Ancient proteins resolve the evolutionary history of Darwin's South American ungulates

Frido Welker; Matthew J. Collins; Jessica A. Thomas; Marc Wadsley; Selina Brace; Enrico Cappellini; Samuel T. Turvey; Marcelo Reguero; Javier N. Gelfo; Alejandro Kramarz; Joachim Burger; Jane Thomas-Oates; David A. Ashford; Peter D. Ashton; Keri Rowsell; Duncan M. Porter; Benedikt Kessler; Roman Fischer; Carsten Baessmann; Stephanie Kaspar; Jesper V. Olsen; Patrick Kiley; James A. Elliott; Christian D. Kelstrup; Victoria Mullin; Michael Hofreiter; Eske Willerslev; Jean Jacques Hublin; Ludovic Orlando; Ian Barnes; Ross D E Macphee

doi:10.1038/nature14249

Ancient proteins resolve the evolutionary history of Darwin's South American ungulates

Frido Welker, Matthew J. Collins, Jessica A. Thomas, Marc Wadsley, Selina Brace, Enrico Cappellini, Samuel T. Turvey, Marcelo Reguero, Javier N. Gelfo, Alejandro Kramarz, Joachim Burger, Jane Thomas-Oates, David A. Ashford, Peter D. Ashton, Keri Rowsell, Duncan M. Porter, Benedikt Kessler, Roman Fischer, Carsten Baessmann, Stephanie KasparJesper V. Olsen, Patrick Kiley, James A. Elliott, Christian D. Kelstrup, Victoria Mullin, Michael Hofreiter, Eske Willerslev, Jean Jacques Hublin, Ludovic Orlando, Ian Barnes, Ross D E Macphee

Research output: Contribution to journal › Article › peer-review

Abstract

No large group of recently extinct placental mammals remains as evolutionarily cryptic as the approximately 280 genera grouped as South American native ungulates'. To Charles Darwin, who first collected their remains, they included perhaps the strangest animal[s] ever discovered'. Today, much like 180 years ago, it is no clearer whether they had one origin or several, arose before or after the Cretaceous/Palaeogene transition 66.2 million years ago, or are more likely to belong with the elephants and sirenians of superorder Afrotheria than with the euungulates (cattle, horses, and allies) of superorder Laurasiatheria. Morphology-based analyses have proved unconvincing because convergences are pervasive among unrelated ungulate-like placentals. Approaches using ancient DNA have also been unsuccessful, probably because of rapid DNA degradation in semitropical and temperate deposits. Here we apply proteomic analysis to screen bone samples of the Late Quaternary South American native ungulate taxa Toxodon (Notoungulata) and Macrauchenia (Litopterna) for phylogenetically informative protein sequences. For each ungulate, we obtain approximately 90% direct sequence coverage of type I collagen α1- and α2-chains, representing approximately 900 of 1,140 amino-acid residues for each subunit. A phylogeny is estimated from an alignment of these fossil sequences with collagen (I) gene transcripts from available mammalian genomes or mass spectrometrically derived sequence data obtained for this study. The resulting consensus tree agrees well with recent higher-level mammalian phylogenies. Toxodon and Macrauchenia form a monophyletic group whose sister taxon is not Afrotheria or any of its constituent clades as recently claimed, but instead crown Perissodactyla (horses, tapirs, and rhinoceroses). These results are consistent with the origin of at least some South American native ungulates from 'condylarths', a paraphyletic assembly of archaic placentals. With ongoing improvements in instrumentation and analytical procedures, proteomics may produce a revolution in systematics such as that achieved by genomics, but with the possibility of reaching much further back in time.

Original language	English
Pages (from-to)	81-84
Number of pages	4
Journal	Nature
Volume	522
Issue number	7554
Early online date	18 Mar 2015
DOIs	https://doi.org/10.1038/nature14249
Publication status	Published - 4 Jun 2015

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© 2015 The Authors. This is an author produced version of a paper published in Nature. Uploaded in accordance with the publisher's self-archiving policy.
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Welker, F., Collins, M. J., Thomas, J. A., Wadsley, M., Brace, S., Cappellini, E., Turvey, S. T., Reguero, M., Gelfo, J. N., Kramarz, A., Burger, J., Thomas-Oates, J., Ashford, D. A., Ashton, P. D., Rowsell, K., Porter, D. M., Kessler, B., Fischer, R., Baessmann, C., ... Macphee, R. D. E. (2015). Ancient proteins resolve the evolutionary history of Darwin's South American ungulates. Nature, 522(7554), 81-84. https://doi.org/10.1038/nature14249

