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Journal of Vertebrate Paleontology 20(1):187–190, March 2000 q 2000 by the Society of Vertebrate Paleontology


ON THE PHYLOGENETIC RELATIONSHIPS OF PACHYRHACHIS WITHIN SNAKES: A RESPONSE TO ZAHER (1998) MICHAEL W. CALDWELL, Paleobiology Division, Canadian Museum of Nature, Box 3443, Stn. ‘D’, Ottawa, Ontario, Canada, K1P 6P4, e-mail:

Concerning the snake interrelationships of Pachyrhachis problematicus Haas, 1979, Zaher (1998) criticized Caldwell and Lee (1997) and proposed an alternative phylogenetic hypothesis. The following is a response to Zaher’s (1998) criticisms and a critique of Zaher’s characters and resultant phylogeny. I do not present a new analysis of snake interrelationships, but rather present alternative cladograms to the one found by Zaher (1998). This is accomplished by reconstructing his probable character matrix with character states recoded against observable morphologies. RESPONSE TO ZAHER (1998) Criticism I: Absence of Dinilysia as a Discrete Terminal Taxon Zaher (1998:1, para. 1) notes that, ‘‘Curiously, the well known Cretaceous snake Dinilysia (Estes et al., 1970) was not included in their analysis.’’, and that, ‘‘Understanding the phylogeny and origin of snakes is a difficult problem, best attacked using all the relevant evidence at our disposal, including important fossils.’’ (Zaher, 1998:2, para. 3). The criticism leveled is one of taxon sampling; did Caldwell and Lee exclude an important taxon from their analysis? Dinilysia, a fossil snake from the Cretaceous (Coniacian–Santonian) of Argentina, was most recently described by Estes et al. (1970); these authors noted a mix of characters that were both anilioid-like and booidlike. Based on Estes et al. (1970), Rieppel (1988) considered Dinilysia to be the sister-taxon to alethinophidian snakes (in the sister-group position to modern anilioids), while Rage (1984) reconstructed Dinilysia as more derived than anilioids, nested within alethinopidian snakes, and in the sister-group position to all other macrostomatan snakes. Resolving the relationships of Dinilysia was not the intent of Caldwell and Lee’s (1997) analysis. Clearly, literature based studies, i.e., Rieppel (1988) and Rage (1984), were insufficient means for resolving the problem as neither reached the same conclusion. Caldwell and Lee (1997) restricted their analysis to 26 terminal taxa and used Scolecophia and Alethinophidia as monophyletic terminals with the intent of addressing the higher level squamate interrelationships of Pachyrhachis. If the uncertain relationships of Dinilysia (Estes et al., 1970; Rage, 1984; Rieppel, 1988) were to be simultaneously tested, it would have been necessary to include Dinilysia, anilioids and macrostomatans as terminal taxa. Zaher accepts Scolecophidia as a monophylum; Caldwell and Lee accepted Alethinophidia (Rieppel or Rage’s constitution) as a monophylum. The principle question Caldwell and Lee (1997) attempted to test, was the hypothesis that Pachyrhachis was a ‘snake-like’ dolichosaur (Haas, 1979). Carroll (1988) and Rieppel (1994) had discussed Ophiomorphus (reassigned by Caldwell and Lee [1997] to Pachyrhachis) as a dolichosaur, and the holotype of Pachyrhachis, as a snake-like reptile with dolichosaur affinities. To be fair to these presumptions of dolichosaur affinities, Coniasaurus (a dolichosaur), and the Mosasauroidea (considered closely related to dolichosaurs), were included as terminals. Criticism II: Specific Characters Presence/Absence of a Jugal Bone—Zaher is correct in noting that Caldwell and Lee (1997) did not code for the anomalolepidid polymorphism of this character within Scolecophidia. Caldwell and Lee elected not to re-characterize the postorbital of Anomalepis (see Haas, 1968) as a jugal (see List, 1966), but instead treated Alethinophidia and Scolecophidia as ‘‘jugal absent or highly reduced’’. Despite Zaher’s ci-

