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The Evolution of Early Hominin Diet

Introduction

Diet is an essential part of the relationship between an organism and its environment

(Ungar 2012). For living primates, diet influences several facets of their lives, including

geographic range, body size, breeding strategy, and locomotion (Clement and Hillson 2013;

Ungar and Sponheimer 2011). Likewise, it was undoubtedly equally as important and

influential in the lives of our extinct hominin ancestors. Environmental changes, which often

alter available food resources and introduce new challenges, “have surely driven changes in

early hominin diets and with them the evolution of our genus” (Ungar 2012). In fact, major

changes in diet are often considered “key milestones” in hominin evolution (Ungar and

Sponheimer 2011). The change from a primarily plant-based diet to one with meat has often

been cited as a key motivation behind the transition to early Homo (Bunn 2006), although

others suggest the inclusion of underground storage organs was more important (O’Connell

et al. 2002; O’Connell et al. 1999; Ungar 2012). Still others suggest that the additional

preparation of food with tools and cooking was critical (Ungar 2012; Wrangham and

Conklin-Brittain 2003; Wrangham et al. 1999). Understanding how diet shifted between

Australopithecus, Paranthropus, and early Homo can illuminate some of the major driving

forces of human evolution.

Modeling major changes in the evolution of hominin diet can be done through the

examination of several lines of evidence, using both direct and indirect methods. However,

which methods are usable varies depending on the time period being studied, as well as the

archaeological and fossil evidence available. Archaeological remains, such as stone tools and

animal bones, can be used to estimate the diet of more recent hominins, however the earliest

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hominins are non-existent archaeologically. Their limited representation in the fossil record is

an additional problem. Fortunately, the parts of the skeleton most relevant to the study of diet,

teeth and jaws, are also the most likely tissue to fossilize (Lee–Thorp 2002). Dental tissues

are considerably more resistant than normal bone to chemical and physical degradation

(Clement and Hillson 2013; Lee–Thorp 2002). The size, shape, structure, and microwear

patterns of teeth are commonly examined to infer aspects of diet (Ungar 2012). Further

information can be gathered through stable isotope analyses and trace elements (Lee‐Thorp et

al. 2003; Sponheimer et al. 2013). Reconstructing paleoenvironments can also suggest what

types of food were available during the time periods and regions in which our hominin

ancestors lived (Alemseged and Bobe 2009). In this essay I will discuss the various lines of

evidence used to study and evaluate the diet of early hominins and how it evolved over time.

I will also discuss the dietary importance of plants and animal foods and how the

development of cooking influenced human evolution.

Lines of Evidence

Adaptive Evidence

Teeth are adapted to provide preliminary processing of food and for most mammals,

the morphology of their teeth is correlated with diet (Andrews et al. 1991). The abundance of

teeth in the hominin fossil record has allowed researchers to investigate the evolution of

hominin diet using several aspects of dental morphology including tooth size, tooth shape,

and enamel structure.

Incisor Size

For primates, there is a correlation between incisor size (relative to body or first molar

(M1) size) and type of diet. Frugivorous primates tend to have relatively large incisors, likely

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adapted for consuming large, husked fruits, while folivores tend to have relatively small

incisors, as they eat smaller objects that do not require large front teeth (Andrews et al. 1991;

Groves and Napier 1968; Hylander 1975; Teaford and Ungar 2000; Ungar 2012). In the

hominin lineage, Australopithecus taxa plot on or near the regression line for incisor

allometry in extant catarrhines (Figure 1), demonstrating a moderate incisor size, while

Paranthropus robustus plots below with a relatively small incisor. Relative incisor size

appears to then increase above the line with Homo habilis and Homo rudolfensis, followed by

a decrease back to the line in Homo erectus and then below it again with Homo sapiens. The

differences in incisor size suggests that there were notable shifts in diet related to incisor use,

however, it is important to note that sample sizes for each hominin species are extremely

small (n =1-2) and the body weight estimates are rough and uncertain (Teaford et al. 2002;

Ungar 2012).

