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Home , Arctoidea, Bone Valley Formation, Hsanda Gol Formation, Nimravidae, Promephitis, Protictis

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Finarelli and Flynn 10.1073/pnas.0901780106 SI Text comparisons to extant taxa appreciably lower the power of Phylogeny of the . Valid statistical analysis of compara- statistical analyses. tive data in biological systems always requires information on the The still imprecise understanding of the evolutionary rela- phylogenetic relationships of the organisms being analyzed to tionships among and extant musteloid taxa (7–11) presents account for the statistical nonindependence of observed char- further challenges in reconstructing character transformations acter values for closely related taxa (1, 2). We constructed a across this clade. We partitioned both nonfelid feliforms and composite cladogram of the Carnivora based on frameworks musteloids into ‘‘archaic’’ and ‘‘modern’’ groups based on first provided by several recent molecular phylogenies of the Car- appearances of taxa in the fossil record. It should be noted that nivora and further augmented by clade-specific phylogenies both of these cutoffs are necessarily arbitrary, and the groupings derived from DNA and morphological data. Recent phyloge- they produce are both highly paraphyletic. Therefore, in contrast netic analyses of the Carnivora using DNA sequence data have to the preceding use of paraphyletic groups, for which observed greatly improved our understanding of the interrelationships change in the allometries can be mapped to a single branch of the among the traditional family-level clades within this clade. In phylogeny, changes between archaic and modern feliforms or addition, morphological and ‘‘total evidence’’ phylogenies, in- musteloids only represent differences between early and late cluding fossil taxa, provide the means to incorporate extinct appearing members of each group. This approach is similar to carnivoran lineages within a molecular framework encompassing previous attempts to document change in relative brain size modern clades. All phylogenetic hypotheses used in this analysis, within a group through time, by partitioning taxa into early/late and references to supporting analyses, are given in Fig. S3. or extant/fossil partitions, and then assessing change in the We identify 2 paraphyletic groups (‘‘Stem ’’ and residual values across these partitions (see, for example, refs. 12, ‘‘Nandinia/Basal Feliforms’’; Fig. S3) that are incorporated as 13, and 14). Although it is always preferable to map evolutionary stem outgroups to 2 monophyletic clades to facilitate the recon- transformations directly onto branches of a phylogeny, given struction of evolutionary transformations between these clades both ambiguity in the fossil record and the phylogeny for these and inferred plesiomorphic conditions of the stem outgroups. groups, the approach presented here represents a conservative Using this approach, a previous analysis of caniforms found analysis and the best potential hypothesis given the presently evidence for a change in the encephalization allometry between available data. a paraphyletic stem canid group and the crown radiation of To determine the cutoffs between archaic and modern taxon Canidae (, foxes, jackals, etc.) (3). In a similar manner, in partitions within and nonfelid , we as- this analysis several fossil taxa comprising a paraphyletic stem sessed the residuals for fossil taxa in each clade relative to the group lying just outside crown-clade Feliformia (e.g., Stenogale) brain volume/body mass regression for the extant taxa in each (4–6) were clustered with Nandinia (Asian palm civet) into a respective clade. If a transformation in the encephalization group of stem feliforms. Due to low sample size, this group was allometry between archaic and modern sets of taxa for either further combined with the extinct clade (‘‘false group is to be preferred over a hypothesis proposing one sabretooths’’) into a paraphyletic stem group, ‘‘Basal Feli- allometry for all taxa within the group, then it is most likely to formia’’ (see Fig. S3) (4, 5). be supported if the partition corresponds to a dramatic change Two additional paraphyletic groups were also considered (Fig. in the distribution of observed residuals. Plotting the distribution S3). With the exception of (cats) and Nimravidae, of residuals against time (12) for each group reveals sharp sample sizes of brain volume estimates for fossil feliforms are increases in both maximum and median residual values for both small, and within the caniforms a similar situation is encountered groups (at 12 Ma for feliforms and 10 Ma for musteloids). We for the Musteloidea (, , weasels, raccoons, and therefore used these values as temporal cutoffs for archaic and allied taxa). The limited sample sizes of fossil taxa available for modern taxon partitions for the 2 groups.

1. Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1–15. 12. Finarelli JA, Flynn JJ (2007) The of encephalization in caniform carnivorans. 2. Garland T, Ives AR (2000) Using the past to predict the present: Confidence intervals for Evolution 61:1758–1772. regression equations in phylogenetic comparative methods. Am Nat 155:346–364. 13. Radinsky L (1978) Evolution of brain size in carnivores and . Am Nat 112:815– 3. Finarelli JA (2008) Testing hypotheses of the evolution of brain-body size scaling in the 831. Canidae (Carnivora, Mammalia). Paleobiology 34:35–45. 14. Jerison H (1973) Evolution of the Brain and Intelligence (Academic, New York). 4. Wesley-Hunt GD, Flynn JJ (2005) Phylogeny of the Carnivora: Basal relationships 15. Finarelli JA (2006) Estimation of endocranial volume through the use of external among the carnivoramorphans, and assessment of the position of ‘‘Miacoidea’’ rela- measures in the Carnivora (Mammalia). J 87:1027–1036. tive to crown-clade Carnivora. J Syst Palaeo 3:1–28. 16. Smith FA, et al. (2003) Body mass of late Quaternary . Ecology 84:3403. 5. Wesley-Hunt GD, Werdelin L (2005) Basicranial morphology and phylogenetic position 17. Gittleman JL (1986) Carnivore brain size, behavioral ecology, and phylogeny. J Mam- of the upper carnivoramorphan Quercygale. Acta Palaeontol Pol 50:837–846. mal 67:23–36. 6. Polly PD, Wesley-Hunt GD, Heinrich RE, Davis G, Houde P (2006) Earliest known 18. Hunt RM (1998) in Evolution of Tertiary Mammals of , eds Janis CM, carnivoran auditory bulla and support for a recent origin of crown-group Carnivora Scott KM, Jacobs LL (Cambridge Univ Press, New York), pp 196–227. (Eutheria, Mammalia). Palaeontology 49:1019–1027. 19. Alroy J (2002) North American fossil mammal systematics database. Available at: 7. Wolsan M (1993) Phylogeny and classification of early European Mustelida (Mammalia, www.nceas.ucsb.edu/ϳalroy/nafmsd.html. Carnivora). Acta Theriol 38:345–384. 20. Hunt RM (1972) Amphicyonids (Mammalia, Carnivora) from the Agate 8. Wang XM, Qiu ZX, Wang BY (2004) A new leptarctine (Carnivora: ) from the Springs Quarries, Sioux County, Nebraska. Am Mus Nov 2506:1–39. early Miocene of the northern Tibetan Plateau: Implications for the phylogeny and 21. Berta A, Galiano H (1984) A Miocene amphicyonid (Mammalia, Carnivora) from the zoogeography of basal mustelids. Zool J Linn Soc 142:405–421. Formation of . J Vert Paleo 57:122–125. 9. Wang XM, McKenna M, Dashzeveg D (2005) Amphicticeps and Amphicynodon (Arc- 22. Radinsky L (1980) Endocasts of amphicyonid carnivorans. Am Mus Nov 2694:1–11. toidea, Carnivora) from , Central Mongolia and Phylogeny of 23. Gustafson EP (1986) Carnivorous mammals of the late Eocene and early of Basal Arctoids with Comments on Zoogeography. Am Mus Nov 3483:1–57. Trans-Pecos Texas USA. Bull Tex Mem Mus 33:1–66. 10. Wang XM, Whistler DP, Takeuchi GT (2005) A new basal Martinogale (Carnivora, 24. Ginsburg L (1966) Amphicyonids from the Quercy Phosphorites. Ann Pale´ ontol (Vert) Mephitinae) from late Miocene Dove Spring Formation, California, and origin of New 52:21–64 (in French). World mephitines. J Vert Paleo 25:936–949. 25. Radinsky L (1977) Brains of early carnivores. Paleobiology 3:333–349. 11. Finarelli JA (2008) A total evidence phylogeny of the Arctoidea (Carnivora: Mammalia): 26. Hunt RM (2002) New Amphicyonid carnivorans (Mammalia, Daphoeninae) from the Relationships among basal taxa. J Mamm Evol 15:231–259. early Miocene of southeastern Wyoming. Am Mus Nov 3385:1–41.

