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)

https://doi.org/10.1016/j.ympev.2014.03.028Get rights and content

Highlights

  • Yellow-tailed woolly monkeys diverged from other woolly monkeys ~2.1 Ma.

  • Other morphotypes of woolly monkeys shared a recent common ancestor ~840 kyr.

  • The genus Oreonax should be subsumed into Lagothrix.

  • The woolly monkey lineage likely originated in northern Perú.

  • Muriquis are the sister group to woolly monkeys, and these lineages diverged ~8.5 Ma.

Abstract

Using complete mitochondrial genome sequences, we provide the first molecular analysis of the phylogenetic position of the yellow-tailed woolly monkey, Lagothrix flavicauda (a.k.a. Oreonax flavicauda), a critically endangered neotropical primate endemic to northern Perú. The taxonomic status and phylogenetic position of yellow-tailed woolly monkeys have been debated for many years, but in this study both Bayesian and maximum likelihood phylogenetic reconstructions unequivocally support a monophyletic woolly monkey clade that includes L. flavicauda as the basal taxon within the radiation. Bayesian dating analyses using several alternative calibrations suggest that the divergence of yellow-tailed woolly monkeys from other Lagothrix occurred in the Pleistocene, ∼2.1 Ma, roughly 6.5 my after the divergence of woolly monkeys from their sister genus, Brachyteles. Additionally, comparative analysis of the cytochrome oxidase subunit 2 (COX2) gene shows that genetic distances between yellow-tailed woolly monkeys and other Lagothrix from across the genus’ geographic distribution fall well within the range of between-species divergences seen in a large number of other platyrrhine primate genera at the same locus and outside the range of between-genus divergences. Our results thus confirm a position within Lagothrix for the yellow-tailed woolly monkey and strongly suggest that the name Oreonax be formally considered a synonym for this genus. This revision in taxonomic status does not change the dire conservation threats facing the yellow-tailed woolly monkey in Perú, where the remaining wild population is estimated at only ∼10,000 individuals living in a highly fragmented landscape.

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

References (86)

  • J. Opazo et al.

    Phylogenetic relationships and divergence times among New World monkeys (Platyrrhini, Primates)

    Mol. Phylogenet. Evol.

    (2006)
  • M. Osterholz et al.

    Retropositional events consolidate the branching order among New World monkey genera

    Mol. Phylogenet. Evol.

    (2009)
  • R. Raaum et al.

    Catarrhine primate divergence dates estimated from complete mitochondrial genomes: concordance with fossil and nuclear DNA evidence

    J. Hum. Evol.

    (2005)
  • D. Ray et al.

    Alu insertion loci and platyrrhine primate phylogeny

    Mol. Phylogenet. Evol.

    (2005)
  • R.M. Adkins et al.

    Evolution of the primate cytochrome c oxidase subunit II gene

    J. Mol. Evol.

    (1994)
  • U. Arnason et al.

    Pattern and timing of evolutionary divergences among hominoids based on analyses of complete mtDNAs

    J. Mol. Evol.

    (1996)
  • U. Arnason et al.

    Molecular timing of primate divergences as estimated by two nonprimate calibration points

    J. Mol. Evol.

    (1998)
  • U. Arnason et al.

    Molecular estimates of primate divergences and new hypotheses for primate dispersal and the origin of modern humans

    Hereditas

    (2000)
  • U. Arnason et al.

    Mammalian mitogenomic relationships and the root of the eutherian tree

    Proc. Nat. Acad. Sci. U.S.A.

    (2002)
  • M.S. Ascunce et al.

    Description of the cytochrome c oxidase subunit II gene in some genera of New World monkeys (Primates, Platyrrhini)

    Genetica

    (2002)
  • M.S. Ascunce et al.

    COII as a useful tool for phylogenetic studies in some genera of New World monkeys (Primates, Platyrrhini)

    Zoolog. Scr.

    (2003)
  • M.V. Ashley et al.

    Owl monkeys (Aotus) are highly divergent in mitochondrial cytochrome c oxidase (COII) sequences

    Int. J. Primatol.

    (1995)
  • P.L. Babb et al.

    mtDNA diversity in Azara’s owl monkeys (Aotus azarai azarai) of the Argentinean Chaco

    Am. J. Phys. Anthropol.

    (2011)
  • Bi, X., Huang, L., Jing, M., 2011. Cebus apella mitochondrion, complete genome. Published only in NCBI GenBank...
  • S. Botero

    How many species of woolly monkeys inhabit Colombian forests?

    Am. J. Primatol.

    (2010)
  • Botero, S., Stevenson, P.R., in press. Coat color is not an indicator of subspecies identity in Colombian woolly...
  • S. Botero et al.

    How many species of woolly monkeys inhabit Colombian forests?

    Am. J. Primatol.

    (2010)
  • Boubli, J.-P., Di Fiore, A., Rylands, A.B., Wallace, R.B., 2008. Lagothrix cana. IUCN Red List of Threatened Species....
  • J.K.E. Campbell et al.

    The Pan-Amazonian Ucayali Peneplain, late Neogene sedimentation in Amazonia, and the birth of the modern Amazon River system

    Palaeogeogr. Palaeoclimatol. Palaeoecol.

    (2006)
  • A.C. Collins

    Atelinae phylogenetic relationships: the trichotomy revived?

    Am. J. Phys. Anthropol.

    (2004)
  • A.C. Collins et al.

    Phylogenetic relationships of spider monkeys (Ateles) based on mitochondrial DNA sequence variation

    Int. J. Primatol.

    (2000)
  • Cornejo, F., Rylands, A.B., Mittermeier, R.A., Heymann, E., 2008. Oreonax flavicauda. IUCN Red List of Threatened...
  • D. Darriba et al.

    JModelTest 2: more models, new heuristics and parallel computing

    Nat. Methods

    (2012)
  • A.M. DeLuycker

    Notes on the yellow-tailed woolly monkey (Oreonax flavicauda) and its status in the protected forest of Alto Mayo, Northern Peru

    Primate Conserv.

    (2007)
  • A.J. Drummond et al.

    Bayesian phylogenetics with BEAUti and the BEAST 1.7

    Mol. Biol. Evol.

    (2012)
  • W.B. Figueiredo et al.

    Mitochondrial DNA sequences and the taxonomic status of Alouatta seniculus populations in northeastern Amazonia

    Neotrop. Primates

    (1998)
  • K. Finstermeier et al.

    A mitogenomic phylogeny of living primates

    PLoS ONE

    (2013)
  • J. Fooden

    A revision of the woolly monkeys (Genus Lagothrix)

    J. Mammal.

    (1963)
  • J.S. Friedlaender et al.

    Melanesian mtDNA complexity

    PLoS ONE

    (2007)
  • C. Gissi et al.

    Lineage-specific evolutionary rate in mammalian mtDNA

    Mol. Biol. Evol.

    (2000)
  • N.G. Gokey et al.

    Molecular analyses of mtDNA deletion mutations in microdissected skeletal muscle fibers from aged rhesus monkeys

    Aging Cell

    (2004)
  • C. Groves

    Primate Taxonomy

    (2001)
  • S. Guindon et al.

    A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood

    Syst. Biol.

    (2003)
  • Cited by (34)

    View all citing articles on Scopus
    View full text