), there are no large-scale changes evident in sub-Saharan Africa until after the earliest hominids have arrived on the scene (i.e., not until 1.5–2.5 million years ago). There is the slow and inexorable cooling and drying of the Miocene, but perhaps the crucial result of this was an increase in microhabitat variability. Certainly, there are limits to our paleoecological evidence from this period, but as Potts (4) has noted, ‘‘in general, the oldest hominids were associated with a diverse range of habitats.’’ These included lake and river margins, woodland, bushland, and savanna. Potts (4) has emphasized that locomotor versatility was a crucial adaptation of the earliest hominids in the face of such varied environmental conditions. We feel that this perspective needs to be extended to the dietary adaptations of the earliest hominids as well. In such a land of variable opportunities, the generalized craniodental toolkit of the earliest hominids may have had a distinct advantage, as it allowed our forbears the flexibility to cope with short-term and long-term climatic variations and the resultant changes in resource availability.
Because the mechanical properties of foods vary depending on many factors such as species and type of portion consumed, further research is necessary to examine additional foods and processing techniques important to human evolution. More research is also needed to quantify the impacts of variations in masticatory morphology on chewing efficiency because dental topography and facial shape affect the relationship between food fracture and chewing effort (for example, sharper cusps increase applied chewing stresses, and relatively shorter jaws increase the mechanical advantage of the adductor muscles). Even so, we speculate that despite the many benefits of cooking for reducing endogenous bacteria and parasites29, and increasing energy yields23,24, the reductions in jaw muscle and dental size that evolved by H. erectus did not require cooking and would have been made possible by the combined effects of eating meat and mechanically processing both meat and USOs. Specifically, by eating a diet composed of one-third meat, and slicing the meat and pounding the USOs with stone tools before ingestion, early Homo would have needed to chew 17% less often and 26% less forcefully. We further surmise that meat eating was largely dependent on mechanical processing made possible by the invention of slicing technology. Meat requires less masticatory force to chew per calorie than the sorts of generally tough plant foods available to early hominins, but the ineffectiveness of hominin molars to break raw meat would have limited the benefits of consuming meat before the invention of stone tools approximately 3.3 Ma. Although recent and contemporary hunter–gatherers are less dependent on stone tools than early Homo because they eat mostly cooked meat, many of the oldest tools bear traces of being used to slice meat9, and the use of tools (now mostly metal knives) to process foods such as meat is well documented ethnographically30. This dependency on extra-oral mechanical processing, however, does not apply to other animal-based foods such as marrow, brains and visceral organs that might have been difficult to access without tools, but are easier to chew than muscle. Although it is possible that the masticatory benefits of food processing and carnivory favoured selection for smaller teeth and jaws in Homo, we think it is more likely that tool use and meat-eating reduced selection to maintain robust masticatory anatomy, thus permitting selection to decrease facial and dental size for other functions such as speech production, locomotion, thermoregulation, or perhaps even changes in the size and shape of the brain16. Whatever selection pressures favoured these shifts, however, they would not have been possible without increased meat consumption combined with food processing technology.
The shift from fibrous plants to including animal source foods, together with the use of tools, paralleled a decrease in teeth size and jawbones, a reduction in chewing muscles, and weaker maximum bite force capabilities [Teaford & Ungar 2000; Zink & Lieberman 2016]. Homo molars gained steeper slopes and more relief, also suggestive to an adaptation to meat eating [Ungar 2004].