tations regarding the certain identification of a jugal in Dinilysia, Estes et al. (1970) make no such claims. Preliminary study of new specimens of Dinilysia (Caldwell and Albino, pers. observ.) indicates that the jugal is absent. Angular–Coronoid Contact—Caldwell and Lee coded scolecophidians as polymorphic for presence/absence of an angular–coronoid contact. They did not include a polymorphic state of ‘‘inapplicable’’ for anomalepidids. The basis for Zaher’s conclusion that the character is uninformative in Caldwell and Lee’s matrix is unclear as it is coded for 26 snake and lizard taxa; it may be uninformative but it is unclear as to whether or not Zaher excluded the character due to serious discrepancies between this text and figure caption (see discussion below). It is uncertain how Zaher arrived at his conclusion concerning the angular– coronoid contact in Dinilysia. Estes et al. (1970) note that there is a groove for the contact between the angular and coronoid. It is also unclear why Zaher maintains that the contact is absent in Cylindrophis. In specimens of Cylindrophis (FMNH 13100 and USNM 297456) examined by the author, the coronoid contacts the angular. Exoccipitals do not Meet Above Foramen Magnum—Zaher is correct in noting that Caldwell and Lee (1997) coded this character as present in Pachyrhachis based on what was interpreted as the finished margin of the supraoccipital where it framed the dorsal portion of the foramen magnum. Recoding this state as uncertain (?) makes the character uninformative for Zaher’s analysis. A CRITIQUE OF ZAHER (1998) If Zaher’s (1998) phylogenetic alternative is to be preferred it must reduce problems of homoplasy present in Caldwell and Lee (1997), and satisfy requirements of testability (sensu Kluge [1997]) by presenting evidence that supports the hypothesis. The testability of a phylogenetic hypothesis requires the explicit presentation of a data set (characters and matrix) and the analytical protocol; collectively, this information represents the evidence. Zaher (1998) does not provide a data matrix nor any other recoverable form of data. Therefore, it is impossible to test the hypothesis given. Zaher (1998:fig. 1) in citing the data matrix of Caldwell and Lee (1997), indicates that only relevant characters were used (18 of 108 characters), and that six new characters were added, identified as 18– 24. A count indicates that there are seven new characters, not six. Were only 17 of Caldwell and Lee’s characters actually added to Zaher’s 6(7) to achieve a figure-caption total of 24? Which one was excluded? Or should the total count have been 25? This problem is complicated by internal inconsistency between text and figure captions with regards to the numbering of Caldwell and Lee’s (1997) characters C3 and C4. Because the data cannot be examined it is impossible to know the distribution and number of characters and their character states. Zaher’s (1998) Characters (Z18–Z24) Character 19 (Z18)—Quadrate: anteriorly directed (0); vertically or posteriorly directed (1). Zaher’s state assignments: Scolecophidians (0); all other taxa (1). There are clearly three states for this character: vertical, posterior, and anterior. Pachyrhachis is ‘best’ reconstructed with a vertical quadrate. Anilioids and Dinilysia also have vertically oriented quadrates. In most macrostomatans the quadrate is posteroventrally rotated (Rieppel, 1988). Having two states encapsulated within a single binary code avoids an autapomorphy for Macrostomata, but also ensures that this




FIGURE 1. Three most parsimonious cladograms generated from reanalysis of Zaher’s (1998) data showing the relationship of Pachyrhachis to all other snakes. Results: Three Trees; TL 33 steps; CI 0.870; HI 0.242; RI 0.667. A, Tree 1; B, Tree 2; C, Tree 3. In all trees, three consistent sister-group relationships persist: (1) Pachyrhachis as sister-group to all other snakes; (2) a Dinilysia-anilioid clade, whose resolution within Serpentes, above the level of Pachyrhachis, remains unstable; and (3) Scolecophidia nested within Alethinophidia.

