q 2001 The Paleontological Society. All rights reserved. 0094-8373/01/2701-0001/$1.00

Paleobiology, 27(1), 2001, pp. 1–6

MATTERS OF THE RECORD

Snake origins and the need for scientific agreement onvernacular names

Michael S. Y. Lee

Department of Zoology, University of Queensland, Saint Lucia, Brisbane, QLD 4072, Australia.E-mail: mlee@zoology.uq.edu.au

Accepted: 31 August 2000

When transitional fossils blur previouslyclear boundaries between major groups,drawing that line can be problematic. Whilethe need to rigorously define formal taxonnames is widely acknowledged (e.g., de Quei-roz and Gauthier 1992; Cantino et al. 1997),the need for similar precision in the scientificuse of vernacular terms is not widely appre-ciated. The lack of accepted usages for com-mon names has engendered endless argu-ments about when a fish becomes (also?) a tet-rapod (e.g., Clack 1997), when a dinosaur be-comes (also?) a bird (e.g., Padian and Chiappe1998), and when a mammal-like reptile be-comes (also?) a mammal (e.g., Rowe and Gau-thier 1992). Recent descriptions of fossilsnakes with well-developed hindlimbs haveraised similar questions about where to drawthe line between lizards and snakes and ini-tiated a lively debate over the origin of snakes.However, lack of a precise definition of thevernacular term ‘‘snake,’’ as well as lack of aconsensus on what constitutes a higher taxon’s‘‘origins,’’ has seriously hindered discussionof ‘‘snake origins.’’ Here, precise definitions ofboth terms are proposed and justified andtheir paleobiological implications discussed.The origin of higher taxa remains one of themost intriguing macroevolutionary problems,but scientists risk arguing at cross-purposesunless they agree on the exact boundaries ofvernacular groups, and the exact meaning ofthe term ‘‘origin.’’

Some recent descriptions of Cretaceouslimbed marine snakes (‘‘pachyophiids’’) con-sidered them the sister group to all other(modern) snakes, and thus transitional be-

tween lizards and snakes. The difficulties de-fining snakes and thus snake origins (Lee andCaldwell 1998; Greene and Cundall 2000)have been debated in the context of this phy-logeny, even though the latter authors aresympathetic to the alternative view that pach-yophiids are not transitional forms but are de-rived snakes that have re-evolved limbs(Tchernov et al. 2000). However, even if this isthe case, the same conceptual problems willarise if Dinilysia and madtsoiids (Scanlon andLee 2000) or any other fossils are proposed tooccupy this basal position.

Pachyophiids were considered transitionalbetween lizards and snakes (Lee and Caldwell1998) because they exhibited most of the ad-vanced features of snakes (such as highly ki-netic skull, enclosed braincase, loss of externalear, elongate and almost limbless body) butretained a largely complete (albeit tiny) pelvisand hindlimb. Therefore, the vernacular term‘‘snake’’ might be applied in two places (Fig.1). There is almost universal agreement thatthe short-bodied, four-limbed mosasauroidsand Adriosaurus are ‘‘lizards,’’ and that theelongated and nearly (or totally) limbless sco-lecophidians and alethinophidians are true‘‘snakes.’’ To remain consistent with acceptedusage, the vernacular term ‘‘snakes’’ shouldbe applied to some group that includes sco-lecophidians and alethinophidians but ex-cludes mosasauroids and Adriosaurus. Thisleaves two places in the tree where the termcan be applied—for the clade including onlyscolecophidians and alethinophidians or forthe slightly more inclusive clade that also in-cludes pachyophiids.

2 MICHAEL S. Y. LEE

FIGURE 1. A proposed phylogeny of snakes and their nearest lizard relatives, based on Lee and Caldwell (2000).‘‘1’’ denotes extinct taxa. The two possible places to apply the vernacular term ‘‘snakes’’ are shown. Representativesynapomorphies of each clade are as follows; note that the most significant and numerous changes occur alongbranch ‘‘C.’’ A1, Mobile intramandibular and symphysial joints. B1, Supratemporal positioned dorsal to parietal.C1, Enclosed braincase. C2, Loss of external ear. C3, Mobile maxillary-premaxillary joint. C4, Elongated body withover 120 presacral vertebrae. C5, Loss of shoulder girdle and forelimb. C6, Reduction of pelvic girdle and hindlimb.D1, Loss of jugal. D2, Loss of pes.