Finarelli and Flynn www.pnas.org/cgi/content/short/0901780106 1of5 27. Wang XM, Tedford RH, Taylor BE (1999) Phylogenetic systematics of the Borophaginae 57. Werdelin L (1988) Studies of fossil Hyaenas—The genera Thalassictis (Gervais ex (Carnivora: Canidae). Bull Am Mus Nat Hist 243:1–391. Nordmann), Palhyaena (Gervais), Hyaenictitherium (Kretzoi), Lycyaena (Hensel) and 28. Gittleman JL (1991) Carnivore olfactory bulb size: Allometry, phylogeny and ecology. Palinhyaena (Qiu, Huang and Guo). Zool J Linn Soc 92:211–265. J Zool 225:253–272. 58. Colbert EH (1935) Siwalik mammals in the American Museum of Natural History. Trans 29. Fortelius M (2003) of the Old World Database of Fossil Mammals (NOW). Am Phil Soc 26:1–401. (University of Helsinki), Version 4.0. Available at www.helsinki.fi/science/now/. Ac- 59. Hunt RM, Solounias N (1991) Evolution of the aeluroid Carnivora. Hyaenid affinities of cessed July, 2003. the Miocene carnivoran Tungurictis spocki from Inner Mongolia. Am Mus Nov 3030:1– 30. Gittleman JL (1986) Carnivore life history patterns: Allometric, phylogenetic, and 25. ecological associations. Am Nat 127:744–771. 60. Bryant HN (1996) in The Terrestrial Eocene-Oligocene Transition in North America, eds 31. Wang XM (1994) Phylogenetic systematics of the Hesperocyoninae (Carnivora: Cani- Prothero DR, Emry RJ (Cambridge Univ Press, New York), pp 453–475. dae). Bull Am Mus Nat Hist 221:1–207. 32. Fuller TK, Johnson WE, Franklin WL, Johnson KA (1987) Notes on the Patagonian 61. Radinsky LB (1982) Evolution in skull shape in carnivores—3. Paleobiology 8:177–195. Hog-Nosed Skunk (Conepatus humboldti) in Southern Chile. J Mammal 68:864–867. 62. Flynn JJ, Finarelli JA, Zehr S, Hsu J, Nedbal MA (2005) Molecular phylogeny of the 33. Wang XM, Carranza-Castan˜ eda O (2009) Earliest hog-nosed skunk, Conepatus (Me- Carnivora (Mammalia): Assessing the impact of increased sampling on resolving enig- phitidae, Carnivora), from early Pliocene of Guanajuato, Mexico and origin of South matic relationships. Syst Biol 54:317–337. American skunks. Zool J Linn Soc, in press. 63. Flynn JJ, Nedbal MA (1998) Phylogeny of the Carnivora (Mammalia): Congruence vs. 34. Stevens MS, Stevens JB (2003) Carnivora (Mammalia, Felidae, Canidae, and Mustelidae) incompatibility among multiple data sets. Mol Phyl Evol 9:414–426. from the earliest Hemphillian Screw Bean Local Fauna, Big Bend National Park, 64. Flynn JJ, Neff NA, Tedford RH (1988) in Phylogeny and Classification of the Tetrapods, Brewster County, Texas. Bull Am Mus Nat Hist 279:177–211. ed Benton MJ (Clarendon Press, Oxford), pp 73–116. 35. Wang XM, Qui Z (2004) Late Miocene Promephitis (Carnivora, ) from China. 65. Wyss AR, Flynn JJ (1993) in Mammal Phylogeny: Placentals, eds Szalay FS, Novacek MJ, J Vert Paleo 24:721–731. McKenna MC (Springer-Verlag, New York), pp 32–52. 36. Galbreath EC (1953) A contribution to the Tertiary geology and paleontology of 66. Ledje C, Arnason U (1996) Phylogenetic relationships within caniform carnivores based northeastern Colorado. University of Kansas Paleontological Contributions: Verte- on analyses of the mitochondrial 12S rRNA gene. J Mol Evol 43:641–649. brata 4:1–120. 67. Ledje C, Arnason U (1996) Phylogenetic analyses of complete cytochrome b genes of 37. Pilgrim GE (1931) Catalogue of the Pontian Carnivora of (William Clowes and the order Carnivora with particular emphasis on the . J Mol Evol 42:135–144. Sons Ltd., London). 68. Flynn JJ, Galiano H (1982) Phylogeny of Early Tertiary Carnivora, with a description of 38. Lariviere S (1998) Lontra felina. Mammalian Species 575:1–5. a new species of Protictis from the Middle Eocene of Northwestern Wyoming. Am Mus 39. Berta A, Morgan GS (1985) A new Sea Otter (Carnivora, Mustelidae) from the Late Miocene and Early Pliocene (Hemphillian) of North-America. J Paleontol 59:809–819. Nov 2725:1–64. 40. Kurten B (1970) The Neogene Plesigulo and the origin of Gulo (Carnivora, 69. Veron G (1995) The systematic position of Cryptoprocta ferox (Carnivora): Cladistic Mammalia). Acta Zool Fenn 131:1–22. analysis of morphological characters of extant and fossil aeluroid carnivorans. Mam- 41. Banyue W, Zhanxiang Q (2003) Notes on early Oligocene ursids (Carnivora, Mammalia) malia 59:551–582 (in French). from Saint Jaques, Nei Mongol, China. Bull Am Mus Nat Hist 279:116–124. 