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title = "Ancient proteins resolve the evolutionary history of Darwin's South American ungulates",

abstract = "No large group of recently extinct placental mammals remains as evolutionarily cryptic as the approximately 280 genera grouped as South American native ungulates'. To Charles Darwin, who first collected their remains, they included perhaps the strangest animal[s] ever discovered'. Today, much like 180 years ago, it is no clearer whether they had one origin or several, arose before or after the Cretaceous/Palaeogene transition 66.2 million years ago, or are more likely to belong with the elephants and sirenians of superorder Afrotheria than with the euungulates (cattle, horses, and allies) of superorder Laurasiatheria. Morphology-based analyses have proved unconvincing because convergences are pervasive among unrelated ungulate-like placentals. Approaches using ancient DNA have also been unsuccessful, probably because of rapid DNA degradation in semitropical and temperate deposits. Here we apply proteomic analysis to screen bone samples of the Late Quaternary South American native ungulate taxa Toxodon (Notoungulata) and Macrauchenia (Litopterna) for phylogenetically informative protein sequences. For each ungulate, we obtain approximately 90% direct sequence coverage of type I collagen α1- and α2-chains, representing approximately 900 of 1,140 amino-acid residues for each subunit. A phylogeny is estimated from an alignment of these fossil sequences with collagen (I) gene transcripts from available mammalian genomes or mass spectrometrically derived sequence data obtained for this study. The resulting consensus tree agrees well with recent higher-level mammalian phylogenies. Toxodon and Macrauchenia form a monophyletic group whose sister taxon is not Afrotheria or any of its constituent clades as recently claimed, but instead crown Perissodactyla (horses, tapirs, and rhinoceroses). These results are consistent with the origin of at least some South American native ungulates from 'condylarths', a paraphyletic assembly of archaic placentals. With ongoing improvements in instrumentation and analytical procedures, proteomics may produce a revolution in systematics such as that achieved by genomics, but with the possibility of reaching much further back in time.",

author = "Frido Welker and Collins, {Matthew J.} and Thomas, {Jessica A.} and Marc Wadsley and Selina Brace and Enrico Cappellini and Turvey, {Samuel T.} and Marcelo Reguero and Gelfo, {Javier N.} and Alejandro Kramarz and Joachim Burger and Jane Thomas-Oates and Ashford, {David A.} and Ashton, {Peter D.} and Keri Rowsell and Porter, {Duncan M.} and Benedikt Kessler and Roman Fischer and Carsten Baessmann and Stephanie Kaspar and Olsen, {Jesper V.} and Patrick Kiley and Elliott, {James A.} and Kelstrup, {Christian D.} and Victoria Mullin and Michael Hofreiter and Eske Willerslev and Hublin, {Jean Jacques} and Ludovic Orlando and Ian Barnes and Macphee, {Ross D E}",

note = "{\textcopyright} 2015 The Authors. This is an author produced version of a paper published in Nature. Uploaded in accordance with the publisher's self-archiving policy.",

year = "2015",

month = jun,

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doi = "10.1038/nature14249",

language = "English",

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Welker, F, Collins, MJ , Thomas, JA, Wadsley, M, Brace, S, Cappellini, E, Turvey, ST, Reguero, M, Gelfo, JN, Kramarz, A, Burger, J, Thomas-Oates, J, Ashford, DA, Ashton, PD, Rowsell, K, Porter, DM, Kessler, B, Fischer, R, Baessmann, C, Kaspar, S, Olsen, JV, Kiley, P, Elliott, JA, Kelstrup, CD, Mullin, V, Hofreiter, M, Willerslev, E, Hublin, JJ, Orlando, L, Barnes, I & Macphee, RDE 2015, 'Ancient proteins resolve the evolutionary history of Darwin's South American ungulates', Nature, vol. 522, no. 7554, pp. 81-84. https://doi.org/10.1038/nature14249

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AU - Welker, Frido

AU - Collins, Matthew J.

AU - Thomas, Jessica A.

AU - Wadsley, Marc

AU - Brace, Selina

AU - Cappellini, Enrico

AU - Turvey, Samuel T.

AU - Reguero, Marcelo

AU - Gelfo, Javier N.

AU - Kramarz, Alejandro

AU - Burger, Joachim

AU - Thomas-Oates, Jane

AU - Ashford, David A.

AU - Ashton, Peter D.

AU - Rowsell, Keri

AU - Porter, Duncan M.

