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1 advances.sciencemag.org/cgi/content/full/1/10/e /dc1 The PDF file includes: Supplementary Materials for The burrowing origin of modern snakes Hongyu Yi and Mark A. Norell Published 27 November 2015, Sci. Adv. 1, e (2015) DOI: /sciadv Materials and Methods Fig. S1. Vestibular shape of all samples. Fig. S2. Placement of shape variables. Fig. S3. Regression of centroid size to scores of principal component 1. Fig. S4. Distribution of shape variables reconstructed for the hypothetical ancestor of crown snakes. Fig. S5. Principal components analyses of vestibular shape. Fig. S6. Missing data in shape variables. Fig. S7. An alternative phylogeny for all samples. Table S1. Taxon sampling in the three habitat groups. Table S2. MANOVA test of Procrustes coordinates among the three habitat groups. Table S3. Scores of the first two principal components. Table S4. Accuracy of the linear discriminant function analysis. Table S5. Habit predictions for D. patagonica and the hypothetical ancestor of modern snakes. Table S6. Habit predictions for D. patagonica and the hypothetical ancestor of modern snakes. Table S7. Habit predictions for D. patagonica and the hypothetical ancestor of modern snakes. Table S8. CT scanning parameters*. Reference (32)
2 Materials and Methods: X-ray Computed Tomography (CT) was completed at the American Museum of Natural History. Among the 44 samples, 37 were scanned in a GE v tome x dual-tube CT scanner. We CT scanned Dinilysia patagonica (MACN-RN 1014) at the resolution of 26 μm, and X-ray of 170 kv and 130 ma. Modern samples include dry skeletons and alcohol-preserved specimens, and were scanned at kv and ma (Table S8). We obtained CT data of seven samples (non-amnh specimens) from the CT lab of the University of Texas, Austin. We built virtual models of the inner ear for all samples; the models in PLY format are deposited in MorphoBank (29) Project We used six type-2 landmarks (17) and 22 semilandmarks placed along the lateral surface of the vestibule and the medial surface of the lateral semicircular canal (Fig. S2). Vestibule expansion or shrinkage was captured with the curvature of the vestibule, and the distance between the vestibule and lateral semicircular canal. The six type 2 landmarks are: intersection of the vestibule and lateral semicircular canal (c0-0: [curve number]-[landmark number]), intersection of the vestibule and utricle (c0-15), medial intersection of the posterior and lateral semicircular canals (c1-0), intersection of the lateral semicircular canal and lateral ampulla (c1-9), intersection of the anterior and lateral ampullae (s0), and intersection of the anterior and posterior semicircular canals (s1). The semilandmarks are equidistant points along two curves surrounding the vestibule and lateral semicircular canal, automatically placed in Landmark Editor 3.6 (32) (Fig. S2D). The six type-2 landmarks are defined as intersection points between two homologous structures, but they can move along the sutures without additional position
3 constraint. To increase the consistency in landmark placement, we incorporated a reference plane (Fig. S2B) the plane contains landmarks c0-0, c0-15, and s0, and intersects as much of the medial line of the lateral semicircular canal as possible. In some samples, taxon-specific morphologies can render the position of some landmarks uncertain or inapplicable. We define a landmark as missing when its position cannot be determined due to separation of two anatomical structures that are fused in other samples, or vice versa. For instance, the posterior and lateral semicircular canals are connected in most squamates, but separate in Varanus indicus (Fig. S6). In this case, landmark c1-0 was first placed at an approximate position on the lateral semicircular canal, and later estimated using the position of landmark c1-0 in the average Procrustes shape of all samples. After generalized Procrustes analysis, the dataset contains no missing data of shape coordinates. Generalized Procrustes Analysis aligns the 28 landmarks and semilandmarks of all samples. We used the semilandmark sliding algorithm that minimizes bending energy in the R program Geomorph V (30). Phylogenetic signal is insignificant in the dataset (p = 0.28, iteration = 10), tested by permuting Procrustes shape coordinates of terminal taxa on the snake cladogram (Fig. 1G). In contrast, signal for function (habitat) is significant. MANOVA test using the Procrustes coordinates returned significant difference among the three habitat groups (p = 0.01, Table S2). Principal component analysis extracts major shape variations as principal components (PCs) in the order of percent total variance explained. The first six PCs explain 87 percent of the total variance, of which 47 percent is explained by PC1. Linear
4 relationship between centroid size of Procrustes shapes and PC1 score was insignificant in a regression test (p = 0.09 for slope = 0; Fig. S3). Linear discriminant analysis was performed among the three habit groups to describe between-group shape separation. The group memberships of Dinilysia patagonica and the hypothetical ancestor were both assigned as unknown in the input data. The linear discriminant analysis then predicted both taxa to belong to the burrowing group. We used standard statistical software (Minitab 17) for the linear discriminant function analysis. We mapped the shape coordinates on the phylogenies using squared-change parsimony, implemented in MorphoJ (31). For the hypothetical ancestor of crown snakes, shape coordinates of the inner ear were reconstructed with and without Dinilysia patagonica. For both reconstructions, the hypothetical ancestor was predicted as a burrower using principal component analysis (Fig. 3; Fig. S5) and linear discriminant analysis (Table S5 to 7).