character will be synapomorphic for all snakes above Scolecophidia. I have coded Macrostomata as polymorphic for this character and created three separate states (see Appendices 1 and 2). Character 20 (Z19)—Toothed anterior process of the palatine: absent (0); present (1). Zaher’s state assignments: Scolecophidians and Dinilysia (0); all other taxa (1). This is a two part character and should be coded as such. The anterior process of the palatine must be present in order for it to be toothed. There is no occurrence in Zaher’s matrix where a non-toothed anterior process is present. Scolecophidians do not have teeth anywhere on the palatine, nor do they have an anterior process (such a process extends anterior to the maxillary process and vomerine processes of the palatine). In contrast, Dinilysia does possess teeth on the palatine, but not an anterior process due to the presence of a deep choanal groove, and is qualitatively different from the scolecophidan condition. Thirdly, regarding the toothed process, in anilioids there are seldom more than 1– 3 small teeth; in basal macrostomatans the number can be very high, while in some colubroids it can be reduced. I have coded Scolecophidia as ‘inapplicable’ and Dinilysia as ‘0’ (see Appendices 1 and 2). Character 21 (Z20)—Free-ending process of the supratemporal: absent (0); present (1). Zaher’s state assignments: Scolecophidia, Dinilysia, anilioids (0); Pachyrhachis, Macrostomata (1). From the character description (Zaher, 1998:fig. 1, caption), Scolecophidia, Dinilysia, and Anilioids are coded as possessing comparable states, but this is simply not the case. Scolecophidans have no supratemporal and therefore cannot have a free-ending process; the quadrate loosely abuts against the sidewall of the braincase. This is different from Dinilysia and anilioids which possess a large supratemporal with a distinct facet for the articulation with the quadrate. This character would better correspond to the observed variation if it were broken into at least three distinct states. I have recoded this character ‘inapplicable’ for Scolecophidia (see Appendices 1 and 2). Character 22 (Z21)—Dorsal surface of the prootic: not concealed by supratemporal (0); concealed by the supratemporal (1). Zaher’s state assignments: Scolecophidians, Dinilysia, anilioids (0); Pachyrhachis, Macrostomata (1). First, in neither specimen of Pachyrhachis is the prootic identifiable (Caldwell and Lee, 1997), therefore it cannot be known whether or not some part of the bone was concealed by the supratemporal. Zaher codes Anilioids and Dinilysia as sharing the plesiomorphic state with scolecophidians. In both anilioids and Dinilysia the supratemporal conceals the dorsal part of the prootic. For scolecophidians, the supratemporal cannot conceal the prootic because it is absent. I have coded scolecophidians as ‘inapplicable’ (see Appendices 1 and 2). Character 24 (Z23)—Dentigerous process of the dentary: absent (0); present and short (1); present and enlarged (2). Zaher’s state assignments: Scolecophidians (0); Dinilysia, anilioids (1); Pachyrhachis, Macrostomata (2). This character is difficult to interpret, and is even more difficult to reconstruct onto Zaher’s (1998) phylogeny. In snakes, the posterodorsal and posteroventral processes of the dentary are equivalent in length. At their posterior termini these dorsal and ventral processes form vertical joints with the postdentary elements, with the exception of the compound bone. The compound bone is the only postdentary bone that crosses the intramandibular joint to any appreciable degree. When the

compound bone is anteriorly elongate, it excavates the lateral surface of the dentary. It is the extent of dentary excavation that Zaher identifies as producing a longer or shorter dentigerous process of the dentary. However, in medial view the dentary above Meckel’s Canal is a solid sheet of bone that folds medially to produce the dental shelf. Again, the ventral portion of the dentary is equivalent in length to the dorsal, toothed portion. The dentigerous process does not exist. The extent to which the compound bone invades the dentary appears to be related to the length of the lower jaw. Where the mandible is short and bears only a few teeth, the compound bone extends only a short distance into the dentary, giving the toothed portion the appearance of being abbreviated (Dinilysia, anilioids). Where many teeth are present and the dentary is elongated, the toothed portion seems posteriorly elongated only because the compound bone extends further into the dentary (Pachyrhachis and Macrostomata). The absence of the feature in scolecophidians should be recoded as ‘‘inapplicable’’ because there are often no dentary teeth, and if such teeth are present, the compound bone does not invade the dentary, thus there is no process, and not, as Zaher describes, an absence of a toothed process. The landmark for redescription and recoding of this character (Appendix 1) is the contact between the coronoid and the dentary (see Appendices 1 and 2). Character 25 (Z24)—Suprastapedial process: present (0); absent (1). Zaher’s state assignments: Scolecophidians, Dinilysia, anilioids (0); Pachyrhachis, Macrostomata (1). The scolecophidian and macrostomatan quadrates do not possess identifiable suprastapedial processes. The quadrates of anilioids and Dinilysia are short, stout, robust elements that have large, ventrally directed suprastapedial processes. As Zaher notes, these quadrates are similar to those of mosasauroids. However, they are very different from those of other squamates such as varanoids, iguanids, or amphisbaenids. In contrast, the scolecophidian quadrate is a straight element that articulates not with a supratemporal suspensorium, but rather is buttressed against the prootic-opisthotic. In some taxa, the quadrate bears a large, vertically directed dorsal process; in others it is expanded at its dorsal end, but it is not hooked posteroventrally, nor is it C-shaped and similar to that of anilioids or Dinilysia. I have recoded the scolecophidian condition as ‘1’ (see Appendices 1 and 2). REANALYSIS Reanalysis and recharacterization of Zaher’s (1998) characters produced a taxon–character matrix composed of five terminal taxa and 25 characters (Appendix 2). Characters were polarized using Zaher’s (1998) ‘‘Other Squamates,’’ but only after coding these ‘22’ taxa (see Caldwell and Lee, 1997) as a single terminal. I have included polymorphic states as given by Caldwell and Lee (1997). All characters were examined unordered and no characters were weighted (contra Zaher, 1998: Character 23). Character C4 (angular–coronoid contact [see Appendix 1]) was added to the data set since there is no justification for Zaher’s determination that it is uniformative (see above). Ten of Zaher’s characters, from Caldwell and Lee (1997; characters B1–B10; see Appendix 1), are uninformative (see Appendix 1). The new data matrix (Appendix 2) was analyzed using Exhaustive Searches Options in the computer software PAUP 3.1.1 for the Macintosh. Analysis of these data found three most parsimonious trees (Fig. 1A–