The latter, more inclusive definition wasadopted (Lee and Caldwell 1998), since pach-yophiids already exhibit almost all of the fea-tures traditionally considered ‘‘diagnostic’’ ofsnakes. A phylogenetic analysis revealed thatmost of the features separating snakes from‘‘lizards’’ evolved at the base of the pachy-ophiid-scolecophidian-alethinophidian clade,and only a few additional ones evolved at thebase of the scolecophidian-alethinophidianclade (Fig. 1). Earlier studies were also in-structive in this respect. Estes and colleagues(Estes et al. 1988) presented a detailed list ofdiagnostic characters of ‘‘snakes’’ in 1988 andthus summarized the traits ‘‘traditionally’’considered to separate snakes from lizardsimmediately before the problematic interme-diate forms were identified. Of the 50 ‘‘snake’’characters, pachyophiids can be scored for 24:they exhibit the snake condition in 21 but thelizard condition in only 3. Similar results arealso obtained if less-scientific character listsare consulted: for example, standard detaileddictionaries (e.g., Gove 1976) list as snakecharacters traits such as a highly kinetic skull,enclosed braincase, loss of external ear, elon-gate almost limbless body—all of which arefound in pachyophiids. Thus, the great major-

ity of the characters traditionally used to sep-arate lizards and snakes, in both the scientificand popular literature, placed pachyophiidson the snake side of the divide. We furtherconfirmed this conclusion by showing pic-tures of varanids, mosasauroids, pachy-ophiids, scolecophidians, and alethinophidi-ans to a cross-section of scientists and laypeo-ple, and asking them what forms they consid-ered ‘‘lizards’’ and what they considered‘‘snakes.’’ All identified varanids and mosa-sauroids as lizards, and pachyophiids, scole-cophidians, and alethinophidians as snakes.The understanding of ‘‘snake’’ held by mostpeople (‘‘traditional usage’’) therefore ap-pears to include pachyophiids.

Thus, a phylogenetic analysis demonstratedthat pachyophiids had evolved nearly all thefeatures usually considered diagnostic ofsnakes. Also, an inspection of ‘‘snake’’ char-acter lists revealed that pachyophiids pos-sessed the majority of these traits, and mostpeople intuitively identified pachyophiids assnakes. Pachyophiids were thus clearly morethan halfway along the branch leading from‘‘lizards’’ to ‘‘snakes,’’ and should be consid-ered primitive snakes rather than advanced(snakelike) lizards. Accordingly, the more in-

3SNAKE ORIGINS

clusive definition of ‘‘snake’’ was adopted. De-spite this detailed justification (see Lee andCaldwell 1998), Greene and Cundall (2000: p.1940) state that we ‘‘dodge the crucial ques-tion of the point on the phylogenetic tree stemconnecting mosasaurs and Pachyrhachis wherea fossil becomes more snake-like than lizard-like,’’ and furthermore that we ‘‘arbitrarily de-fine ‘‘snake’’ so that Pachyrhachis must be one.’’The above, I hope, shows that our preferreddefinition of ‘‘snake’’ was not quite so capri-cious.