Molar Size

Relative molar size has also been used as an indicator of diet, although the same

limitations in sample size and weight estimates still apply. In living primates, folivores have

longer molars than frugivores for most primate groups, however this is not the case in

cercopithecoids (Kay 1977; Vinyard and Hanna 2005) and in many primate species, there is a

significant difference in relative cheek teeth size between males and females (Harvey et al.

1978). Because the relationship between molar size and diet is inconsistent among living

primates, any conclusions drawn should be done cautiously. Several studies have shown an

increase in molar size (in both absolute surface area and megadontia quotient) throughout

time in the Australopithecus and Paranthropus taxa, followed by a reduction in Homo

(Figure 2) (McHenry and Coffing 2000; Teaford and Ungar 2000; Ungar 2012). The

significance of this change is unclear, although the enlarged cheek teeth and robust jaws of

the australopithecines are typically explained as an adaptation to processing large amounts of

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low-quality, hard foods, such as nuts and hard-shelled fruits (Ungar and Sponheimer 2011),

while the reduction in Homo could be the result of a relaxation in selection pressures due to

the introduction of tools and cooking (Ungar and Sponheimer 2011).

Tooth Morphology and Structure

The shape of primate teeth, in particular molar teeth, also reflects the fracture

properties of the food each species eats. For example, primates that eat tough leaves often

have more occlusal relief than those who typically eat hard objects and these relationships are

conserved with wear (Kay 1984; M'kirera and Ungar 2003; Meldrum and Kay 1997; Ungar

and M'kirera 2003). Occlusal morphology differences between hominins suggest that

Paranthropus consumed more hard-brittle food, while early Homo would have been better at

shearing tough items and Australopithecus falls somewhere in the middle (Bailey and Wood

2007; Teaford et al. 2002; Ungar 2007; Wood and Strait 2004). Tooth enamel thickness is

also argued to be an adaptation related to diet and food fracture properties. Thicker enamel

protects better against breakage, but thinner enamel wears quicker and provides a jagged

surface, beneficial for processing tough foods (Dumont 1995; Kay 1981; Ungar et al. 2006;

Ungar and M'kirera 2003).

Studies focusing on tooth size, shape, and structure offer important evidence about

fracture properties and masticatory stresses in early hominin diets, however their results can

be misleading (Ungar and Sponheimer 2011). They indicate the dietary adaptation and

phylogenetic history of each species and what they are capable of eating, but that does not

always match what specific individuals actually eat (Lee‐Thorp et al. 2003; Ungar and

Sponheimer 2011). Even extant primate taxa regularly eat food that does not match the

current morphology of their teeth (Lee‐Thorp et al. 2003). For more precise evidence of what

each fossil specimen ate, we need to use other methods.

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Non-Adaptive Evidence

Dental Microwear

Dental microwear, the study of microscopic wear on the surface of teeth, is one of the

best methods for reconstructing early hominin diets (Scott et al. 2005; Walker et al. 1978).

Scratches and pits appear on the surface of a tooth as a direct result of use and each mark is

representative of an actual chewing event (Ungar 2011; Ungar and Sponheimer 2011).

Different types of food leave behind different wear patterns. Hard, brittle foods (nuts, bones)

typically leave pit marks on the occlusal surface of teeth, while tough foods that require

shearing (leaves, meat) leave long, parallel striations (Figure 3) (Ungar 2010; Ungar and

Sponheimer 2011). Surface complexity corresponds to the hardness of food eaten (Figure 4)

(high complexity = heavy pitting) and the directionality (anisotropy) of the wear corresponds

to food toughness (high anisotropy = highly aligned scratches) (Ungar and Sponheimer 2011).

Studies of early hominin microwear (Scott et al. 2005; Ungar et al. 2008; Ungar et al.

2012; Ungar et al. 2010) reveal somewhat surprising microwear patterns that do not always

match what is expected based on morphology. Australopithecus individuals and

Paranthropus boisei do not have the microwear pattern of high complexity and heavy pitting

consistent with a hard-object feeder, unlike originally expected; they also have low to

moderate anisotropy, indicating they did not shear tough leaves (Ungar and Sponheimer

2011). Paranthropus robustus, in contrast, had very high complexity and very low anisotropy,

as well as the highest amount of variation of all early hominins (Scott et al. 2005). This

distribution is similar to hard-object fallback feeders, which eat harder foods when their

preferred softer foods are absent (Scott et al. 2005). Early Homo microwear patterns show

evidence of a generalized diet (Ungar et al. 2012). Homo erectus, in particular, has much

more variation in the levels of microwear complexity than Homo habilis, suggesting a very

broad diet (Ungar and Sponheimer 2011).

