The rise and fall of a genus: Complete mtDNA genomes shed light on the phylogenetic position of yellow-tailed woolly monkeys, Lagothrix flavicauda, and on the evolutionary history of the family Atelidae (Primates: Platyrrhini)
Graphical abstract
Introduction
The yellow-tailed woolly monkey, Lagothrix (Oreonax) flavicauda, is one of five currently recognized morphotypes of woolly monkeys distributed throughout the central and western Amazonian lowlands and in montane and submontane regions of the eastern cordillera of the Andes (Fig. 1). Endemic to northern Perú, the yellow-tailed woolly monkey has long been considered critically endangered (Cornejo et al., 2008, Mittermeier et al., 2009), and its phylogenetic position and taxonomic status within the Atelidae (the neotropical primate family that includes all of the large-bodied, prehensile-tailed platyrrhines) have been controversial. While an early comprehensive review (Fooden, 1963) considered the yellow-tailed woolly monkey as one of two allopatric species of Lagothrix, a cladistic analysis of craniodental characters (Groves, 2001) elevated the taxon to its own monotypic genus, under the resurrected name Oreonax, and considered it a sister taxon to spider monkeys (Ateles) rather than Lagothrix. A more recent reanalysis, however, argued that the craniodental evidence is insufficient to warrant assigning this primate to a distinct genus (Matthews and Rosenberger, 2008, Rosenberger and Matthews, 2008), and other morphological studies have confirmed a closer relationship between L. flavicauda and other woolly monkeys instead of Ateles (e.g., Paredes Esquivel, 2003).
To address this thorny taxonomic question as well as other unresolved issues concerning atelid evolutionary history, we undertook a new molecular phylogenetic study of the radiation using a large, comparative, mitogenomic dataset. While several previous molecular studies have attempted to resolve relationships within the Atelidae (Canavez et al., 1999, Collins, 2004, Meireles et al., 1999, Opazo et al., 2006), none has included all of the putative genera in the radiation and none has employed a sequence dataset of the size we use here. Our study thus had three main goals: (1) to reconstruct the phylogenetic relationships among the atelid primates using a large mtDNA dataset encompassing all putative genera, (2) to estimate the timing of major divergences within the atelid clade, and (3) to evaluate whether or not the yellow-tailed woolly monkey should be placed in a separate genus from Lagothrix.
To address these objectives, we sequenced the complete mtDNA genomes of three of the five putative species of woolly monkeys – Lagothrix (Oreonax) flavicauda, Lagothrix poeppigii, and L. lugens – plus two other atelid taxa, Alouatta seniculus and Brachyteles hypoxanthus. We also sequenced roughly 8 kb of the mtDNA genomes of the remaining two currently recognized woolly monkey morphotypes, L. cana and L. lagotricha. These were aligned with existing mitogenomic data for a large and taxonomically diverse set of primates (Chiou et al., 2011, Finstermeier et al., 2013, Hodgson et al., 2009) and then used for both maximum likelihood and Bayesian phylogenetic inference analysis as well as for Bayesian estimation of lineage divergence times. Additionally, we mined NCBI GenBank for mitochondrial cytochrome oxidase subunit II (COX2) gene sequences from all platyrrhine primate genera where more than one named species within the genus was represented. We then used these sequence data to characterize the pairwise genetic diversity found among species within the same genus as well as between genera for comparison to the pairwise diversity between sequences from the different putative species of woolly monkeys at the same locus.
Section snippets
Taxon samples and DNA extraction
Tissue, feces, or extracted DNA were obtained from a variety of sources and collaborators for each of the five putative forms of woolly monkeys, plus red howler monkeys (Alouatta seniculus) and northern muriquis (Brachyteles hypoxanthus) (Table 1). We extracted DNA from tissue samples using the QIAamp DNA Mini Kit (Qiagen, Inc.) following the protocol for DNA Purification from Tissues. The final steps of the protocol were modified slightly in that we heated Buffer AE to 70 °C before applying it
Phylogenetic reconstruction
All of our Bayesian and maximum likelihood analyses recovered the exactly same tree topology for the best inference of phylogenetic relationships among the genera in our dataset, with the exception of the branching patterns among different putative species of common woolly monkeys (i.e., Lagothrix apart from the yellow-tailed woolly monkey) (Fig. 2). Support for this topology was very strong, with all but four nodes outside of the Lagothrix clade having >99% bootstrap support averaged across
Atelid phylogenetic history and divergence dates
Our mitogenomic analysis of platyrrhine evolutionary history, which incorporates new sequence data from seven additional atelid taxa (including red howler monkeys, northern muriquis, and all five currently recognized morphotypes of woolly monkeys) corroborates and fills in other recent molecular reconstructions of New World monkey phylogeny, several of which have been based on less extensive mitogenomic datasets for the taxa in question (Chiou et al., 2011, Finstermeier et al., 2013, Hodgson et
Acknowledgments
A large number of people and institutions helped make this research possible. Foremost, we are very grateful to the governments of Ecuador, Colombia, and Perú for permission to conduct field research on woolly monkeys in all of these countries and to collect and export fecal and tissue samples for genetic analysis. Todd Disotell, Kenny Chiou, Luca Pozzi, Jason Hodgson, and Cliff Jolly of the NYU Molecular Anthropology Laboratory all provided important technical advice and assistance, as did
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