Phylogenetic rate shifts in feeding time during the evolution of Homo

Abstract

Unique among animals, humans eat a diet rich in cooked and nonthermally processed food. The ancestors of modern humans who invented food processing (including cooking) gained critical advantages in survival and fitness through increased caloric intake. However, the time and manner in which food processing became biologically significant are uncertain. Here, we assess the inferred evolutionary consequences of food processing in the human lineage by applying a Bayesian phylogenetic outlier test to a comparative dataset of feeding time in humans and nonhuman primates. We find that modern humans spend an order of magnitude less time feeding than predicted by phylogeny and body mass (4.7% vs. predicted 48% of daily activity). This result suggests that a substantial evolutionary rate change in feeding time occurred along the human branch after the human-chimpanzee split. Along this same branch, Homo erectus shows a marked reduction in molar size that is followed by a gradual, although erratic, decline in H. sapiens. We show that reduction in molar size in early Homo (H. habilis and H. rudolfensis) is explicable by phylogeny and body size alone. By contrast, the change in molar size to H. erectus, H. neanderthalensis, and H. sapiens cannot be explained by the rate of craniodental and body size evolution. Together, our results indicate that the behaviorally driven adaptations of food processing (reduced feeding time and molar size) originated after the evolution of Homo but before or concurrent with the evolution of H. erectus, which was around 1.9 Mya.

Fig. 1.

The relationship between feeding time (percent of the time spent feeding per active hours of the day) and body mass in nonhuman primates. (A) Phylogenetic generalized least square regression (average of the Bayesian posterior distribution) relating feeding time to body mass. Feeding time was logit-transformed to range from negative infinity when feeding time equals 0 to positive infinity when feeding time equals 100. (B) The posterior distribution of the slope parameter for the regression model compared with the null hypothesis (slope = 0). (C) The posterior predictive distribution of feeding time in H. sapiens compared with the actual value (phylogenetic outlier test) indicates that humans have evolved to spend significantly less time feeding than would be predicted by the model and phylogeny (i.e., the observed values fall outside the 99% credible intervals).

Fig. 2.

Phylogenetic trees for great apes and extinct hominins along the human lineage. (A) This tree is inferred using morphological characters in a Bayesian framework, and it has branch lengths relative to the amount of evolutionary change in the characters. (B) A time-calibrated tree shows the same general relationships. Labels at nodes are posterior probability support (the fraction of times that the node appeared in the posterior distribution of trees) for A and B.

Fig. 3.

The relationship between molar size and body mass. (A) The phylogenetic generalized least square regression (average of the Bayesian posterior distribution) relates the area of the second lower molar (mesio-distal length multiplied by bucco-lingual breadth), a proxy for chewing surface area, with body mass. (B) The posterior distribution of the slope parameter for the regression model compared with the null hypothesis (slope = 0). (C–G) The posterior predictive distributions of molar size in Homo compared with actual values (a phylogenetic outlier test). The actual molar size values fall outside the 99% credible intervals for H. sapiens, H. neanderthalensis, and H. erectus.