Successive radiations, not stasis, in the South American primate fauna

Abstract

The earliest Neotropical primate fossils complete enough for taxonomic assessment, Dolichocebus, Tremacebus, and Chilecebus, date to approximately 20 Ma. These have been interpreted as either closely related to extant forms or as extinct stem lineages. The former hypothesis of morphological stasis requires most living platyrrhine genera to have diverged before 20 Ma. To test this hypothesis, we collected new complete mitochondrial genomes from Aotus lemurinus, Saimiri sciureus, Saguinus oedipus, Ateles belzebuth, and Callicebus donacophilus. We combined these with published sequences from Cebus albifrons and other primates to infer the mitochondrial phylogeny. We found support for a cebid/atelid clade to the exclusion of the pitheciids. Then, using Bayesian methods and well-supported fossil calibration constraints, we estimated that the platyrrhine most recent common ancestor (MRCA) dates to 19.5 Ma, with all major lineages diverging by 14.3 Ma. Next, we estimated catarrhine divergence dates on the basis of platyrrhine divergence scenarios and found that only a platyrrhine MRCA less than 21 Ma is concordant with the catarrhine fossil record. Finally, we calculated that 33% more change in the rate of evolution is required for platyrrhine divergences consistent with the morphologic stasis hypothesis than for a more recent radiation. We conclude that Dolichocebus, Tremacebus, and Chilecebus are likely too old to be crown platyrrhines, suggesting they were part of an extinct early radiation. We note that the crown platyrrhine radiation was concomitant with the radiation of 2 South American xenarthran lineages and follows a global temperature peak and tectonic activity in the Andes.

Fig. 1.

Topology and branch lengths used for divergence time estimates. Phylogeny was inferred through maximum likelihood (PAUP*) and Bayesian (MrBayes) analysis with Lemur and Nycticebus as outgroups. Maximum likelihood bootstrap percentages are left of the branches, and Bayesian clade credibility proportions are right. Maximum likelihood branch lengths were estimated using the F84 + G model of evolution (estbranches).

Fig. 2.

Divergence time estimates with Bayesian credibility intervals (BCI) using the best available fossil constraints. Gray bars indicate constraint ranges for the nodes indicated on them. Arrows indicate that no lower constraint was used.

Fig. 3.

Surface plot of predicted catarrhine divergence times given various platyrrhine divergence scenarios. The figure summarizes the results of 540 multidivtime analyses. The constraints used for each analysis are given on the x and y axes, and the predicted catarrhine divergence times given these constraints are shown on the z axis. Shaded regions indicate platyrrhine calibrations that predict catarrhine divergences concordant with the catarrhine fossil record.

Fig. 4.

Change in the rate of evolution between branches given various platyrrhine divergence scenarios. The figure gives the estimated autocorrelation parameter (ν) for 35 multidivtime runs. Five constraint intervals were constant for all runs (Table 2, constraints 1–5). The cebid MRCA was varied for each run, and the constraint intervals used are shown on the x axis. The dashed lines indicate the La Venta fossils at 12.5 Ma and the disputed early Miocene fossils at 20 Ma and demarcate the SRH and the MSH.