In contrast to the above interpretation of thevernacular term ‘‘snakes,’’ Greene and Cun-dall (2000) adopt a crown-group definition(Gauthier 1986; Rowe 1988; de Queiroz andGauthier 1992; Bryant 1994), i.e., restricting itto the most recent common ancestor of livingsnakes and all its descendants. This would at-tach ‘‘snakes’’ to the scolecophidian-alethino-phidian clade, termed ‘‘modern snakes’’ byLee and Caldwell (1998; see also Scanlon andLee 2000). However, even for formal taxonnames like Tetrapoda, Mammalia, and Aves,the use of such restricted crown-group defi-nitions is questionable. The contents of crown-group taxa are often much more restrictedthan traditional concepts. Also, employingliving forms as landmarks (reference taxa) fordrawing taxon boundaries does not circum-vent problematic fossils, which still might fallinside or outside the crown group (e.g., Lee1996; Padian and Chiappe 1998; Sereno 1999).Indeed, in the current example, a crown-cladedefinition of Ophidia (snakes) is more unsta-ble than the more traditional definition ad-vocated here. Ophidia (crown-group) mightor might not include pachyophiids, dependingon which phylogenetic position is accepted(basal or macrostomatan), whereas Ophidia(traditional) always includes pachyophiids,regardless of which of these two positions isadopted.

For vernacular terms, such restrictedcrown-group definitions are clearly inappro-priate—for instance, applying crown-groupinterpretations would mean that Ichthyostega isnot a tetrapod, Morganucodon is not a mam-mal, and Archaeopteryx is not a bird. All theseextinct forms have evolved most of the diag-nostic features of their respective groups (e.g.,

dactylous limbs, dentary-squamosal jaw joint,and powered flight, respectively) yet lie out-side the diversity of living forms. Greene(1997) advocates such a crown-group defini-tion of ‘‘snakes’’ in a magnificent book intend-ed for a general audience, suggesting that heinterprets and/or wishes this to be the pop-ular or traditional definition. Greene andCundall (2000) indeed state this (p. 1940),though obliquely: ‘‘the traditional version [ofsnake origins] is based on a narrower defini-tion of the word snake.’’ However, this pro-posal is not substantiated in that paper orelsewhere. In contrast, the above discussionshows that traditional definitions of snakesimplicitly included pachyophiids—most ofthe characters diagnostic of snakes are presentin pachyophiids, and most people identifythem as snakes.

Greene and Cundall (2000) further arguethe ‘‘survey’’ approach is flawed, by mention-ing (correctly) that many laypeople wouldalso (mis)identify as ‘‘snakes’’ anguids, py-gopodids, amphisbaenians, caecilians, eels,and other assorted elongate limb-reduced ver-tebrates. However, this objection rather missesthe point. Surely, the question must be, if pre-sented with the relevant taxa (those that con-stitute the snake stem lineage), where wouldmost people draw the line? Showing peopleconfusing convergent taxa (which no modernbiologist would advocate including in‘‘snakes’’ anyway) would have represented anirrelevant distraction. By analogy, if one is in-terested in whether the term ‘‘birds’’ is morewidely understood to apply to a group in-cluding or excluding Archaeopteryx, one wouldpresumably show people an assortment of(non-avian) theropod dinosaurs, Archaeopter-yx, and an assortment of modern birds. Ifmost people identify Archaeopteryx as well asmodern birds as ‘‘birds,’’ this would demon-strate the term is usually understood to applyto this more inclusive group. To minimize con-fusion, therefore, one should thus advocatethat the vernacular term ‘‘birds’’ be used forsuch a group. The possibility that some lay-people might also identify bats or pterosaursas ‘‘birds’’ is not particularly relevant. Thegeneral public, as well as scientists, will usevernacular terms, and the general public out-

4 MICHAEL S. Y. LEE

FIGURE 2. Illustration of how characters on the single branch leading to modern (crown-group) snakes might haveevolved in a marine ancestor, even though the latest common ancestor of modern snakes was undoubtedly terres-trial. ‘‘1’’ denotes extinct taxa. Black lines indicate marine lineages, stippled lines indicate terrestrial lineages.

numbers scientists by several orders of mag-nitude. Scientists should attempt to make theirdefinition and usage of vernacular names assimilar as possible to those adopted by themajority of users, while still maintaining thenecessary scientific rigor (e.g., for taxonomicgroups, monophyly). Thus, ‘‘snakes’’ shouldinclude modern (crown-group) snakes andalso those forms along the snake stem lineagethat the majority of people identify as snakes,but to maintain monophyly should excludeamphisbaenians, caecilians, and other unre-lated limbless forms regardless of public opin-ion. Similarly, ‘‘birds’’ should include crown-group birds and forms along the bird stem lin-eage that the majority of people identify asbirds, but should exclude pterosaurs, bats, andother flying forms.

