Equality for the sexes in human evolution? Early hominid sexual dimorphism and implications for mating systems and social behavior.

S ince the publication of Charles Darwin’s The Descent of Man and Selection in Relation to Sex in 1871 (1), there has been a vigorous debate about the meaning of sexual dimorphism for a range of physical attributes in numerous animal species, including primates and humans, extinct and extant. Key points of discussion are how to interpret size dimorphism in past humans and human-like ancestors and what inferences can be drawn about the evolution of human mating systems and social organization. In this issue of PNAS, Reno et al. (2) report on their investigation of sexual dimorphism in the three-million-year-old Australopithecus afarensis, an important and well known hominid, ancestral to the genus Homo (3). Insight into dimorphism in this taxon has important implications for social behavior and organization in later and present-day humans. Body mass dimorphism varies dramatically among primate species, both present and past. For most anthropoids, males are bigger than females (4–8). Humans today display relatively limited sexual dimorphism ( 15%), whereas some of the other hominoids (gorillas and orangutans) are highly dimorphic ( 50%) (5, 9). Body mass is easily determined in living species. For past nonhuman primates and human ancestors, mostly represented by fragmentary fossil remains, body mass is far less accessible. Recently, the femur head (the ball of bone at the top of the femur that fits into the hip joint) has been invoked as a source for estimating body mass in early hominids, Homo, and its evolutionary predecessor, Australopithecus (10, 11). Comparisons of body mass in fossil hominids reveal that general levels of dimorphism have likely remained more or less the same for most of the evolution of Homo, or most of the last two million years to the present (9). In hominids predating Homo, namely the multiple species of Australopithecus, the consensus among paleoanthropologists that has emerged over the last two decades is that pre-Homo species are characterized by high levels of sexual dimorphism (4, 5, 12–15). Close scrutiny of the fossil record, however, suggests that this consensus is built on a data set replete with limitations, especially in regard to reconstructing size dimorphism in Australopithecus. First, the sample used to estimate dimorphism is very small (fewer than six individuals for A. afarensis). Second, estimates of dimorphism are based on the assumption that sex identification in fragmentary fossil remains used to derive these estimates is accurate. Indeed, the secondary sex characteristics exhibited in the bony pelvis, by far the most reliable of the indicators for humans (16, 17), are largely missing. Thus, investigators are left with size of skeletal elements alone (males have big bones and females have small bones), a poor proxy for pelvic sex identification. Third, accuracy in determination of sexual dimorphism is predicated on correct taxonomic identification. This is especially problematic given that level of sexual dimorphism shows substantial intertaxa variation. Fourth, levels of dimorphism can shift over broad expanses of time (potentially hundreds of thousands of years) or even relatively narrow expanses of time involving hundreds or tens of years (18). Finally, sexual dimorphism levels across broad geographic areas and ecological variation therein may be exaggerated in comparison with contemporary members of a species living in the same place (9). Reno et al. (2) draw on advances made in statistical modeling to circumvent these limitations of the early hominid fossil record. They apply a new and robust method of simulating dimorphism to an assemblage of A. afarensis representing the remains of individuals who likely died simultaneously in a single catastrophic event some 3.2 million years ago at site A.L. 333, Hadar, Ethiopia. Using the 40% complete skeleton (‘‘Lucy’’) from site A.L. 288 as a morphometric template (she has a relatively well preserved femur head and other long bones; Fig. 1), they calculated femoral head diameters from measurements for the postcranial elements from A.L. 333 and other A. afarensis remains. In contrast to the consensus, their analysis