70. Gaubert P, Veron G (2003) Exhaustive sample set among Viverridae reveals the sister- 42. Bonis Ld (1973) Contribution to the study of the mammals of Aquitanien and Angenais. group of felids: The linsangs as a case of extreme morphological convergence within —Carnivores—Perissodactyls. Mem Mus Natl Hist Nat (Ser C) 28:1–192 (in Feliformia. Proc R Soc Lond B 270:2523–2530. French). 71. Yoder AD, et al. (2003) Single origin of Malagasy Carnivora from an African ancestor. 43. Nowak RM (1999) Walker’s Mammals of the World (the Johns Hopkins Univ Press, Nature 421:734–737. Baltimore). 72. Yu L, Li Q, Ryder OA, Zhang Y (2004) Phylogenetic relationships within mammalian 44. Garcia N, Santos E, Arsuaga JL, Carretero JM (2007) Endocranial morphology of Ursus Order Carnivora indicated by sequences of two nuclear DNA genes. Mol Phyl Evol deningeri Von Reichenau, 1904, from the Sima de Los Huesos (Sierra de Atapuerca) 33:694–705. Middle site. J Vert Paleo 27:1007–1017. 73. Yoder AD, Flynn JJ (2003) in The Natural History of Madagscar, eds Goodman SM, 45. Hunt RM (2001) Basicranial anatomy of the living linsangs Prionodon and Poiana Benstead J (Univ of Chicago Press, Chicago), pp 1253–1256. (Mammalia, Carnivora, Viverridae), with comments on the early evolution of aeluroid 74. Flynn JJ, Nedbal MA, Dragoo JW, Honeycutt RL (2000) Whence the red panda? Mol Phyl carnivorans. Am Mus Nov 3330:1–24. Evol 17:190–199. 46. Hunt RM (1998) Evolution of the aeluroid Carnivora. Diversity of the earliest aeluroids from Eurasia (Quercy, Hsanda-Gol) and the origin of felids. Am Mus Nov 3252:1–65. 75. Tedford RH, Taylor BE, Wang XM (1995) Phylogeny of the Caninae (Carnivora: Cani- 47. Werdelin L, Lewis ME (2001) A revision of the (Mammalia, Felidae). dae): The living taxa. Am Mus Nov 3146:1–37. Zool J Linn Soc 132:147–258. 76. Fulton TL, Strobeck C (2006) Molecular phylogeny of the Arctoidea (Carnivora): Effect 48. Petter G, Howell FC (1988) A new machairodont felid (Mammalia, Carnivora) from the of missing data on supertree and supermatrix analyses of multiple gene data sets. Mol Pliocene fauna of Afar (Ethiopia): Homotherium hadarensis n. sp. C R Acad Sc, Ser 2 Phyl Evol 41:165–181. 306:731–738 (in French). 77. Arnason U, Gullberg A, Janke A, Kullberg M (2007) Mitogenomic analyses of caniform 49. Van Valkenburgh B (1991) Iterative evolution of hypercarnivory in canids (Mammalia, relationships. Mol Phyl Evol 45:863–874. Carnivora)—Evolutionary interactions among sympatric predators. Paleobiology 78. Sato JJ, Hosoda T, Wolsan M, Suzuki H (2004) Molecular phylogeny of arctoids (Mam- 17:340–362. malia: Carnivora) with emphasis on phylogenetic and taxonomic positions of the 50. Kurten B, Werdelin L (1984) The relationships of Lynx shansius—Teilhard. Ann Zool ferret-badgers and skunks. Zool Sci 21:111–118. Fenn 21:129–133. 79. Sato JJ, et al. (2006) Evidence from nuclear DNA sequences sheds light on the phylo- 51. Peigne SP, Salesa MJ, Anton M, Morales J (2005) Ailurid carnivoran mammal genetic relationships of Pinnipedia: Single origin with affinity to Musteloidea. Zool Sci from the late Miocene of Spain and the systematics of the genus. Acta Palaeontol Pol 23:125–146. 50:219–238. 80. Yonezawa T, et al. (2007) Molecular phylogenetic study on the origin and evolution of 52. Rothwell T (2004) New felid material from the Ulaan Tologoi locality, Loh Formation Mustelidae. Gene 396:1–12. (Early Miocene) of Mongolia. Bull Am Mus Nat Hist 285:157–165. 81. Vrana PB, Milinkovitch MC, Powell JR, Wheeler WC (1994) Higher level relationships of 53. Christiansen P, Harris JM (2005) Body size of (Mammalia: Felidae). J Morphol 266:369–384. the arctoid Carnivora based on sequence data and total evidence. Mol Phyl Evol 54. Filhol H (1879) A Study of the fossil mammals from Saint-Ge´ rand-le-Puy (Allier). Ann Sci 3:47–58. Geolog 10, 1–252 (in French). 82. Dragoo JW, Honeycutt RL (1997) Systematics of mustelid-like carnivores. J Mammal 55. Pilgrim GE (1932) The fossil Carnivora of India. Palaeontol Ind 18:1–232. 78:426–443. 56. Tseng ZJ, Wang XM (2007) The first record of the late Miocene Hyaenictitherium 83. Veron G, Colyn M, Dunham AE, Taylor P, Gaubert P (2004) Molecular systematics and hyaenoides Zdansky (Carnivora: Hyaenidae) in Inner Mongolia and an evaluation of origin of sociality in (Herpestidae, Carnivora). Mol Phyl Evol 30:582–598. the genus. J Vert Paleo 27:699–708.

