Ancient Mitogenomes Reveal the Evolutionary History and Biogeography of Sloths

doi:10.1016/j.cub.2019.05.043

. 2019 Jun 17;29(12):2031-2042.e6.

doi: 10.1016/j.cub.2019.05.043. Epub 2019 Jun 6.

Ancient Mitogenomes Reveal the Evolutionary History and Biogeography of Sloths

Affiliations

¹ Institut des Sciences de l'Evolution de Montpellier (ISEM), CNRS, IRD, EPHE, Université de Montpellier, Place Eugène Bataillon, 34095 Montpellier Cedex 5, France. Electronic address: [email protected].
² McMaster Ancient DNA Centre, Departments of Anthropology and Biochemistry, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada.
³ Institut des Sciences de l'Evolution de Montpellier (ISEM), CNRS, IRD, EPHE, Université de Montpellier, Place Eugène Bataillon, 34095 Montpellier Cedex 5, France; Wildlife and Ecology Group, School of Agriculture and Environment, Massey University, Centennial Drive, Hokowhitu, Palmerston North 4410, New Zealand.
⁴ McMaster Ancient DNA Centre, Departments of Anthropology and Biochemistry, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada; Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada.
⁵ Department of Anthropology, Trent University, 1600 West Bank Drive, Peterborough, ON K9L 0G2, Canada.
⁶ Instituto Superior de Estudios Sociales, CONICET-Instituto de Arqueología y Museo, Universidad Nacional de Tucumán, San Martín 1545, CP4000 San Miguel de Tucumán, Argentina.
⁷ The Mammoth Site, Hot Springs, Hot Springs, SD 57747, USA; East Tennessee State University Natural History Museum, 1212 Suncrest Drive, Johnson City, TN 37615, USA.
⁸ Bureau of Land Management, Utah State Office, 440 West 200 South #500, Salt Lake City, UT 84101, USA.
⁹ Division of Vertebrate Zoology/Mammalogy, American Museum of Natural History, Central Park West & 79th Street, New York, NY 10024, USA.
¹⁰ Centre de Recherche en Paléontologie - Paris (CR2P), UMR CNRS 7207, Sorbonne Université, Muséum National d'Histoire Naturelle, 57 Rue Cuvier, 75005 Paris, France.
¹¹ Institut des Sciences de l'Evolution de Montpellier (ISEM), CNRS, IRD, EPHE, Université de Montpellier, Place Eugène Bataillon, 34095 Montpellier Cedex 5, France; Mammal Section, Life Sciences, Vertebrate Division, The Natural History Museum, Cromwell Road, South Kensington, London SW7 5BD, UK.
¹² McMaster Ancient DNA Centre, Departments of Anthropology and Biochemistry, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada. Electronic address: [email protected].

PMID: 31178321
DOI: 10.1016/j.cub.2019.05.043

Free article

Ancient Mitogenomes Reveal the Evolutionary History and Biogeography of Sloths

Frédéric Delsuc et al. Curr Biol. 2019.

Free article

. 2019 Jun 17;29(12):2031-2042.e6.

doi: 10.1016/j.cub.2019.05.043. Epub 2019 Jun 6.

Authors

Affiliations

¹ Institut des Sciences de l'Evolution de Montpellier (ISEM), CNRS, IRD, EPHE, Université de Montpellier, Place Eugène Bataillon, 34095 Montpellier Cedex 5, France. Electronic address: [email protected].
² McMaster Ancient DNA Centre, Departments of Anthropology and Biochemistry, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada.
³ Institut des Sciences de l'Evolution de Montpellier (ISEM), CNRS, IRD, EPHE, Université de Montpellier, Place Eugène Bataillon, 34095 Montpellier Cedex 5, France; Wildlife and Ecology Group, School of Agriculture and Environment, Massey University, Centennial Drive, Hokowhitu, Palmerston North 4410, New Zealand.
⁴ McMaster Ancient DNA Centre, Departments of Anthropology and Biochemistry, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada; Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada.
⁵ Department of Anthropology, Trent University, 1600 West Bank Drive, Peterborough, ON K9L 0G2, Canada.
⁶ Instituto Superior de Estudios Sociales, CONICET-Instituto de Arqueología y Museo, Universidad Nacional de Tucumán, San Martín 1545, CP4000 San Miguel de Tucumán, Argentina.
⁷ The Mammoth Site, Hot Springs, Hot Springs, SD 57747, USA; East Tennessee State University Natural History Museum, 1212 Suncrest Drive, Johnson City, TN 37615, USA.
⁸ Bureau of Land Management, Utah State Office, 440 West 200 South #500, Salt Lake City, UT 84101, USA.
⁹ Division of Vertebrate Zoology/Mammalogy, American Museum of Natural History, Central Park West & 79th Street, New York, NY 10024, USA.
¹⁰ Centre de Recherche en Paléontologie - Paris (CR2P), UMR CNRS 7207, Sorbonne Université, Muséum National d'Histoire Naturelle, 57 Rue Cuvier, 75005 Paris, France.
¹¹ Institut des Sciences de l'Evolution de Montpellier (ISEM), CNRS, IRD, EPHE, Université de Montpellier, Place Eugène Bataillon, 34095 Montpellier Cedex 5, France; Mammal Section, Life Sciences, Vertebrate Division, The Natural History Museum, Cromwell Road, South Kensington, London SW7 5BD, UK.
¹² McMaster Ancient DNA Centre, Departments of Anthropology and Biochemistry, McMaster University, 1280 Main Street West, Hamilton, ON L8S 4L8, Canada. Electronic address: [email protected].