Many vernacular names are usually consid-ered synonymous with particular formalnames—for instance, ‘‘birds’’ is equated withAves, ‘‘mammals’’ with Mammalia, and‘‘snakes’’ with Ophidia or Serpentes. If theabove arguments for defining vernacularnames are accepted, then to minimize confu-sion any tightly associated formal namesshould also be defined to refer to the sameclade. Alternative solutions are likely to bevery confusing. Redefining both the vernac-

ular and formal names to refer to the crowngroup can mean that both terms are given newand unfamiliar meanings, while continuing touse the vernacular name to refer to the ‘‘tra-ditional’’ clade and but redefining the formalname to refer to the crown group would meanthat previously synonymous terms are no lon-ger equivalent (e.g., Archaeopteryx would be a‘‘bird’’ but not belong to Aves).

The suggestion of a marine origin forsnakes was based on the inference (based onparsimony) that the snake stem lineage un-derwent a marine phase (Fig. 2), during whichit acquired most of the features usually inter-preted as ‘‘diagnostic’’ of snakes, such as along limb-reduced body and highly flexibleskull (Scanlon et al. 1999; Lee and Caldwell2000) (Fig. 1). In contrast, a new definition ofsnake origins proposed by Greene and Cun-dall considers this aquatic phase irrelevant.These authors first restrict the term ‘‘snakes’’to modern (crown-group) snakes. Then, theysuggest that the origin of ‘‘snakes’’ consists ofthe (few) changes that occurred at the singlebranch leading to that clade (branch D in Fig.1). As the latest common ancestor of thecrown-clade was terrestrial, they further sug-gest, snakes can be considered to have had ex-clusively terrestrial origins—regardless of any

5SNAKE ORIGINS

earlier marine interlude during which farmore substantial changes toward a snakemorphology occurred. However, this view ap-pears problematic for several reasons.

First, the origin of the snake bodyplan, likethat of any higher taxon, cannot be attached toany single branch—these changes (and thussnake origins) must have occurred graduallyand cumulatively over multiple branches onthe snake stem lineage (e.g., Greene 1983;Cundall 1995; Kardong et al. 1997). If some ofthese branches were aquatic, this would by def-inition imply an aquatic phase in snake ori-gins. Focusing only on a single node, and ig-noring all previous and subsequent changes,amounts to a semantic sleight of hand. For in-stance, it would be analogous to defining‘‘birds’’ to refer to modern (crown-group)birds, and ‘‘bird origins’’ to refer only to thechanges separating crown-group birds fromArchaeopteryx and similar taxa. Since feathersand flight evolved earlier on the cladogram, itcould then be argued that feathers and flighthad nothing whatsoever to do with bird ori-gins. However, Greene and Cundall are justi-fied in suggesting that there must be a ‘‘lowerlimit’’ on where one considers the ‘‘origin’’ ofa taxon to begin. For instance, given that thefeatures diagnostic of modern snakes accu-mulated gradually from the lineage leadingfrom the first living organism to the ancestorof crown-group snakes, where should we con-sider ‘‘snake origins’’ to begin—and end forthat matter? My proposal is this: The origin ofan extant taxon should be considered to be theevolutionary changes that accumulated in thestem lineage of a group between the time it di-verged from its nearest extant sister groupand the time crown-group forms radiated.Thus, under this definition, ‘‘snake origins’’consists of the changes occurring alongbranches A to D of Figure 1, i.e., the changesthat occurred between the common ancestorof thecoglossans (varanid lizards and snakes)and the latest ancestor of crown-group snakes.This definition implicates in snake originstraits that evolved slightly before, coincidentwith, and slightly after the precise taxonomicboundary between lizards and snakes (de-fined above to correspond with traditionalviews). However, the definition excludes traits