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1 Ln Brain Volume in ml Ln Brain Volume

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Ln Body Mass in kg

Fig. S1. Comparison brain volume and body mass data for social (gray filled diamonds) vs. solitary hyaenas (black filled diamonds). Data for all members of the basal Carnivora allometry (open squares) and for fossil hyaenas (solid gray squares) are included for comparison. Under the Social Brain Hypothesis, social hyaenas should display an increase in relative brain volume as compared with nonsocial forms, and should plot relatively high with respect to the remainder of the basal carnivoran allometry. This is not observed.

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Fig. S2. Comparison brain volume and body mass data for social and nonsocial species. Data for all members of the basal Carnivora allometry (open squares) are included for comparison. Social mongooses (gray filled squares) form a monophyletic sister clade to solitary mongooses (black filled squares) (83). Under the Social Brain Hypothesis, the social clade should display an increase in relative brain volume as compared with its sister clade, as well as plotting relatively high with respect to the remainder of the basal carnivoran allometry. This is not observed.

Finarelli and Flynn www.pnas.org/cgi/content/short/0901780106 4of5 Nimravidae

2 Nandinia / Basal Feliforms

3 Felidae

4 Hyaenidae 6 Herpestidae / Eupleridae 1 5

Viverridae

Amphicyonidae

Stem Canidae

7 9 Crown Canidae

8 Ursidae

Mephitidae 10

Ailurus 11

Procyonidae 12

Mustelidae

Fig. S3. Cladogram depicting the relationships among the major lineages of the mammalian order Carnivora. The phylogenetic analyses supporting numbered nodes within this cladogram follow. (Branch 1) Monophyly of Carnivora (4, 5, 62–65). (Branch 2) Monophyly of Feliformia (62–64, 66–68). (Branch 3) Nimravidae basal to crown Feliformia (4, 6), although it should be noted that Wesley-Hunt and Werdelin (5) recovered Nimravidae as basal to all Carnivora. (Branch4) Nandinia biontata and other taxa forming a stem to feliform crown clade (4–6, 62, 63, 65, 69–71). (Branch 5) Reciprocal monophyly of Felidae and Viverridae (s.s.) plus Hyaenidae and ‘‘mongooses,’’ although there is some instability with respect to this result (62, 72). The term mongooses in this analysis includes both Herpestidae and Eupleridae, or the endemic Malagasy carnivorans (62, 63, 70, 71, 73). It should also be noted that our concept of ‘‘Felidae’’ also includes the genus Prionodon, because linsangs have been recovered as the sister taxon to Felidae (‘‘Prionodontidae’’) and are not members of the Viverridae (s.s.) (70). (Branch 6) Monophyly of Hyaenidae plus mongooses (62, 63, 70–73). (Branch 7) Monophyly of Caniformia (62–67, 72, 74). (Branch 8) Amphicyonidae basal to caniform crown clade (4, 5). (Branch 9) Monophyly of Canidae and distinction of a stem clade including the extinct subfamilies Borophaginae and Hesperocyoninae and the genus Leptocyon (27, 31, 62, 63, 66, 67, 74, 75). (Branch 10) Monophyly of Arctoidea (62, 63, 72, 74). (Branch 11) Monophyly of Musteloidea (62, 63, 65, 72, 74, 76–79). Although the internal topology among families within the Musteloidea remains ambiguously supported (see discussion in ref. 80), the Mephitidae (as distinct from Mustelidae), , Mustelidae, and are repeatedly recovered as monophyletic musteloid subclades (62, 66, 67, 74, 78, 79, 81, 82). (Branch 12) Monophyly of Procyonidae plus Mustelidae to the exclusion of other musteloid taxa (62, 63, 65, 72, 74, 76–79).

Other Supporting Information Files

Table S1 Table S2

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