NOTES C) of 33 steps each (CI 0.870; HI 0.242; RI 0.667). In all trees, three consistent sister-group relationships persist: (1) Pachyrhachis as sistergroup to all other snakes; (2) a Dinilysia-anilioid clade, whose resolution within Serpentes, above the level of Pachyrhachis, remains unstable; and (3) Scolecophidia as sister taxon to, or nested within, Alethinophidia. SUMMARY The origins and relationships of snakes continue to be fascinating and intriguing problems. The complex and conflicting characters present in a number of well-preserved Cretaceous snakes have now been added to the pool of data used to examine snake phylogeny. As a result of ingroup and outgroup analysis of snake interrelationships, a marine origin for snakes is now a reasonable alternative to the received position that snakes originated from a burrowing or fossorial ancestor (Lee, 1997; Caldwell and Lee, 1997; Caldwell, 1999; Lee and Caldwell, 1998; Lee et al., in press). Such ‘assaults’ on conventional hypotheses are always resisted forcibly, and justifiably so. However, Zaher’s (1998) hypothesis is not a well-supported criticism of Caldwell and Lee (1997) despite its appeal to more conventional phylogenetic hypotheses, and its underlying support for the fossorial origin of snakes. Zaher finds Scolecophidia to be the sistergroup to Dinilysia. The reanalysis of Zaher’s characters, and subsequent PAUP analysis of a character matrix constructed from that re-analysis, finds no such relationship. Scolecophidia are either a derived clade of alethinophidians, or are nested within ‘dinilysioid’ snakes (Fig. 1A–C). Dinilysia, as was noted by Estes et al. (1970), shares a number of apomorphies with anilioids that in this reanalysis link these two taxa as a clade. Phylogenies reconstructing Pachyrhachis as the sister-taxon to all other snakes are the most parsimonious hypotheses of snake relationship, and are supported here in all three trees. Zaher’s appeals to homoplastic characters not identified as primary homologues by Caldwell and Lee (1997) are satisfied without creating more homoplasy regarding re-acquisition of limbs, etc. (for a list see Zaher [1998]). Acknowledgments—For reading various drafts of this manuscript and for discussions on snake origins, I thank Adriana Albino, Adriana Lo´pez Arbarello, Gorden Bell, Steve Cumbaa, David Cundall, Kevin de Quieroz, David Gower, Rob Holmes, Mike Lee, Les Lowcock, John Merck, Alison Murray, Mike Polcyn, John Scanlon, and Kathlyn Stewart.


