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Collagen Sequence Analysis of the Extinct Giant Ground Sloths Lestodon and Megatherium.

Buckley M, Fariña RA, Lawless C, Tambusso PS, Varela L, Carlini AA, Powell JE, Martinez JG - PLoS ONE (2015)

Bottom Line: However, proteomics results generate partial sequence information that could impact upon the phylogenetic placement that has not been appropriately tested.The ground sloths were placed as sister taxa to extant sloths, but with a closer relationship between Lestodon and the extant sloths than the basal Megatherium.These results highlight that proteomics methods could yield plausible phylogenies that share similarities with other methods, but have the potential to be more useful in fossils beyond the limits of ancient DNA survival.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, Manchester Interdisciplinary Biocentre, The University of Manchester, Manchester, United Kingdom.

ABSTRACT
For over 200 years, fossils of bizarre extinct creatures have been described from the Americas that have ranged from giant ground sloths to the 'native' South American ungulates, groups of mammals that evolved in relative isolation on South America. Ground sloths belong to the South American xenarthrans, a group with modern although morphologically and ecologically very different representatives (anteaters, armadillos and sloths), which has been proposed to be one of the four main eutherian clades. Recently, proteomics analyses of bone collagen have recently been used to yield a molecular phylogeny for a range of mammals including the unusual 'Malagasy aardvark' shown to be most closely related to the afrotherian tenrecs, and the south American ungulates supporting their morphological association with condylarths. However, proteomics results generate partial sequence information that could impact upon the phylogenetic placement that has not been appropriately tested. For comparison, this paper examines the phylogenetic potential of proteomics-based sequencing through the analysis of collagen extracted from two extinct giant ground sloths, Lestodon and Megatherium. The ground sloths were placed as sister taxa to extant sloths, but with a closer relationship between Lestodon and the extant sloths than the basal Megatherium. These results highlight that proteomics methods could yield plausible phylogenies that share similarities with other methods, but have the potential to be more useful in fossils beyond the limits of ancient DNA survival.

No MeSH data available.


Phylogenetic analyses of COL1A2 sequences of eutherian mammals including the extinct South American native ungulates and two extinct ground sloths Lestodon and Megatherium in comparison to extant sloths Bradypus and Choloepus showing (A) Maximum Likelihood analysis of consensus peptide matches observed in the PMF, (B) Maximum Likelihood of peptide matches observed in the PMF from either specimen, (C) Maximum Likelihood of the alpha 2 (I) sequences only, using the Ensembl Choloepus sequence and (D) Bayes analysis of consensus peptide matches observed in the PMF.
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pone.0139611.g003: Phylogenetic analyses of COL1A2 sequences of eutherian mammals including the extinct South American native ungulates and two extinct ground sloths Lestodon and Megatherium in comparison to extant sloths Bradypus and Choloepus showing (A) Maximum Likelihood analysis of consensus peptide matches observed in the PMF, (B) Maximum Likelihood of peptide matches observed in the PMF from either specimen, (C) Maximum Likelihood of the alpha 2 (I) sequences only, using the Ensembl Choloepus sequence and (D) Bayes analysis of consensus peptide matches observed in the PMF.

