Impact of Carnivory on Human Development

Impact of Carnivory on Human Development and Evolution Revealed by a New Unifying Model of Weaning in Mammals

Elia Psouni / Axel Janke / Martin Garwicz

Source - http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0032452

Abstract

Our large brain, long life span and high fertility are key elements of human evolutionary success and are often thought to have evolved in interplay with tool use, carnivory and hunting. However, the specific impact of carnivory on human evolution, life history and development remains controversial. Here we show in quantitative terms that dietary profile is a key factor influencing time to weaning across a wide taxonomic range of mammals, including humans. In a model encompassing a total of 67 species and genera from 12 mammalian orders, adult brain mass and two dichotomous variables reflecting species differences regarding limb biomechanics and dietary profile, accounted for 75.5%, 10.3% and 3.4% of variance in time to weaning, respectively, together capturing 89.2% of total variance. Crucially, carnivory predicted the time point of early weaning in humans with remarkable precision, yielding a prediction error of less than 5% with a sample of forty-six human natural fertility societies as reference. Hence, carnivory appears to provide both a necessary and sufficient explanation as to why humans wean so much earlier than the great apes. While early weaning is regarded as essentially differentiating the genus Homo from the great apes, its timing seems to be determined by the same limited set of factors in humans as in mammals in general, despite some 90 million years of evolution. Our analysis emphasizes the high degree of similarity of relative time scales in mammalian development and life history across 67 genera from 12 mammalian orders and shows that the impact of carnivory on time to weaning in humans is quantifiable, and critical. Since early weaning yields shorter interbirth intervals and higher rates of reproduction, with profound effects on population dynamics, our findings highlight the emergence of carnivory as a process fundamentally determining human evolution.

Introduction

The evolutionary, ecological, social, behavioral and cognitive implications of the relatively high level of carnivory in humans compared to other extant primates have been the subject of vigorous debates in a variety of research fields over the past fifty years. In an evolutionary context, a ‘significant’ amount of carnivory has been suggested to correspond to a shift from 10% to 20% of food from meat. In extant primate species, this shift corresponds to the difference between chimpanzees, with on average around 5% of their diet being meat, and tropical populations of hunter-gatherers living in environments similar to those of the African Pliocene, with estimated carnivorous diet of between 20% and 50%.

A crucial obstacle to reaching a consensus regarding the impact of carnivory on human development, life history and evolution is that its effects have been difficult to evaluate in quantitative terms. A case in point is the relatively short duration of lactation and suckling in humans in relation to other milestones in our life history and as compared to the great apes. To date, factors that may have determined the timing of weaning in humans are poorly understood, resulting in a wide scatter of attempted predictions of ‘natural’ weaning age in humans from other life history variables. However, as emphasized by syntheses of large numbers of studies, most of these predictions suggest a substantially later weaning age than practiced by modern humans, not only in the industrial world, but also in human natural fertility societies (the latter displaying an average of ca. 27 months).

The early human weaning has implications not only for offspring development, but also for interbirth intervals and thereby for the reproductive rate of the female, which in turn influences population dynamics and fitness of the species. According to a longstanding hypothesis, the human weaning pattern was derived specifically from an ancestral hominid pattern and is due to the introduction of meat into the diet of early hominins some 2.6-2.0 million years ago. However, this hypothesis has not been possible to test since no model has been available for making a quantitative prediction of the consequences for time to weaning if a large brained primate species were to increase its intake of meat.

Relative time scales of early development appear to be very similar across mammals and lactation is a defining feature of Mammalia, common to all species of this class. We therefore suggest that a potential key to understanding the timing of human weaning is to interpret it in a broad phylogenetic context by using a comparative analysis that includes not only hominids and other primates, but also species and traits representing other mammalian orders. The importance of a broad comparative perspective was emphasized by a recent radical reappraisal of another fundamental milestone in early human development – the timing of walking onset. Our approach is quantitative and focused on the ontogenetic level of analysis, in search for proximate causes for the timing of weaning.

In accordance with principles previously emphasized in the literature, we developed a parsimonious, straight forward and biologically readily interpretable model. The model was based on sixty-seven species representing a wide taxonomic range of mammals and collected from twelve different orders (Fig. 1).

Figure 1. Phylogenetic relatedness and evolutionary divergence times of species in the present sample.

To avoid sample bias by overrepresentation of single lineages no more than one species was included from any given genus. Thus the 67 species in the sample represent 67 genera. A phylogenetic analysis and an independent contrasts analysis were performed to investigate if evolutionary dependence between the 67 species influenced the statistical analyses. The sample was carefully balanced for various species characteristics as outlined in Materials and Methods. In line with previous literature, we employed adult brain mass and adult female body mass as fundamental continuous independent variables that could potentially serve as predictors of time to weaning. Adult brain mass reflects the time during which the brain has developed during ontogenesis since mammalian brains develop at similar rates. Therefore, if interspecies variation in weaning depends on brain mass, the duration of suckling may be assumed to reflect primarily the developmental time course and the needs of the offspring. If, on the other hand, interspecies variation in weaning depends on adult female body mass, it would primarily reflect the metabolic limitations of the lactating female. The dependent variable was expressed either as time to weaning postnatal or post conception. Although the former measure is more conventional, the latter appears biologically more relevant as it represents both the total developmental time of the offspring and the total time invested by the female.

Figure 2. Brain mass is a better fundamental predictor of time to weaning than is female body mass.