Evidence for a convergent slowdown in primate molecular rates and its implications for the timing of early primate evolution

Abstract

A long-standing problem in primate evolution is the discord between paleontological and molecular clock estimates for the time of crown primate origins: the earliest crown primate fossils are ~56 million y (Ma) old, whereas molecular estimates for the haplorhine-strepsirrhine split are often deep in the Late Cretaceous. One explanation for this phenomenon is that crown primates existed in the Cretaceous but that their fossil remains have not yet been found. Here we provide strong evidence that this discordance is better-explained by a convergent molecular rate slowdown in early primate evolution. We show that molecular rates in primates are strongly and inversely related to three life-history correlates: body size (BS), absolute endocranial volume (EV), and relative endocranial volume (REV). Critically, these traits can be reconstructed from fossils, allowing molecular rates to be predicted for extinct primates. To this end, we modeled the evolutionary history of BS, EV, and REV using data from both extinct and extant primates. We show that the primate last common ancestor had a very small BS, EV, and REV. There has been a subsequent convergent increase in BS, EV, and REV, indicating that there has also been a convergent molecular rate slowdown over primate evolution. We generated a unique timescale for primates by predicting molecular rates from the reconstructed phenotypic values for a large phylogeny of living and extinct primates. This analysis suggests that crown primates originated close to the K-Pg boundary and possibly in the Paleocene, largely reconciling the molecular and fossil timescales of primate evolution.

Fig. 1.

Time-scaled phylogeny depicting divergence dates for the main groups of primates. Dates along the x axis are in Ma. Average molecular clock date estimates are from six recent studies (Table S1). The fossil femur cartoon indicates the earliest paleontological crown representatives of each taxon: crown Primates and crown Haplorhini, Teilhardina asiatica, 55.8 Ma, or, less securely, slightly older Altiatlasius koulchii (15, 57, 58); crown Strepsirrhini, Saharagalago, 37 Ma (–61); crown Anthropoidea, Biretia, 37 Ma (59); crown Catarrhini, Morotopithecus, 20.6 Ma (62), crown Cebidae, long-lineage hypothesis (63), Branisella, 26–27 Ma (64); crown Cebidae, successive radiation hypothesis (65), Lagonimico (66) and others, 13.3 Ma (66, 67); crown Cercopithecoidea, Microcolobus, 9.9 Ma (68); crown Hominidae, Sivapithecus, 12.5 Ma (69). The colored circles indicate the average divergence estimates from both uncorrected and corrected methods (Table 3).

Fig. 2.

Phenotypic reconstructions of ancestral BS, EV, and REV. Cladogram depicts ancestral trait reconstructions for BS, EV, and REV at key nodes in primate evolution. For BS, the area of the outside circle includes the area under the colored circle. Branches are not to scale.

Fig. 3.

Phenotypic data and molecular rate scatter plots. Scatter plots of molecular rate (per 10⁸ y; y axis) and BS, EV, and REV. PGLS regression lines are shown. All regression statistics are found in Table 2. Red, Perelman et al. (7); green, the CYP7A1 region (16); blue, Jameson et al. (14); purple, the CFTR region of Prasad et al. (49).