which occurred earlier or later along the snakestem lineage from being considered part ofsnake origins (depending on their exact posi-tion along the stem lineage such changeswould instead be implicated in, for example,thecoglossan origins, or alethinophidian ori-gins). It thus strikes a balance between ‘‘tele-scoping’’ snake origins deep down into thereptile tree (which Greene and Cundall rightlycriticize) and restricting it to changes occur-ring along a single branch (the overly narrowinterpretation they advocate). Similarly, underthe definition here proposed, ‘‘mammal ori-gins’’ would consist of all the changes whichoccurred between the latest ancestor of am-niotes (mammals plus reptiles) and the ances-tor of crown-group mammals, and ‘‘bird ori-gins’’ would consists of all the changes whichoccurred between the latest ancestor of archo-saurs (birds plus crocodilians) and the ances-tor of crown-group birds. This coincides quiteclosely with the changes discussed in manyreviews of mammal and bird origins (e.g.,Kemp 1982; Padian and Chiappe 1998) andthus previous implicit ideas about what con-stitutes ‘‘origins.’’

The second problem with Greene and Cun-dall’s interpretation of ‘‘snake origins’’ is thateven if one chooses to identify a single branchas representing ‘‘the’’ origin of snakes, thisshould (arguably) be the branch during whichthe most numerous and significant changesfrom ‘‘lizardness’’ toward ‘‘snakeness’’ oc-curred. This, by most objective criteria (Fig. 1caption), would be the branch leading to thepachyophiid-modern snake clade, rather thanthe branch Greene and Cundall prefer (the oneleading to modern snakes alone). Finally, evenif one accepts the suggestion that ‘‘snake ori-gins’’ be considered synonymous with a par-ticular branch, and further accepts that itshould be the branch leading to modernsnakes, these changes still might have oc-curred in a marine context. If one accepts thescenario that marine habits were primitive forthe mososaur-snake clade and that terrestri-ality re-evolved in the branch leading to mod-ern snakes (Lee and Caldwell 2000)—whichGreene and Cundall acknowledge is possi-ble—then a reversion to terrestriality occurredsomewhere along this branch. The corollary is

6 MICHAEL S. Y. LEE

that at least a portion of this lineage—thebranch considered synonymous with ‘‘snakeorigins’’—must have been marine. If the mor-phological changes occurred mostly beforethe ecological reversion to terrestriality, thenmost of ‘‘snake origins’’ would have occurredin a marine context (Fig. 2). Thus, even if oneaccepts Greene and Cundall’s restricted(crown-group) definition of the term‘‘snakes,’’ and that snake origins be restrictedto a single branch, and that this branch shouldbe the one leading to crown-group snakes,snakes might have had marine origins

In conclusion, lack of precise definitions ofvernacular names can severely hinder debateon the origins of major groups. However, thereis no clear consensus on the precise meaningsof many, if not most, vernacular terms (e.g.,tetrapod, amphibian, reptile, bird, or mam-mal). Various solutions are possible. One is toavoid the use of such terms when there is anypossible ambiguity, such as when transitionalfossils are being discussed. The alternativeand perhaps more desirable solution is to tryand reach some agreement, by adopting a sci-entifically acceptable (monophyletic) defini-tion that is as similar as possible to the exist-ing interpretation used by the majority of peo-ple (both scientists and laypeople). However,there will be cases where such an agreementcannot be reached, and in such cases the in-tended meaning should be explicitly noted ev-ery time these terms are used. In the currentexample, there are clear reasons to apply thevernacular term ‘‘snakes’’ to embrace not justmodern snakes, but also recently describedfossil limbed forms (pachyophiids). Also,there is no generally accepted definition ofwhat constitutes a group’s ‘‘origins,’’ and verybroad and very narrow interpretations arepossible. An explicitly phylogenetic definitionof ‘‘origins’’ is proposed here: The origin of agroup consists of the changes that accumulat-ed along its stem lineage between its diver-gence from its nearest living sister group andthe radiation of extant (crown-group) forms.