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Microwear analyses provide important and direct details of hominin diets, but they

still have limitations. Microwear can really only indicate the consistency of food eaten and

studies must omit foods that do not leave impressions on the surfaces of teeth, such as insects

and flesh (Lee‐Thorp et al. 2003). The “last supper effect” should also be taken into account;

microwear features are constantly worn over and only reflect diet in the last few days or

weeks of life (Grine 1986).

Stable Carbon Isotopes

Stable carbon isotope analyses can be used to determine the relative proportion of C3

(trees, bushes, shrubs, forbs) and C4 (grasses, sedges) plants in an extinct hominin

individual’s diet (Ungar and Sponheimer 2011). The stable isotopes of plants eaten by an

individual (or for faunivores, the plants eaten by its prey) are incorporated into the teeth and

bones of that individual and the isotopic composition of these tissues becomes reflective of

its diet (Cerling et al. 1999; Koch et al. 1998; Lee-Thorp et al. 1989; Ungar and Sponheimer

2011). In the case of human evolution, stable isotope analyses can be used to determine if any

of the early hominin species had diets similar to those of extant apes and evaluate the

percentage of C3 and C4 plants in their diets based on δ13C values (Figure 5).

Results indicate that the early hominins that have been analyzed using stable isotopes

can be roughly separated into three groups: those with relatively low δ13C values

(Ardipithecus ramidus and Australopithecus anamensis) similar to the C3 dominated diets of

savanna chimpanzees (Schoeninger et al. 1999; Sponheimer et al. 2013; Sponheimer et al.

2006a), those with intermediate δ13C values (Australopithecus africanus, Australopithecus

afarensis, Paranthropus robustus, and early Homo) (Lee-Thorp et al. 2000; Sponheimer et al.

2006b; van der Merwe et al. 2008; van der Merwe et al. 2003) indicating a mixed C3/C4 diet,

and those with high δ13C values and strongly a C4 diet (Paranthropus boisei) (van der Merwe

et al. 2008).

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While stable carbon isotope analyses reveal useful and interesting information, there

is some difficulty in explaining the results, as there can be several possible explanations for

what is observed. In particular, we cannot discriminate between folivorous, frugivorous, or

carnivorous diets as all three are based on C3 plants, nor can we tell which type of C3 or C4

foods were eaten (Clement and Hillson 2013; Sponheimer et al. 2013).

Trace Elements (Sr/Ca)

It is possible, however, to distinguish between folivorous, carnivorous, or

underground storage organ based diets through the use of trace elements (Lee‐Thorp et al.

2003). The ratio of strontium (Sr) to calcium (Ca) in an individual’s teeth or bones is

reflective of the foods eaten and their trophic level. Herbivores have lower Sr/Ca ratios than

the plants they eat, and carnivores have lower Sr/Ca ratios relative to their prey (Elias et al.

1982; Ungar and Sponheimer 2013). Additionally, leaf-eating herbivores would have lower

Sr/Ca ratios compared to animals that eat stems or underground storage organs (Sillen et al.

1995). It is important to note however, that a carnivore would only have a reduced Sr/Ca ratio

compared to the particular prey it eats, and as a result, it may overlap with herbivores (Lee‐

Thorp et al. 2003). There is also a high level of variability within species, further

complicating any analyses (Burton et al. 1999; Sillen 1992).

When Sr/Ca ratios are examined in South African early hominins, Australopithecus

africanus had the highest ratios, early Homo the lowest, and Paranthropus robustus was

intermediary (Figure 6) (Balter et al. 2012). When compared to other fauna, early Homo fit

within the Sr/Ca range for carnivores, Paranthropus robustus for browsers, and

Australopithecus africanus was indistinguishable from both grazers and browser (Balter et al.