AU - Kessler, Benedikt

AU - Fischer, Roman

AU - Baessmann, Carsten

AU - Kaspar, Stephanie

AU - Olsen, Jesper V.

AU - Kiley, Patrick

AU - Elliott, James A.

AU - Kelstrup, Christian D.

AU - Mullin, Victoria

AU - Hofreiter, Michael

AU - Willerslev, Eske

AU - Hublin, Jean Jacques

AU - Orlando, Ludovic

AU - Barnes, Ian

AU - Macphee, Ross D E

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N2 - No large group of recently extinct placental mammals remains as evolutionarily cryptic as the approximately 280 genera grouped as South American native ungulates'. To Charles Darwin, who first collected their remains, they included perhaps the strangest animal[s] ever discovered'. Today, much like 180 years ago, it is no clearer whether they had one origin or several, arose before or after the Cretaceous/Palaeogene transition 66.2 million years ago, or are more likely to belong with the elephants and sirenians of superorder Afrotheria than with the euungulates (cattle, horses, and allies) of superorder Laurasiatheria. Morphology-based analyses have proved unconvincing because convergences are pervasive among unrelated ungulate-like placentals. Approaches using ancient DNA have also been unsuccessful, probably because of rapid DNA degradation in semitropical and temperate deposits. Here we apply proteomic analysis to screen bone samples of the Late Quaternary South American native ungulate taxa Toxodon (Notoungulata) and Macrauchenia (Litopterna) for phylogenetically informative protein sequences. For each ungulate, we obtain approximately 90% direct sequence coverage of type I collagen α1- and α2-chains, representing approximately 900 of 1,140 amino-acid residues for each subunit. A phylogeny is estimated from an alignment of these fossil sequences with collagen (I) gene transcripts from available mammalian genomes or mass spectrometrically derived sequence data obtained for this study. The resulting consensus tree agrees well with recent higher-level mammalian phylogenies. Toxodon and Macrauchenia form a monophyletic group whose sister taxon is not Afrotheria or any of its constituent clades as recently claimed, but instead crown Perissodactyla (horses, tapirs, and rhinoceroses). These results are consistent with the origin of at least some South American native ungulates from 'condylarths', a paraphyletic assembly of archaic placentals. With ongoing improvements in instrumentation and analytical procedures, proteomics may produce a revolution in systematics such as that achieved by genomics, but with the possibility of reaching much further back in time.

AB - No large group of recently extinct placental mammals remains as evolutionarily cryptic as the approximately 280 genera grouped as South American native ungulates'. To Charles Darwin, who first collected their remains, they included perhaps the strangest animal[s] ever discovered'. Today, much like 180 years ago, it is no clearer whether they had one origin or several, arose before or after the Cretaceous/Palaeogene transition 66.2 million years ago, or are more likely to belong with the elephants and sirenians of superorder Afrotheria than with the euungulates (cattle, horses, and allies) of superorder Laurasiatheria. Morphology-based analyses have proved unconvincing because convergences are pervasive among unrelated ungulate-like placentals. Approaches using ancient DNA have also been unsuccessful, probably because of rapid DNA degradation in semitropical and temperate deposits. Here we apply proteomic analysis to screen bone samples of the Late Quaternary South American native ungulate taxa Toxodon (Notoungulata) and Macrauchenia (Litopterna) for phylogenetically informative protein sequences. For each ungulate, we obtain approximately 90% direct sequence coverage of type I collagen α1- and α2-chains, representing approximately 900 of 1,140 amino-acid residues for each subunit. A phylogeny is estimated from an alignment of these fossil sequences with collagen (I) gene transcripts from available mammalian genomes or mass spectrometrically derived sequence data obtained for this study. The resulting consensus tree agrees well with recent higher-level mammalian phylogenies. Toxodon and Macrauchenia form a monophyletic group whose sister taxon is not Afrotheria or any of its constituent clades as recently claimed, but instead crown Perissodactyla (horses, tapirs, and rhinoceroses). These results are consistent with the origin of at least some South American native ungulates from 'condylarths', a paraphyletic assembly of archaic placentals. With ongoing improvements in instrumentation and analytical procedures, proteomics may produce a revolution in systematics such as that achieved by genomics, but with the possibility of reaching much further back in time.

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Ancient proteins resolve the evolutionary history of Darwin's South American ungulates

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Matthew James Collins, FBA

Jane Elizabeth Thomas-Oates

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Ancient proteins resolve the evolutionary history of Darwin's South American ungulates

Abstract

Bibliographical note

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Matthew James Collins, FBA

Jane Elizabeth Thomas-Oates

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