PMID: 31178321
DOI: 10.1016/j.cub.2019.05.043

Abstract

Living sloths represent two distinct lineages of small-sized mammals that independently evolved arboreality from terrestrial ancestors. The six extant species are the survivors of an evolutionary radiation marked by the extinction of large terrestrial forms at the end of the Quaternary. Until now, sloth evolutionary history has mainly been reconstructed from phylogenetic analyses of morphological characters. Here, we used ancient DNA methods to successfully sequence 10 extinct sloth mitogenomes encompassing all major lineages. This includes the iconic continental ground sloths Megatherium, Megalonyx, Mylodon, and Nothrotheriops and the smaller endemic Caribbean sloths Parocnus and Acratocnus. Phylogenetic analyses identify eight distinct lineages grouped in three well-supported clades, whose interrelationships are markedly incongruent with the currently accepted morphological topology. We show that recently extinct Caribbean sloths have a single origin but comprise two highly divergent lineages that are not directly related to living two-fingered sloths, which instead group with Mylodon. Moreover, living three-fingered sloths do not represent the sister group to all other sloths but are nested within a clade of extinct ground sloths including Megatherium, Megalonyx, and Nothrotheriops. Molecular dating also reveals that the eight newly recognized sloth families all originated between 36 and 28 million years ago (mya). The early divergence of recently extinct Caribbean sloths around 35 mya is consistent with the debated GAARlandia hypothesis postulating the existence at that time of a biogeographic connection between northern South America and the Greater Antilles. This new molecular phylogeny has major implications for reinterpreting sloth morphological evolution, biogeography, and diversification history.

Keywords: GAARlandia; ancient DNA; biogeography; convergence; extinct sloths; mitogenomics; molecular dating; morphology; phylogenetics.

PubMed Disclaimer

Cited by

An efficient pipeline for ancient DNA mapping and recovery of endogenous ancient DNA from whole-genome sequencing data.
Xu W, Lin Y, Zhao K, Li H, Tian Y, Ngatia JN, Ma Y, Sahu SK, Guo H, Guo X, Xu YC, Liu H, Kristiansen K, Lan T, Zhou X. Xu W, et al. Ecol Evol. 2020 Dec 21;11(1):390-401. doi: 10.1002/ece3.7056. eCollection 2021 Jan. Ecol Evol. 2020. PMID: 33437437 Free PMC article.
Bayesian Total-Evidence Dating Revisits Sloth Phylogeny and Biogeography: A Cautionary Tale on Morphological Clock Analyses.
Tejada JV, Antoine PO, Münch P, Billet G, Hautier L, Delsuc F, Condamine FL. Tejada JV, et al. Syst Biol. 2024 May 27;73(1):125-139. doi: 10.1093/sysbio/syad069. Syst Biol. 2024. PMID: 38041854 Free PMC article.
A macroevolutionary common-garden experiment reveals differentially evolvable bone organization levels in slow arboreal mammals.
Alfieri F, Botton-Divet L, Wölfer J, Nyakatura JA, Amson E. Alfieri F, et al. Commun Biol. 2023 Sep 28;6(1):995. doi: 10.1038/s42003-023-05371-3. Commun Biol. 2023. PMID: 37770611 Free PMC article.
Early Oligocene chinchilloid caviomorphs from Puerto Rico and the initial rodent colonization of the West Indies.
Marivaux L, Vélez-Juarbe J, Merzeraud G, Pujos F, Viñola López LW, Boivin M, Santos-Mercado H, Cruz EJ, Grajales A, Padilla J, Vélez-Rosado KI, Philippon M, Léticée JL, Münch P, Antoine PO. Marivaux L, et al. Proc Biol Sci. 2020 Feb 12;287(1920):20192806. doi: 10.1098/rspb.2019.2806. Epub 2020 Feb 12. Proc Biol Sci. 2020. PMID: 32075529 Free PMC article.
Assessing the relative performance of fast molecular dating methods for phylogenomic data.
Costa FP, Schrago CG, Mello B. Costa FP, et al. BMC Genomics. 2022 Dec 3;23(1):798. doi: 10.1186/s12864-022-09030-5. BMC Genomics. 2022. PMID: 36460948 Free PMC article.

See all "Cited by" articles

Publication types

Actions

MeSH terms

Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions
Actions

Substances

Actions

LinkOut - more resources

Full Text Sources
- Elsevier Science

Save citation to file

Email citation

Add to Collections

Add to My Bibliography

Your saved search

Create a file for external citation management software

Your RSS Feed

Ancient Mitogenomes Reveal the Evolutionary History and Biogeography of Sloths

Affiliations

Ancient Mitogenomes Reveal the Evolutionary History and Biogeography of Sloths

Authors

Affiliations

Abstract

Similar articles

Cited by

Publication types

MeSH terms

Substances

LinkOut - more resources

Full Text Sources

Abstract

Similar articles

Cited by

Publication types

MeSH terms

Substances

Related information

LinkOut - more resources

Full Text Sources