2012). It is possible that early Homo and Paranthropus robustus both had relatively typical

browser/carnivore diets, while Australopithecus africanus had a more complex diet.

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Contextual Evidence

Paleoenvironmental Reconstruction

As diet is a direct link between an individual and its environment, dynamic changes in

environment likely influenced dietary and adaptive changes throughout human evolution

(Alemseged and Bobe 2009; Ungar et al. 2006). Reconstructing the paleoenvironmental

context of each hominin taxa can provide an additional angle from which to assess potential

hominin diets. The type of environment an individual lives in can limit and influence their

food choices (e.g a savanna animal is more likely to rely on grasses than tree fruits) (Ungar

and Sponheimer 2013). Additionally, if any of the early hominins depended on a specific

food for survival and those food sources disappeared with an environmental shift, it could

have led to their extinction or been the driving force behind an adaptive morphological

transition (Ungar et al. 2006). Environments can be reconstructed using many different

methods. Often the most common taxa of a fossil assemblage are used to infer the most likely

environment and confirmed using sedimentological and other related evidence (Alemseged

and Bobe 2009). Fossilized plant remains, pollen, phytoliths, and soil isotopes are additional

methods that are useful in interpreting paleoenvironments (Bamford 1999; Bonnefille et al.

2004; Cerling 1992; WoldeGabriel et al. 1994).

Unfortunately, even if we are able to reconstruct the environments early hominins

likely inhabited, this does not tell us much about what they actually ate. Rather, it shows what

would have been available and provides context for other lines of evidence. Additionally, we

need to know the distribution of edible foods in these landscapes in order to understand their

eating habits (Peters 2007; Ungar and Sponheimer 2013). It can show, however, whether

specific hominin taxa were specialized for particular environments or more generalized and

lived in diverse habitats, as well any similarities or inconsistencies in hominin diet across

environment type (Alemseged and Bobe 2009).

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Archaeological and Zooarchaeological Remains

Archaeological evidence can be an important source of information for the diets of

hominin taxa, however there are limitations on what survives in the archaeological record.

For most early hominins we do not have any archaeological artifacts from the time period

that they were alive. Of the early hominin archaeological material we do have, stone tools

and butchery marks on animal bones reveal the most about diet. The earliest examples of

stone tools appear around 2.6 million years ago (Semaw et al. 1997; Semaw et al. 2003) and

the earliest cut marks on bone are from around 2.5 million years ago (De Heinzelin et al.

1999) (although there is controversial evidence of cut-marked bones from 3.4 million years

ago (McPherron et al. 2010)). It is likely that hominins from earlier time periods also made

and used tools, but out of perishable materials (Panger et al. 2002). The existence of early

stone tools alone does not prove they were used in food acquisition, however the presence of

butchery marks on animal bones provides support for this idea (Ungar et al. 2006).

Furthermore, stone tools were probably very versatile implements. Microwear on some

Oldowan stone tool artifacts suggests they were used to prepare vegetation, possibly for food

or to construct tools from plant materials (Keeley and Toth 1981). The function of stone tool

kits also probably varied between hominin taxa and groups, as they do for extant chimpanzee

groups and modern human foragers (Ungar et al. 2006). At any rate, it is clear that the

development of stone tools greatly expanded hominin dietary options.

The presence of cut-marked animals bones suggests that the development of stone

tools enabled a shift in the hominin diet from a primarily frugivorous diet that may have

included small animals, to one that included medium to large sized animals (Blumenschine

and Pobiner 2007). The combination of both cut marks and carnivore teeth marks on

zooarchaeological remains demonstrates which other animals hominins interacted and

competed with for food sources (Blumenschine and Pobiner 2007). Butchery marks from

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stone tools are clearly morphologically distinct from carnivourous teeth marks, as well as

rodent gnawing and other taphonomic marks (Blumenschine and Pobiner 2007).

