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Correspondence PILOSA

The phylogenetic Dasypodidae


*
Dasypus kappleri
Dasypus septemcinctus
*
affinities of the extinct *
Dasypus hybridus
Dasypus novemcinctus FG

glyptodonts CINGULATA *
Dasypus yepesi
Dasypus sabanicola
Long-nosed
Armadillos
* 0.50 / - / - *
Dasypus novemcinctus US (Dasypodinae)
Frdric Delsuc1,*, Gillian C. Gibb1,2, Dasypus pilosus
Melanie Kuch3, Guillaume Billet4, Euphractus sexcinctus Hairy, Six-banded
* Chaetophractus villosus & Pichi Armadillos
Lionel Hautier1, John Southon5, 0.99 / 1.0 / 88 (Euphractinae)
Zaedyus pichiy
Jean-Marie Rouillard6, Chlamyphoridae * Chaetophractus vellerosus
*
Juan Carlos Fernicola7, 35 3 Mya Doedicurus sp. (Glyptodontinae)
[42-30]
Sergio F. Vizcano8, Ross D.E. MacPhee9, * Chlamyphorus truncatus Fairy Armadillos
and Hendrik N. Poinar3,* 0.97 / 1.0 / 69 Calyptophractus retusus (Chlamyphorinae)
Priodontes maximus
0.93 / 1.0 / 73 Tolypeutes tricinctus
*
Among the fossils of hitherto unknown PPCAT / PPPART / BPPART
* Tolypeutes matacus Giant,
Cabassous tatouay Three-banded
mammals that Darwin collected in South * * & Naked-tailed Armadillos
Cabassous chacoensis (Tolypeutinae)
America between 1832 and 1833 during Cabassous centralis
the Beagle expedition [1] were examples * Cabassous unicinctus
*
of the large, heavily armored herbivores
later known as glyptodonts. Ever since, E M L E M L E L E M L
glyptodonts have fascinated evolutionary Paleo. Eocene Oligocene Miocene Pli. P.
biologists because of their remarkable 66 62 59 56 48 38 34 28 23 16 12 5 3 0 Million years ago
skeletal adaptations and seemingly
isolated phylogenetic position even Figure 1. Phylogenetic position of glyptodonts.
within their natural group, the cingulate Phylogeny and molecular timescale of extant armadillos including the extinct glyptodont Doedi-
xenarthrans (armadillos and their allies curus sp. (in red). Bayesian chronogram was obtained using a rate-autocorrelated log-normal
[2]). In possessing a carapace comprised relaxed molecular clock model using PhyloBayes under the CAT-GTR-G mixture model with a
birth death prior on the diversification process, and six soft calibration constraints. Mean diver-
of fused osteoderms, the glyptodonts
gence dates and associated 95% credibility intervals are represented as node bars. Plain black
were clearly related to other cingulates, node bars indicated calibration constraints. The main geological periods follow Geological Time
but their precise phylogenetic position Scale of the Geological Society of America (E = Early, M = Middle, L = Late; Paleo. = Paleocene,
as suggested by morphology remains Pli. = Pliocene, P. = Pleistocene). Statistical support values obtained from three different phy-
unresolved [3,4]. To provide a molecular logenetic reconstruction methods (PPCAT: Bayesian Posterior Probability under the CAT-GTR+G
perspective on this issue, we designed mixture model; PPPART: Bayesian PP under the best partition model; BPPART: Maximum likelihood
Bootstrap Percentage under the best partition model) are indicated with stars corresponding to
sequence-capture baits using in silico
nodes with PP > 0.95 and BP > 90. The full chronogram and phylogram are provided in Figure S2.
reconstructed ancestral sequences and
successfully assembled the complete recent proposal that, despite numerous a recently assembled dataset
mitochondrial genome of Doedicurus differences in body size and carapace encompassing all modern xenarthran
sp., one of the largest glyptodonts. structure, glyptodonts do not constitute a species [5], we reconstructed, in silico, a
Our phylogenetic reconstructions sister-group to armadillos, as traditionally set of ancestral mitogenomic sequences,
establish that glyptodonts are in fact assumed [2], but are instead nested which permitted the synthesis of a
deeply nested within the armadillo within them [4,6]. This hypothesis is, set of target capture RNA baits. Baits
crown-group, representing a distinct however, based on a restricted set constructed in this way may allow for
subfamily (Glyptodontinae) within family of cranio-dental characters. Here, a more specific sequence capture
Chlamyphoridae [5]. Molecular dating we put this proposition to the test by of phylogenetically distant ancient
suggests that glyptodonts diverged analyzing the mitochondrial genome of a specimens than baits based solely
no earlier than around 35 million years specimen of the late surviving glyptodont on available modern sequences. This
ago, in good agreement with their fossil Doedicurus. One of the largest members permitted the reconstruction of a nearly
record. Our results highlight the derived of its clade, with an estimated body mass complete mitochondrial genome of
nature of the glyptodont morphotype, of ~1.5 tons [7], Doedicurus exhibited Doedicurus at 76x coverage. Illumina
one aspect of which is a spectacular numerous distinctive characters, reads mapping to the newly assembled
increase in body size until their extinction famously including a club-shaped, Doedicurus mitogenome were 45 base
at the end of the last ice age. armored tail adorned with spikes, pairs on average and displayed C-to-T
Although the phylogenetic unity of presumably used in intraspecific combat. damage patterns at both 3 and 5
order Cingulata has never been seriously Using ancient DNA (aDNA) extraction ends, characteristic of authentic aDNA.
questioned, how its three constituent techniques, we recovered endogenous We have ruled out the possibility of
groups (armadillos, glyptodonts, and DNA from a carapace fragment the inadvertent enrichment of nuclear
pampatheres) are related to one another (MACN Pv 6744) dated to 12,015 50 copies of mitochondrial origin (NUMTs)
14
has been difficult to resolve in fine detail. C radiocarbon years before present by performing additional phylogenetic
Of special interest in this regard is the (Supplemental information). Utilizing controls (Supplemental information).