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8 Fig. S1. Vestibular shape of all samples. (A) Specimen (1) to (12). (B) Specimen (13) to (24). (C) Specimen (25) to (36). (D) Specimen (37) to (44). Not to scale.
9 Fig. S2. Placement of shape variables. (A) General anatomy of the snake bony labyrinth represented by Ptyas mucosa. (B) Virtual model of the bony labyrinth and the reference plane. (C) Landmarks s0 and s1, and two surface curves consisting of semilandmarks. (D) Landmarks: c0-0, c0-15, c1-0, and c1-9. Semilandmarks: c0-1 to c0-14, and c1-1 to c1-8. Not to scale.
10 Fig. S3. Regression of centroid size to scores of principal component 1. Blue squares are aquatic species; black triangles are generalists; red dots are burrowing species. The cross is Dinilysia patagonica.
11 Fig. S4. Distribution of shape variables reconstructed for the hypothetical ancestor of crown snakes. (A) the hypothetical ancestor reconstructed with Dinilysia patagonica. (B) The hypothetical ancestor reconstructed without Dinilysia patagonica.
12 Fig. S5. Principal components analyses of vestibular shape. (A) The hypothetical ancestor of crown snakes (45) was reconstructed with Dinilysia patagonica (44). (B) The hypothetical ancestor of crown snakes (45) was reconstructed without Dinilysia patagonica (44). Taxon list: 1. Laticauda colubrina, 2. Aipysurus laevis, 3. Laticauda semifasciata, 4. Acrochordus javanicus, 5. Platecarpus coryphaeus, 6. Hydrophis caerulescens, 7. Heloderma suspectum, 8. Lampropeltis getulus, 9. Anguis fragilis, 10. Varanus indicus, 11. Pareas hamptoni, 12. Lamprophis lineatus, 13. Corallus caninus,
13 14. Python molurus, 15. Naja naja, 16. Eunectes murinus, 17. Vermicella annulata, 18. Trimeresurus stejnegeri, 19. Rhinobothryum lentiginosum, 20. Echiopsis curta, 21. Ptyas mucosa, 22. Boiga irregularis, 23. Pygopus nigriceps, 24. Chrysopelea ornata, 25. Aprasia pulchella, 26. Cylindrophis maculatus, 27. Uropeltis ceylanica, 28. Anniella pulchra, 29. Typhlops jamaicensis, 30. Eryx colubrinus, 31. Anilius scytale, 32. Loxocemus bicolor, 33. Heterodon platirhinos, 34. Simoselaps bertholdi, 35. Rhinotyphlops caecus, 36. Sonora semiannulata, 37. Exiliboa placata, 38. Achalinus spinalis, 39. Typhlosaurus lineatus, 40. Rhinophis philippinus, 41. Xenopeltis unicolor, 42. Dibamus novaeguineae, 43. Bipes canaliculatus, 44. Dinilysia patagonica, and 45. the hypothetical ancestor of crown snakes.