The development of stone tools greatly expanded the dietary options of early

hominins, and butchery marks on zooarchaeological remains provides concrete evidence that,

beginning about 2.5 million years ago, these hominins were incorporating food from larger

animals into their diet. What is less clear, however, is exactly which hominin taxa were

making these stones tools and using them in food acquisition. Several hominin species were

alive around 2.5 million years ago and multiple species are often found at the same site. This

makes it nearly impossible to determine which species was the creator of the stone tool

artifacts or cut marks on bones (Lee‐Thorp et al. 2003; Ungar et al. 2006).

Plant vs. Animal Food in Hominin Diets

The increasing incorporation of animal meat and tissue into the hominin diet was one

of the most dramatic and influential dietary changes that occurred during human evolution

(Bunn 2006). It is thought that the spread of savanna grasslands and the decrease of forest

resources pushed hominins to include more and more meat in their diets in order to maintain

the same level of dietary quality (Milton 1999; Milton 2003; Ungar et al. 2006). The

development of stone tools also improved and expanded their hunting abilities and strategies.

A feedback loop was created, with the increase in protein and energy from the meat allowing

for the growth of larger brains, which in turn led to greater intelligence and more complex

cognition; resulting in more complex social systems, division of labor, and better hunting

strategies (Isaac 1971; Isler and van Schaik 2009; Ungar et al. 2006; Washburn 1963).

Several hypotheses have been proposed to explain the role meat eating has played in human

evolution, with particular emphasis on a relationship with brain size (Aiello and Wheeler

1995; Isler and van Schaik 2009; Milton 1999; Milton 2003). The habitual eating of large

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amounts of meat provided an important nutritional increase. The “Expensive Tissue

Hypothesis” (Aiello and Wheeler 1995) and “Expensive Brain Hypothesis” (Isler and van

Schaik 2009) both point to an increase in available metabolic energy as crucial to the growth

of a larger brain.

Although it is clear that meat eating was critical to the evolution of the human lineage,

other researchers suggest that underground storage organs played an important role in the diet

of early human evolution (Dominy et al. 2008; Laden and Wrangham 2005; O’Connell et al.

2002; O’Connell et al. 1999). It is suggested that hominins are specially adapted to eating

underground storage organs (such as tubers, roots, corms, and bulbs), particularly as fallback

foods, and the development of these adaptations was key in the initial differentiation between

early hominins and other primate species (Hatley and Kappelman 1980; Laden and

Wrangham 2005; Wolpoff 1973). Additionally, O’Connell et al. (1999) suggest that climate

and food resource changes around 2 million years ago led to adjustments in foraging

practices, reducing the foods that children could gather themselves and increasing the

importance of grandmothers helping to gather food for the children. Underground storage

organs are suggested as the mostly likely exploited resource at this time due to their

availability and nutrients (O’Connell et al. 2002; O’Connell et al. 1999; Ungar et al. 2006).

Impact of Cooking on Hominin Diets

The development of cooking was another dramatic and crucial event in hominin

evolution (Wrangham and Conklin-Brittain 2003; Wrangham et al. 1999). It is argued that

cooking selected for a more human-like social system, due to the delay in the consumption of

food and necessity to be stored and protected from theft (Wrangham and Conklin-Brittain

2003; Wrangham et al. 1999). Additionally, cooking makes food easier to digest and

increases energy intake, expanding the range of possible plant and animal foods that were

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edible to early hominins (Wrangham and Carmody 2010; Wrangham et al. 1999). It also

alleviated effects of toxic and digestion-inhibiting elements found in many plants, meaning

more of these plants could be consumed if cooked than raw (Attwell et al. 2015; Stahl et al.

1984; Wrangham and Carmody 2010). The “pre-digesting” done by cooking reduces the

energy needed for digestion once eaten, opening up more energy for allocation elsewhere

(Attwell et al. 2015; Carmody and Wrangham 2009). It is likely that cooking, in addition to

the inclusion of meat in the diet, had a morphological effect on hominin evolution,

particularly brain size and cranial and dental morphology. Both the “Expensive Tissue

Hypothesis” (Aiello and Wheeler 1995) and “Expensive Brain Hypothesis” (Isler and van

Schaik 2009) can be applied to the higher quality diet cooking provides. The reduced

masticatory strain caused by cooking also probably relaxed the selective pressures on tooth

size, leading to a reduction in the cheek teeth of Homo erectus and an eventual reduction in

facial size of later hominin species (Lieberman et al. 2004).

