Next-Generation Museomics Disentangles One of the Largest Primate Radiations

Abstract

Guenons (tribe Cercopithecini) are one of the most diverse groups of primates. They occupy all of sub-Saharan Africa and show great variation in ecology, behavior, and morphology. This variation led to the description of over 60 species and subspecies. Here, using next-generation DNA sequencing (NGS) in combination with targeted DNA capture, we sequenced 92 mitochondrial genomes from museum-preserved specimens as old as 117 years. We infer evolutionary relationships and estimate divergence times of almost all guenon taxa based on mitochondrial genome sequences. Using this phylogenetic framework, we infer divergence dates and reconstruct ancestral geographic ranges. We conclude that the extraordinary radiation of guenons has been a complex process driven by, among other factors, localized fluctuations of African forest cover. We find incongruences between phylogenetic trees reconstructed from mitochondrial and nuclear DNA sequences, which can be explained by either incomplete lineage sorting or hybridization. Furthermore, having produced the largest mitochondrial DNA data set from museum specimens, we document how NGS technologies can “unlock” museum collections, thereby helping to unravel the tree-of-life. [Museum collection; next-generation DNA sequencing; primate radiation; speciation; target capture.]

Formal monkey linguistics

“…To give but two examples: booms are found in various points of the phylogenetic tree of cercopithecines. This is compatible with the view (among others) that they were present in the most recent common ancestor of all cercopithecines, who according to the DNA study of Guschanski et al (2013) lived more than 10 million years ago (see the detailed tree at http://sysbio.oxfordjournals.org/content/62/4/539/F1.expansion.html); we will remain agnostic below concerning such ancient periods, but we will make claims about what happened 2-3 million years ago.…”

“…More recently, Putty-nosed and Blue monkeys separated approximately 2.5 million years ago (Guschanski et al 2013), but they have very similar pyows and hacks. The prospect of an evolutionary linguistics of monkey calls is tantalizing, and we will come back to it below.…”

“…6 Importantly, different DNA methods may lead to different results -e. g. divergence dates may differ between Guschanski et al (2013), based on mitochondrial DNA, and Perelman (2011), based on nuclear DNA. When details matter (as in the evolutionary considerations of Section 7), such differences should be revisited in future research.…”

“…Putty-nosed monkeys and Blue monkeys have a most recent common ancestor that lived approximately 2.5 million years ago. In turn, their most recent common ancestor with Campbell's monkeys lived approximately 7.5 million years ago (Guschanski et al 2013). We will also be concerned with Black-and-White Colobus monkeys, which are part of another family of Old World monkeys, called 'colobinae'.…”

Formal monkey linguistics: The debate

“…disappeared long ago without telling us what kind of language abilities they had, if any. In the latter respect, the situation is considerably more favorable in monkey languages: as we discussed in connection with cercopithecines, plotting the distribution of boom calls in a phylogenetic tree (from Guschanski et al 2013) suggests that booms are at least several million years old in quite a few species. Similar evolutionary inferences could be drawn on several other calls, including Putty-nosed and Blue monkey pyows and hacks/kas.…”