14 Fig. S6. Missing data in shape variables. (A) The inner ear of Ptyas mucosa in lateral view; the posterior and lateral semicircular canals are connected. (B) The inner ear of Varanus indicus in lateral view; the posterior and lateral semicircular canals are separate. (C) Close-up view of the lateral semicircular canal in Varanus indicus. Not to scale.
15 Fig. S7. An alternative phylogeny for all samples. Mosasauria is the sister group to all snakes in this phylogeny adapted from refs No. 7 and 22.
16 Table S1. Taxon sampling in the three habitat groups. Snakes are listed separately from lizards and amphisbaenians. Daggers denote fossils. AQUATIC GENERALIST BURROWING SNAKES Laticauda colubrina Lampropeltis getulus Cylindrophis maculatus Aipysurus laevis Pareas hamptoni Uropeltis ceylanica Laticauda semifasciata Lamprophis lineatus Typhlops jamaicensis Acrochordus javanicus Corallus caninus Eryx colubrinus Hydrophis caerulescens Python molurus Anilius scytale Naja naja Loxocemus bicolor Eunectes murinus Heterodon platirhinos Vermicella annulata Simoselaps bertholdi Trimeresurus stejnegeri Rhinotyphlops caecus Rhinobothryum lentiginosum Sonora semiannulata Echiopsis curta Exiliboa placata Ptyas mucosa Achalinus spinalis Boiga irregularis Rhinophis philippinus Chrysopelea ornata Xenopeltis unicolor Dinilysia patagonica NON-SNAKE SQUAMATES Platecarpus coryphaeus Heloderma suspectum Aprasia pulchella Anguis fragilis Anniella pulchra Varanus indicus Typhlosaurus lineatus Pygopus nigriceps Dibamus novaeguineae Bipes canaliculatus
17 Table S2. MANOVA test of Procrustes coordinates among the three habitat groups. df SS.obs MS P.val Habitat groups Total NA
18 Table S3. Scores of the first two principal components. Taxon PC1 (47%) PC2 (17%) 1 Aprasia pulchella Cylindrophis maculatus Heloderma suspectum Lampropeltis getulus Laticauda colubrina Uropeltis ceylanica Aipysurus laevis Anguis fragilis Anniella pulchra Laticauda semifasciata Varanus indicus Pareas hamptoni Lamprophis lineatus Corallus caninus Typhlops jamaicensis Python molurus Naja naja Eryx colubrinus Anilius scytale Loxocemus bicolor Heterodon platirhinos Eunectes murinus Vermicella annulata Trimeresurus stejnegeri Simoselaps bertholdi Rhinotyphlops caecus Rhinobothryum lentiginosum Sonora semiannulata Exiliboa placata Echiopsis curta Acrochordus javanicus Achalinus spinalis Ptyas mucosa Platecarpus coryphaeus Typhlosaurus lineatus Rhinophis philippinus Hydrophis caerulescens Boiga irregularis Pygopus nigriceps Xenopeltis unicolor Dibamus novaeguineae
19 42 Chrysopelea ornata Bipes canaliculatus Dinilysia patagonica Hypothetical ancestor of crown snakes (Reconstructed with Dinilysia patagonica)
20 Table S4. Accuracy of the linear discriminant function analysis. Predicted group True group Aquatic Generalists Burrowing Aquatic Generalists Burrowing Total N N correct N correct proportion N = 43 N correct = 29 Proportion correct = 0.674
21 Table S5. Habit predictions for D. patagonica and the hypothetical ancestor of modern snakes. The hypothetical ancestor was reconstructed with D. patagonica. Observation Predicted Groups From Group Squared Distance Probability Dinilysia Burrowing Aquatic patagonica Generalists Burrowing Hypothetical Burrowing Aquatic ancestor Generalists Burrowing