Mentions: Previous studies on the phylogenetic relationships of sloths showed a clear distinction between the two extant families (Megalonychidae and Bradypodidae) well supported by both morphological and molecular differences. In particular, Sarich [44] found considerable evolutionary distance between the albumins of the two genera. Previous aDNA studies on extinct sloths [19, 45] indicated a relationship between, on the one hand, Mylodon darwinii (Mylodontidae) and Choloepus (Megalonychidae), and, on the other, between Nothrotheriops shastensis (Megatheriidae) and Bradypus spp. (Bradypodidae). However, this assumption was questioned by more recent studies [46]. The inclusion of Mylodontidae as the sister taxon of Megalonychidae does not support the monophyly of Megatherioidea (including the megatheriids, nothrotheriids and megalonychids) as in the widely accepted phylogenetic reconstruction proposals by Gaudin [47] based on craniodental morphological traits. Although in that paper the grouping of Mylodontidae and Megalonychidae is not supported, most of the molecular phylogenetic reconstructions show an allied relation of Mylodon and Choloepus [19, 45, 46, 48], even with the inclusion of other Megatherioidea as Nothrotheriops [20]. Moreover, Gaudin [47] states that the hypothesis of a close relation of Choloepus with mylodontids cannot be statistically rejected and that the position of Choloepus within megalonychids could not unambiguously be resolved. More recently, an aDNA phylogeny by Clack et al. [49] placed Choloepus close to Mylodon, with Bradypus occupying a derived position among megalonychids and Nothrotheriops occupying a basal position as the sister group of all the mentioned sloths. Our study shows a relationship between the extant and extinct sloths not previously proposed by molecular or morphological phylogenies, since both extant sloths appear as sister taxa with Lestodon (Mylodontidae) and Megatherium (Megatheriidae) forming a successive grade. As noted before, a basal position of Megatheriidae (Nothrotheriops) is reported by Clack et al. [49] but the Mylodontidae groups with Choloepus, as most aDNA phylogenies. The discrepancies between the collagen, aDNA and morphological phylogenies could be due to the incompleteness of the collagen data, as alluded to earlier. One of the limitations of proteomics-based approaches to phylogenetic reconstruction that needs to be addressed is deciding on an appropriate level of confidence—in this case we have chosen to rely on a peptide score equivalent to the highest false positive match in order to accommodate for differences in the quality of each analysis; this approach is likely to unnecessarily reduce sequence coverage, but comparison of the phylogenies recovered here (e.g., Fig 3A and 3B) imply that the variation in percentage sequence coverage alone in this study is not an issue. Also, the fact that the MALDI fingerprints also show greater similarity between the two extant taxa implies that perhaps it is more likely related to the more limited source information of the collagen-based approach in relation to the other methods. In regard to the phylogenetic relationships of the fossil sloths, belonging to Mylodontidae and Megatheriidae, it should be noted that the absence of northotheriids in our analysis leaves uncertain the possible placement of this taxon, which has been closely associated to Megatheriidae in most morphological studies [47, 50].


Collagen Sequence Analysis of the Extinct Giant Ground Sloths Lestodon and Megatherium.

Buckley M, Fariña RA, Lawless C, Tambusso PS, Varela L, Carlini AA, Powell JE, Martinez JG - PLoS ONE (2015)

Phylogenetic analyses of COL1A2 sequences of eutherian mammals including the extinct South American native ungulates and two extinct ground sloths Lestodon and Megatherium in comparison to extant sloths Bradypus and Choloepus showing (A) Maximum Likelihood analysis of consensus peptide matches observed in the PMF, (B) Maximum Likelihood of peptide matches observed in the PMF from either specimen, (C) Maximum Likelihood of the alpha 2 (I) sequences only, using the Ensembl Choloepus sequence and (D) Bayes analysis of consensus peptide matches observed in the PMF.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4634953&req=5