Caldwell, M. W. 1999. Squamate Phylogeny and the relationships of snakes and mosasauroids. Zoological Journal of the Linnean Society 125:115–147. , and M. S. Y. Lee. 1997. A snake with legs from the marine Cretaceous of the Middle East. Nature 386:705–709. Carroll, R. L. 1988. Vertebrate Paleontology and Evolution. W.H. Freeman and Company, New York, New York, 698 pp. Estes, R., T. H. Frazetta, and E. E. Williams. 1970. Studies on the fossil snake Dinilysia patagonica Woodward: Part 1. Cranial morphology. Bulletin of the Museum of Comparative Zoology 140:25–74. Haas, G. 1968. Anatomical observations on the head of Anomalepis aspinosus. Acta Zoologica 49:63–139. 1979. On a new snake-like reptile from the Lower Cenomanian of Ein Jabrud, near Jerusalem. Bulletin de la Museum Nationale d’histoire Naturelle, Paris, Ser. 4, 1:51–64. Kluge, A. 1997. Testability and the refutation and corroboration of cladistic hypotheses. Cladistics 13:81–96 Lee, M. S. Y. 1997 The phylogeny of varanoid lizards and the affinities of snakes. Philosophical Transactions of the Royal Society, London: Biological Sciences 352:53–91. , and M. W. Caldwell. 1998. Anatomy and relationships of Pachyrhachis, a primitive snake with hindlimbs. Philosophical Transactions of the Royal Society, London: Biological Sciences 353: 1521–1552. , , and J. S. Scanlon. 1999. A second primitive marine snake: Pachyophis woodwardi Nopcsa. Journal of Zoology List, J. C. 1966. Comparative osteology of the snake families Typhlopidae and Leptotyphlopidae. Illinois Biological Monographs 36:1– 112. Rage, J.-C. 1984. Serpentes. Handbuch der Pala¨oherpetologie Teil 11. Gustav Fischer Verlag, Stuttgart, pp. Rieppel, O. 1988 A review of the origin of snakes. Evolutionary Biology 22:37–130. 1994. The Lepidosauromorpha: an overview with special emphasis on the Squamata; pp. 22–37 in N. C. Fraser and H.-D. Sues (eds.), In the Shadow of the Dinosaurs. Cambridge University Press, Cambridge. Zaher, H. 1998. The phylogenetic position of Pachyrhachis within snakes (Squamata, Serpentes). Journal of Vertebrate Paleontology 18:1–3. Received 1 February 1999; accepted 10 May 1999.



APPENDIX 1. Characters and character states used in the cladistic analysis. The number in parentheses refers to characters taken from Caldwell and Lee (1997); characters 19–25 are derived by reference to Zaher (1998:fig. 1) and are identified by a ‘Z’ in parentheses and the number as given in Zaher’s caption (Zaher, 1998:2). For the taxon character matrix ‘A’ indicates polymorphic states (0, 1) and ‘B’ indicates polymorphic states (1, 2). 1. 2. 3. 4. 5. 6. 7. 8. 9. 10. 11. 12. 13. 14. 15. 16. 17. 18. 19. 20. 21. 22. 23.

(B1) Premaxilla-maxilla articulation: Contact rigid and sutural (0); non-sutural and mobile (1). (B2) Descending process of frontal: does not form optic foramen (0); forms part or all of margin of optic (II) foramen (1). (B3) Descending process of parietal: does not contact parabasisphenoid (0); meets parabasisphenoid (1). (B4) Tympanic recess: present (0); absent (1). (B5) Palatine with distinct rectangular medial process which meets its partner in the midline (process absent); (B6) Dentary, number of mental foramina: three or more (0); two or less (1). (B7) Tooth attachment, marginal teeth: Sockets absent (0); ankylosed to the rims of discrete sockets (1). (B8) Body Length: Short, ,140 precloacal vertebrae (0); .140 precloacal vertebrae (B9) shoulder girdle and forelimb completely absent (present, even in limb-reduced lizards). (B10) Epiphyses: present (0); absent (1). (C8) Tibia, fibula, astragalus and calcaneum: present (0); absent (1). (C7) Femur: present (0); vestigial or lost (1). (C6) Pelvis: when present, external to ribcage with sacral contact (0); when present, lies within ribcage, sacral contact absent (1). (C5) Dentary, number of mental foramina: three or more (0); two (1); one (2). (C4) Angular–coronoid contact: absent (0); present (1). (C3) Exoccipitals: do not meet above foramen magnum (0); do meet (1). (C2) Posterior orbital margin: complete (0); incomplete (1). (C1) Jugal: present (0); absent (1). (Z18) Quadrate: anteriorly directed (0); vertically directed (1); posteriorly directed (2). (Z19) Toothed anterior process of the palatine: absent (0); present (1) (Z20) Free-ending process of the supratemporal: absent (0); present (1). (Z21) Dorsal surface of the prootic: not concealed by supratemporal (0); concealed by the supratemporal (1) (Z22) Basipterygoid processes: developed, and articulating surfaces more lateral than ventral (0); reduced and articulating surfaces face ventrally (1) 24. (Z23) Posterior-most portion of the dentary toothed and overlaps coronoid: absent (0); present (1). 25. (Z24) Suprastapedial process: present (0); absent (1).

APPENDIX 2. Data matrix. Character Taxa Other Squamates Scolecophidia Dinilysia Anilioids Pachyrhachis Macrostomata






A0000 11111 11111 11111 11111 11111

00000 11111 11??1 11111 11111 11111

00000 1112A 1??21 11121 00010 11121

00000 11A0?1110 11111 0?011 111B1

00100 ----1 01010 01010 1??11 11111

Caldwell, 2000a