22 Table S6. Habit predictions for D. patagonica and the hypothetical ancestor of modern snakes. The hypothetical ancestor was reconstructed without D. patagonica). Observation Predicted Groups From Group Squared Distance Probability Dinilysia Burrowing Aquatic patagonica Generalists Burrowing Hypothetical Burrowing Aquatic ancestor Generalists Burrowing
23 Table S7. Habit predictions for D. patagonica and the hypothetical ancestor of modern snakes. The hypothetical ancestor was reconstructed with D. patagonica and an alternative phylogeny in fig. S7. Observation Predicted Groups From Group Squared Distance Probability Dinilysia Burrowing Aquatic patagonica Generalists Burrowing Hypothetical Burrowing Aquatic ancestor Generalists Burrowing
24 Table S8. CT scanning parameters*. Taxon Specimen number Voxel size (x=y, mm) 1 Laticauda colubrina Voxel size (z, mm) Filter Scanning lab AMNH R N AMNH 2 Aipysurus laevis AMNH R mm Cu** AMNH 3 Laticauda AMNH R mm AMNH semifasciata Cu 4 Acrochordus AMNH R N AMNH javanicus 5 Platecarpus AMNH FM mm AMNH coryphaeus Cu 6 Hydrophis AMNH R mm AMNH caerulescens Cu 7 Heloderma AMNH R N AMNH suspectum 8 Lampropeltis AMNH R mm AMNH getulus Cu 9 Anguis fragilis AMNH R N AMNH 10 Varanus indicus AMNH R N AMNH 11 Pareas AMNH R N AMNH hamptoni 12 Lamprophis AMNH R N AMNH lineatus 13 Corallus AMNH R mm AMNH caninus Cu 14 Python molurus TNHC, to be N AMNH accessioned 15 Naja naja FMNH N UTCT 16 Eunectes AMNH R N AMNH murinus 17 Vermicella AMNH R N AMNH annulata 18 Trimeresurus AMNH R N AMNH stejnegeri 19 Rhinobothryum AMNH R N AMNH lentiginosum 20 Echiopsis AMNH R N AMNH curta 21 Ptyas mucosa AMNH R N AMNH 22 Boiga AMNH R mm AMNH
25 irregularis Cu 23 Pygopus AMNH R N AMNH nigriceps 24 Chrysopelea AMNH R N AMNH ornata 25 Aprasia AMNH R N AMNH pulchella 26 Cylindrophis AMNH R N AMNH maculatus 27 Uropeltis AMNH R N AMNH ceylanica 28 Anniella AMNH R N AMNH pulchra 29 Typhlops USNM N UTCT jamaicensis 30 Eryx colubrinus FMNH N UTCT 31 Anilius scytale USNM N UTCT 32 Loxocemus FMNH N UTCT bicolor 33 Heterodon FMNH N UTCT platirhinos 34 Simoselaps AMNH R N AMNH bertholdi 35 Rhinotyphlops AMNH R N AMNH caecus 36 Sonora AMNH R N AMNH semiannulata 37 Exiliboa AMNH R N AMNH placata 38 Achalinus AMNH R N AMNH spinalis 39 Typhlosaurus AMNH R N AMNH lineatus 40 Rhinophis AMNH R N AMNH philippinus 41 Xenopeltis AMNH R N AMNH unicolor 42 Dibamus AMNH R N AMNH novaeguineae 43 Bipes AMNH R N AMNH canaliculatus 44 Dinilysia patagonica MACN-RN mm Cu AMNH
26 * All AMNH specimens were scanned on site, using loans from the herpetological and paleontological collections of the American Museum of Natural History. The specimen of Dinilysia patagonica is non-amnh, but it was scanned at the American Museum of the Natural History. **For AMNH specimens, all scanning parameters follow the output of a GE v tome x dual-tube CT scanner. Copper filter is generally not recommended for recent specimens. For the recent specimens listed with a 0.1 mm Cu filter, it may have been an operational error: a filter may have been selected for data output when it was not actually in place. In these cases, we recommend scanning with and without a filter for optimal results. Institutional abbreviations: American Museum of Natural History (AMNH), Field Museum of Natural History (FMNH), Museo Argentino de Ciencias Narutales, Argentina (MACN), Texas Natural History Collections, University of Texas at Austin (TNHC), and United States National Museum, Smithsonian Institution (USNM).
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