Current Biology 26, R141R156, February 22, 2016 2016 Elsevier Ltd All rights reserved R155
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By comparing our ancient mitogenome the global congruence observed with 2. Hoffstetter, R. (1958). Xenarthra. In Trait de
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1
between glyptodonts and fairy armadillos in glyptodont body mass during the Institut des Sciences de lEvolution, UMR 5554,
(Supplemental information). Neogene (Supplemental Information). CNRS, IRD, EPHE, Universit de Montpellier,
Montpellier, France. 2Ecology Group, Institute
We estimate that glyptodonts diverged This inference is in line with the fossil of Agriculture and Environment, Massey
from Chlamyphorinae + Tolypeutinae record, which indicates that glyptodonts University, Palmerston North, New Zealand.
35 3 million years ago, close to the evolved from medium-sized forms in the 3
McMaster Ancient DNA Centre, Department
EoceneOligocene transition (Figure 1). Miocene (e.g., Propalaehoplophorus, of Anthropology, Biology and Biochemistry,
This molecular estimate is compatible ~80 kg) to become true megafauna in McMaster University, Hamilton, Canada.
4
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CNRS, Musum National dHistoire naturelle,
accepted glyptodont remains (Mustersan ~2,000 kg) before disappearing with most Universit Paris 06, Paris, France. 5Keck-
Glyptatelus osteoderms [8], ca. 3638 other South American large mammals Carbon Cycle AMS facility, Department of
million years old [9]). Tarsal bones from some 10,000 years ago [7]. Earth System Science, University of California,
the Early Eocene locality of Itabora Irvine, CA, USA. 6MYcroarray, Ann Arbor, MI
(Brazil), currently dated to more than SUPPLEMENTAL INFORMATION 48105, United States / Chemical Engineering
50 Myr [9]), have been interpreted as Department, University of Michigan, Ann Arbor,
Supplemental Information including results, ac- MI, USA. 7Consejo Nacional de Investigaciones
glyptodont, but the elements in question Cientficas y Tcnicas, Seccin Paleontologa
are better interpreted as belonging knowledgements, experimental procedures and
de Vertebrados, Museo Argentino de Ciencias
two figures can be found with this article online
to indeterminate dasypodoids [10]. Naturales Bernardino Rivadavia, Buenos Aires,
at http://dx.doi.org/10.1016/j.cub.2016.01.039.
According to our results, they might Argentina. 8Divisin Paleontologa Vertebrados,
belong to stem cingulates that evolved Facultad de Ciencias Naturales y Museo,
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R156 Current Biology 26, R141R156, February 22, 2016 2016 Elsevier Ltd All rights reserved