Acknowledgments

I thank H. Greene and D. Cundall for dis-cussion and encouragement despite our dis-

agreements; M. Benton, D. Fisher, and J. Scan-lon for comments; and the Australian Re-search Council for funding.

Literature CitedBryant, H. N. 1994. Comments on the phylogenetic definition of

taxon names and conventions regarding the naming ofcrown-clades. Systematic Zoology 43:124–130.

Cantino, P. D., R. G. Olmstead, and S. J. Wagstaff. 1997. A com-parison of phylogenetic nomenclature with the current sys-tem: a botanical case study. Systematic Biology 46:313–331.

Clack, J. A. 1997. Devonian tetrapod trackways and trackmak-ers: a review of the fossils and footprints. Palaeogeography,Palaeoclimatology, Palaeoecology 30:227–250.

Cundall, D. 1995. Feeding behaviour in Cylindrophis and itsbearing on the evolution of alethinophidian snakes. Journal ofZoology 237:353–376.

de Queiroz, K., and J. Gauthier. 1992. Phylogenetic taxonomy.Annual Review of Ecology and Systematics 23:449–480.

Estes, R., K. de Queiroz, and J. Gauthier. 1988. Phylogenetic re-lationships within Squamata. Pp. 119–281 in R. Estes and G.K. Pregill, eds. Phylogenetic relationships of the lizard fami-lies. Stanford University Press, Stanford, Calif.

Gauthier, J. 1986. Saurischian monophyly and the origin ofbirds. Memoirs of the California Academy of Sciences 8:1–55.

Gove, P. B., ed. 1976. Webster’s third new international dictio-nary of the English language unabridged, Vols. I–III. Ency-clopaedia Britannica, Chicago.

Greene, H. W. 1873. Dietary correlates of the origin and radia-tion of snakes. American Zoologist 23:431–441.

———. 1997. Snakes: the evolution of mystery in nature. Uni-versity of California Press, Berkeley.

Greene, H. W., and D. Cundall. 2000. Limbless tetrapods andsnakes with legs. Science 287:1939–1940.

Kardong, K. V., T. L. Kiene, and V. Bels. 1997. Evolution of tro-phic systems in squamates. Netherlands Journal of Zoology47:411–427.

Kemp, T. S. 1982. Mammal-like reptiles and the origin of mam-mals. Academic Press, London.

Lee, M. S. Y. 1996. Stability in meaning and content of taxonnames: an evaluation of crown-clade definitions. Proceedingsof the Royal Society of London B 263:1103–1109.

Lee, M. S. Y., and M. W. Caldwell. 1998. The anatomy and re-lationships of Pachyrhachis, a primitive snake with hindlimbs.Philosophical Transactions: Biological Sciences 353:1521–1552.

———. 2000. Adriosaurus and the affinities of mosasaurs, doli-chosaurs, and snakes. Journal of Paleontology 74:915–937.

Padian, K., and L. Chiappe. 1998. The early evolution of birds.Biological Reviews 73:1–42.

Rowe, T. 1988. Definition, diagnosis, and origin of Mammalia.Journal of Vertebrate Paleontology 8:241–264.

Rowe, T., and J. Gauthier. 1992. Ancestry, paleontology, and thedefinition of the name Mammalia. Systematic Biology 41:372–378.

Scanlon, J. D., and M. S. Y. Lee. 2000. The Pleistocene serpentWonambi and the early evolution of snakes. Nature 20:416–420.

Scanlon, J. D., M. S. Y. Lee, M. W. Caldwell, and R. Shine. 1999.The paleoecology of the primitive snake Pachyrhachis. Histor-ical Biology 13:127–150.

Sereno, P. C. 1999. Definitions in phylogenetic taxonomy: cri-tique and rationale. Systematic Biology 48:329–351.

Tchernov, E., O. Rieppel, H. Zaher, M. Polcyn, and L. L. Ja-cobs. 2000. A fossil snake with limbs. Science 287:2010–2012.