Early anthropoid femora reveal divergent adaptive trajectories in catarrhine hind-limb evolution

Sergio Almécija,Ashley S Hammond,Erik R Seiffert,Hesham M Sallam,John G Fleagle,Melissa Tallman

doi:10.1038/s41467-019-12742-0

Abstract

The divergence of crown catarrhines—i.e., the split of cercopithecoids (Old World monkeys) from hominoids (apes and humans)—is a poorly understood phase in our shared evolutionary history with other primates. The two groups differ in the anatomy of the hip joint, a pattern that has been linked to their locomotor strategies: relatively restricted motion in cercopithecoids vs. more eclectic movements in hominoids. Here we take advantage of the first well-preserved proximal femur of the early Oligocene stem catarrhine Aegyptopithecus to investigate the evolution of this anatomical region using 3D morphometric and phylogenetically-informed evolutionary analyses. Our analyses reveal that cercopithecoids and hominoids have undergone divergent evolutionary transformations of the proximal femur from a similar ancestral morphology that is not seen in any living anthropoid, but is preserved in Aegyptopithecus, stem platyrrhines, and stem cercopithecoids. These results highlight the relevance of fossil evidence for illuminating key adaptive shifts in primate evolution.

Highlights

The divergence of crown catarrhines—i.e., the split of cercopithecoids (Old World monkeys) from hominoids—is a poorly understood phase in our shared evolutionary history with other primates
Understanding the sequence of morphological changes in catarrhine, and especially hominoid, evolution is complicated by fossil taxa that exhibit mosaic morphologies that are not seen in any living species[11,12,13,14]
A. zeuxis is at least ~4.5–5.0 Ma older than the oldest known fossil hominoids and cercopithecoids, which have been recovered from a 25.2 Ma site in the Nsungwe Formation of Tanzania[1]

Summary

Introduction

The divergence of crown catarrhines—i.e., the split of cercopithecoids (Old World monkeys) from hominoids (apes and humans)—is a poorly understood phase in our shared evolutionary history with other primates. Our analyses reveal that cercopithecoids and hominoids have undergone divergent evolutionary transformations of the proximal femur from a similar ancestral morphology that is not seen in any living anthropoid, but is preserved in Aegyptopithecus, stem platyrrhines, and stem cercopithecoids These results highlight the relevance of fossil evidence for illuminating key adaptive shifts in primate evolution. This study investigates the evolution of the catarrhine hip complex (from the proximal femoral side) since the Oligocene and the implications for the locomotor capabilities of the cercopithecoid–hominoid ancestor To accomplish this goal, we use a series of stepwise analyses, combining three-dimensional geometric morphometrics (3DGM; see Supplementary Table 1) and evolutionary modelling within a multi-regime, multivariate framework across a large sample of living and fossil anthropoid femora (Supplementary Tables 2 and 3). Given that Aegyptopithecus is close in age to the predicted divergence of cercopithecoids and hominoids[1] and is widely accepted as an advanced stem catarrhine[2], we proceed with the assumption that this taxon is more likely than not to closely approximate the morphology of the last common ancestor of cercopithecoids and hominoids and is not already highly autapomorphic

Methods

Results

Conclusion