Large ancestral effective population size explains the difficult phylogenetic placement of owl monkeys

Abstract

The phylogenetic position of owl monkeys, grouped in the genus Aotus, has been a controversial issue for understanding Neotropical primate evolution. Explanations of the difficult phylogenetic assignment of owl monkeys have been elusive, frequently relying on insufficient data (stochastic error) or scenarios of rapid speciation (adaptive radiation) events. Using a coalescent‐based approach, we explored the population‐level mechanisms likely explaining these topological discrepancies. We examined the topological variance of 2,192 orthologous genes shared between representatives of the three major Cebidae lineages and the outgroup. By employing a methodological framework that allows for reticulated tree topologies, our analysis explicitly tested for non‐dichotomous evolutionary processes impacting the finding of the position of owl monkeys in the cebid phylogeny. Our findings indicated that Aotus is a sister lineage of the callitrichines. Most gene trees (>50%) failed to recover the species tree topology, although the distribution of gene trees mismatching the true species topology followed the standard expectation of the multispecies coalescent without reticulation. We showed that the large effective population size of the common ancestor of Aotus and callitrichines was the most likely factor responsible for generating phylogenetic uncertainty. On the other hand, fast speciation scenarios or introgression played minor roles. We propose that the difficult phylogenetic placement of Aotus is explained by population‐level processes associated with the large ancestral effective size. These results shed light on the biogeography of the early cebid diversification in the Miocene, highlighting the relevance of evaluating phylogenetic relationships employing population‐aware approaches.

Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression

“…Three extant families from this radiation now make up the New World Monkeys (Platyrrhini, Figure 1). Because of the rapidity with which these species spread and diversified across the new continent, relationships at the base of the NWM have been hard to determine [12–14,16–18].…”

“…A recent analysis of NWM genomes found Aotus sister to Callithrix , as in the ML-CONCAT tree, despite the use of gene trees to build the species tree [18]. However, the outgroup used in this analysis is a closely related species ( Brachyteles arachnoides ) that diverged during the NWM radiation and that shares a recent common ancestor with the ingroup taxa [12,13].…”

“…Due to the rapid nature of several independent radiations within primates, these limited data cannot resolve species relationships within some clades [12–14]. For instance, the New World Monkeys (NWM) experienced a rapid period of diversification ~15-18 million years ago (mya) [15] (Figure 1), resulting in ambiguous relationships among the three Cebidae subfamilies (Cebinae=squirrel monkeys and capuchins, Aotinae=owl monkeys, and Callitrichinae=marmosets and tamarins) [12–14,16–18]. High levels of incomplete lineage sorting (ILS) driven by short times between the divergence of distinct lineages have led to a large amount of gene tree discordance in the NWM, with different loci favoring differing relationships among taxa.…”

Do saki monkeys possess a grooming claw?

“…Simplified primate phylogeny showing the presence ( ) or absence ( ) of a grooming claw in different lineages. We used a polytomy for the clade conformed by Aotus, Callitrichidae and Cebidae, as the position of Aotus within this clade is contentious (Kay, 2015;Schrago and Seuánez, 2019).…”

“…In primates, nails (ungulae), claw-like nails (tegulae) and grooming claws can be distinguished. Strepsirrhini possess ungulae, tegulae and a grooming claw on the second pedal digit (Soligo and Müller, 1999;Soligo, 2005). Within Haplorrhini, tarsiers possess ungulae and a grooming claw on the second and third pedal digit; Catarrhini only possess ungulae, whereas within Platyrrhini Callitrichidae also possess tegulae (Maiolino et al, 2011;Soligo and Müller, 1999;Spearman, 1985).…”