pone.0139611.g003: Phylogenetic analyses of COL1A2 sequences of eutherian mammals including the extinct South American native ungulates and two extinct ground sloths Lestodon and Megatherium in comparison to extant sloths Bradypus and Choloepus showing (A) Maximum Likelihood analysis of consensus peptide matches observed in the PMF, (B) Maximum Likelihood of peptide matches observed in the PMF from either specimen, (C) Maximum Likelihood of the alpha 2 (I) sequences only, using the Ensembl Choloepus sequence and (D) Bayes analysis of consensus peptide matches observed in the PMF.
Mentions: Previous studies on the phylogenetic relationships of sloths showed a clear distinction between the two extant families (Megalonychidae and Bradypodidae) well supported by both morphological and molecular differences. In particular, Sarich [44] found considerable evolutionary distance between the albumins of the two genera. Previous aDNA studies on extinct sloths [19, 45] indicated a relationship between, on the one hand, Mylodon darwinii (Mylodontidae) and Choloepus (Megalonychidae), and, on the other, between Nothrotheriops shastensis (Megatheriidae) and Bradypus spp. (Bradypodidae). However, this assumption was questioned by more recent studies [46]. The inclusion of Mylodontidae as the sister taxon of Megalonychidae does not support the monophyly of Megatherioidea (including the megatheriids, nothrotheriids and megalonychids) as in the widely accepted phylogenetic reconstruction proposals by Gaudin [47] based on craniodental morphological traits. Although in that paper the grouping of Mylodontidae and Megalonychidae is not supported, most of the molecular phylogenetic reconstructions show an allied relation of Mylodon and Choloepus [19, 45, 46, 48], even with the inclusion of other Megatherioidea as Nothrotheriops [20]. Moreover, Gaudin [47] states that the hypothesis of a close relation of Choloepus with mylodontids cannot be statistically rejected and that the position of Choloepus within megalonychids could not unambiguously be resolved. More recently, an aDNA phylogeny by Clack et al. [49] placed Choloepus close to Mylodon, with Bradypus occupying a derived position among megalonychids and Nothrotheriops occupying a basal position as the sister group of all the mentioned sloths. Our study shows a relationship between the extant and extinct sloths not previously proposed by molecular or morphological phylogenies, since both extant sloths appear as sister taxa with Lestodon (Mylodontidae) and Megatherium (Megatheriidae) forming a successive grade. As noted before, a basal position of Megatheriidae (Nothrotheriops) is reported by Clack et al. [49] but the Mylodontidae groups with Choloepus, as most aDNA phylogenies. The discrepancies between the collagen, aDNA and morphological phylogenies could be due to the incompleteness of the collagen data, as alluded to earlier. One of the limitations of proteomics-based approaches to phylogenetic reconstruction that needs to be addressed is deciding on an appropriate level of confidence—in this case we have chosen to rely on a peptide score equivalent to the highest false positive match in order to accommodate for differences in the quality of each analysis; this approach is likely to unnecessarily reduce sequence coverage, but comparison of the phylogenies recovered here (e.g., Fig 3A and 3B) imply that the variation in percentage sequence coverage alone in this study is not an issue. Also, the fact that the MALDI fingerprints also show greater similarity between the two extant taxa implies that perhaps it is more likely related to the more limited source information of the collagen-based approach in relation to the other methods. In regard to the phylogenetic relationships of the fossil sloths, belonging to Mylodontidae and Megatheriidae, it should be noted that the absence of northotheriids in our analysis leaves uncertain the possible placement of this taxon, which has been closely associated to Megatheriidae in most morphological studies [47, 50].

Bottom Line: However, proteomics results generate partial sequence information that could impact upon the phylogenetic placement that has not been appropriately tested.The ground sloths were placed as sister taxa to extant sloths, but with a closer relationship between Lestodon and the extant sloths than the basal Megatherium.These results highlight that proteomics methods could yield plausible phylogenies that share similarities with other methods, but have the potential to be more useful in fossils beyond the limits of ancient DNA survival.

View Article: PubMed Central - PubMed

Affiliation: Faculty of Life Sciences, Manchester Interdisciplinary Biocentre, The University of Manchester, Manchester, United Kingdom.

ABSTRACT
For over 200 years, fossils of bizarre extinct creatures have been described from the Americas that have ranged from giant ground sloths to the 'native' South American ungulates, groups of mammals that evolved in relative isolation on South America. Ground sloths belong to the South American xenarthrans, a group with modern although morphologically and ecologically very different representatives (anteaters, armadillos and sloths), which has been proposed to be one of the four main eutherian clades. Recently, proteomics analyses of bone collagen have recently been used to yield a molecular phylogeny for a range of mammals including the unusual 'Malagasy aardvark' shown to be most closely related to the afrotherian tenrecs, and the south American ungulates supporting their morphological association with condylarths. However, proteomics results generate partial sequence information that could impact upon the phylogenetic placement that has not been appropriately tested. For comparison, this paper examines the phylogenetic potential of proteomics-based sequencing through the analysis of collagen extracted from two extinct giant ground sloths, Lestodon and Megatherium. The ground sloths were placed as sister taxa to extant sloths, but with a closer relationship between Lestodon and the extant sloths than the basal Megatherium. These results highlight that proteomics methods could yield plausible phylogenies that share similarities with other methods, but have the potential to be more useful in fossils beyond the limits of ancient DNA survival.

No MeSH data available.