The earliest date for the adoption of cooking is estimated to be at the origin of Homo

erectus, although this is based on biological evidence (reduced teeth, increase in female body

size, increased brain size), not archaeological evidence (Wrangham et al. 1999). A recent

phylogenetic study based on feeding time and molar size, also found results supporting an

origin around the evolution of Homo erectus (~1.9 million years ago) (Organ et al. 2011).

The earliest evidence for the controlled use of fire, however, is from around 1 million years

ago (Berna et al. 2012; Goren-Inbar et al. 2004).

Conclusion

It is clear that hominin diet changed drastically from the beginning of the hominin

lineage to the start of the genus Homo. The earliest hominins had plant-based diets similar to

other primates of the time, although the specific make up each hominin taxa’s diet varied

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widely. The inclusion of more animal foods, as well as the development of cooking, acted as

a catalyst for major morphological changes, such as an increase in brain size and decrease in

dental and facial size. Reconstructing the diet of early hominins and how it evolved

throughout hominin evolution can be done using many difference sources of evidence. Each

line of evidence reveals different aspects of the hominin diet and the results are not always

interpreted to show the same conclusions. Adaptive evidence, such as tooth size and

morphology, can suggest the foods that each hominin taxa has adapted to be able to eat, and

therefore more accurately reflects the diet of past generations rather that the one currently

being studied. Non-adaptive lines of evidence, such as dental microwear, stable isotopes, and

trace elements, provide the best direct indication of individual hominin diets. Contextual

evidence, such as paleoenvironmental reconstructions and archaeological and

zooarchaeological remains, provides context for the interpretation of other dietary evidence,

as well as material evidence for significant dietary shifts, like meat eating and cooking.

Although each method answers different questions and the results are not always in

congruence, all lines of evidence should be used in combination in order to reconstruct the

most complete picture of early hominin diet.

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Figures

Figure 1 “Incisor allometry. The dashed lines indicate 95% confidence limits of the least squares regression.” Reproduced from Ungar (2012).

Figure 2 "Cheeck-tooth occlusal areas and megadontia quotients of early hominins. Occlusal areas (the sum of the products of mesiodistal and buccolingual diameters of P4, M1, and M2) are presented above (A),

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and megadontia quotients (occlusal areas divided by 12.15 x body mass0.86) are illustrated below (B). The values in these graphs are from McHenry and Coffing (2000), and taxonomic attributions are as presented by those authors.” Reproduced from Ungar (2012).

Figure 3 "Microwear textures of early hominins. A model for microwear formation, wherein hard and brittle foods are crushed between opposing teeth, causing pitting with complex, isotropic surface textures; in contrast, soft and tough foods are sheared between opposing teeth that slide past one another, causing parallel scratches and simpler, anisotropic surfaces.” Reproduced from Ungar and Sponheimer (2011).

Figure 4 "Microwear texture complexity values for individual fossil hominins by species." Reproduced from Ungar and Sponheimer (2011)

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Figure 5 "Carbon isotope compositions (13C/12C) of early hominins. Top: Carbon flows from C3 and C4 plants (blue and pink arrows, respectively) into the tooth enamel of the consumer (in this case P. robustus, SK 1), and its resulting carbon isotope composition reveals the proportions of these plant types consumed. Bottom: Quantile plot with carbon isotope ratio data for all early hominins analyzed to date [data from (34–38, 49)]. Darker shading indicates a greater degree of C3 plant consumption. Each data point reflects a hominin’s diet for a period ranging from months to years depending on the sampling procedure used (red rectangles represent hypothetical sampling areas). Carbon isotope ratios (13C/12C) are expressed as d values in parts per thousand relative to the PeeDee Belemnite standard.” Reproduced from Ungar and Sponheimer (2011).

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Figure 6 "Sr/Ca ratios of hominin and bovid enamel. For both ratios, error bars are 2-sigma standard deviations of the mean, and the shaded areas contain data from a previous study (Sponheimer and Lee-Thorp 1999)." Reproduced from Balter et al. (2012).

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