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"PROTOVIPERS" AND THE EVOLUTION OF SNAKE FANGS KENNETHV. KARDONG Department of Zoology, Washington State University, Pullman, Washington 99164 Received September 9, 19i7. Revised August 2, 19i8 Anthony (1955) argued in his summary om toxicity. Certainly, long teeth (fangs) report on the venom apparatus of snakes are effective in delivering venom into a that the fang of viperid snakes evolved prey. It is possible however that injection from a maxillary tooth, specifically a tooth may not have been the initial selective at the posterior end of the maxilla. He factor favoring fang development. In- identified specific colubrid snake genera stead, enlarged teeth may have evolved which, when aligned into a morphocline initially to play a role in prey swallowing (sensu Maslin, 1952), showed an increas- and were secondarily modified into instru- ing similarity in maxillary tooth form to ments for venom injection (Kroll, 1976). the viperid solenoglyph fang. Since then, It is my purpose here 1) to identify possible a search for plausible nacent "protovipers" initial selective advantages of enlarged among the colubrids has continued teeth and, 2) to follow the implications of (Weaver, 1965; Kroll, 1976). enlargement in "protoviper" evolution. Certainly, colubrids are a promising group in which to search for clues to the evolution of the viperid fang and associ- ated apparatus. Over half (51.5%) of the Swallowinrr events were observed di- 309 species of colubrids examined by rectly and by cinematography followed by Marx and Rabb (1972) had enlarged teeth frame-by-frame analysis. Filming was at the posterior end of the maxilla and of done at speeds of 25, 50, or 200 frames these over one-quarter (26.8%) even had per second with a Hycam 16 mm cine- grooves in these enlarged teeth. The fam- matic camera before two 1000 watt tung- ily Colubridae includes many forms harm- sten photoflood lamps. Over two hundred less to humans, as well as some of the most meters of usable swallowing sequences toxic (e.g., Dispholidus, boomslang; Thel- were obtained of adult snakes of Pituophis otornis, bird snake). Toxicity, or at least melanoleucus, Crotaphopeltis hotamboeia, mild-toxicity, may be more widespread in and Xenodon merremii. Pituophis were colubrids than is appreciated. For in- fed mice and the two other species frogs. stance, some colubrids customarily con- .?\dditionally, single radiographs were tak- sidered non-venomous to humans occa- en of Pituophis and Crotaphopeltis at sionally deliver a painful bite (Heatwole various points in the swallowing cycle and and Banuchi, 1966; Willard, 1967; Johan- assembled into swallowing sequences bocke, 1974; Goellner, 1975). Since many much as described elsewhere (Kardong, colubrids have teeth similar in general ap- 1977). pearance to viperid fangs, and because Dissections were performed under a dis- some of these are mildly to highly ven- section microscope and skulls drawn with omous, many investigators have looked to the aid of a camera lucida attachment colubrids for viperid ancestors. (Wild). Teeth (shown in Fig. 4) were re- The changes leading to the evolution of moved from the posterior end of the max- the viperid fang have usually been attrib- illa from dried snake skulls, placed on uted to the selective advantages accruing mounting stubs, sputter coated with ap- from a progressively more efficient injec- proximately 30 nm of gold, and examined tion system together with increasing ven- with a scanning electron microscope FIG. 1. Three species of colubrids showing three degrees of relative length of posterior maxillaw teeth compared to other teeth borne by the maxilla (mx). .I)Pituophis melanolencus, B) Crotaphopeltis hotam- boeia, C) Dispholidus typus. THE EVOLUTIOS OF SSXKE FANGS 435 FIG. 2. Lateral view of Crotaphopeltis hotamboeia swalloaine the severed hind leg of a frog. Even& unfold left to right as the mavilla is carried forward and tilts In C, the mouth closes bringing the large posterior masillap teeth into the prey; in D the maxilla is retracted, pulling the pre>- into the mouth and, as it does, causing wringling (arrow) of the skin. (ETEC .iutoscan UI). .inatomical termi- enlarged posterior maxillary teeth have nology follows Haas (1973). these secretion grooves or functional equivalents. For instance, in Thamnophis elegans vagrans (western terrestrial garter snake) the posterior maxillan teeth are Two aspects of the maxilla in colubrids enlarged as in Crotaphopeltis but lack a deserve mention because of the special sig- secretion groove or its equal. nificance they have for interpretation of Second, the maxilla of colubrids is "ro- tooth evolution. First, varying degrees of tatable" though much less so than in vi- posterior tooth enlargement can be found. perid snakes. In Pituophis the maxilla of For example, in Figure 1 all three are col- one side advances horizontally over the ubrid species yet among them there is con- prey during swallou7ing and is then siderable difference in relative size of teeth brought downward, its posterior end along the maxilla. In Pitz~ophis,the pos- swinging ventrally first so that rear teeth terior maxillary teeth are smaller than the re-engage the prey slightly before more anterior teeth. However, in Crotaphopel- anterior teeth. This is similar to the swal- tis, and especially in Dispholidus, the lowing motions of Elaphe described in posterior maxillary teeth are enlarged and greater detail b>- Xlbright and Selson the long posterior teeth bear a groove (1959a, b). down which secretions from the oral The maxilla of Crotaphopeltis describes glands can pass. Occasionally, the func- a similar displacement pattern (Fig. 2) ex- tional equivalent to such a secretion cept that during jaw advance over the groove is provided by the channel formed prey it experiences a greater degree of ro- between a pair of enlarged teeth (Taub, tation about its articulation with the pre- 1967). However, not all colubrids with frontal. This causes the maxilla to tip 436 KESSETH 1.. ELiRDOSG FIG.3. Lateral photographs (top) of Crotaphopeltis hotamboeia showing the maxilla advancing forward (left)and during contact with prey (right) when mouth closes. Below each photograph is sketched the position of the maxilla (mx)relative to the prefrontal (pO about which it rotates. sharply out of a horizontal plane (Fig. 3), vantage of the entire sweep of the retrac- resulting in upward swing of its anterior tion motion. end and downward swing of its posterior Long arc.-The posterior teeth are geo- end. As the posterior end of the maxilla metrically farther from the point of rota- is rotated ventrally during closure of the tion about the prefrontal than are the mid- jaws, the rear teeth are the first to pene- dle maxillary teeth. This means that trate into the prey and provide a firm pur- posterior teeth swing through a longer arc chase. Thus, in addition to whatever role than teeth closer to the point of rotation. they may play in prey capture, the en- Any object engaged by the posterior teeth larged posterior maxillary teeth of Crota- will likewise be advanced farther (longer phopeltis also function during swallowing arc) than if carried by more anterior max- to engage the prey firmly and aid in mov- illary teeth. The posterior teeth thus enjoy ing it past the angle of the jaws during a geometric advantage over other teeth of maxillary retraction. the maxilla in that they ride through a lon- ger arc and can thus advance the prey far- ther during each swing of the maxilla. Spikes.-If the prey presents special Engage first. -As described above, the mechanical problems in swallowing, then maxilla, during swallowing, experiences one design adaptation favored may be the displacement such that teeth borne on its elongation of the maxillary teeth. Certain- posterior end are first to engage and hence ly, other adaptive responses are conceiv- the first teeth to start moving the prey able (e.g., increase in tooth number, and1 along. If the prey was not advanced until or change in tooth orientation). However, mid or anterior teeth engaged it, then the lengthening of the teeth allows for much of the retraction motion of the max- deeper penetration. Further, with teeth of illa would have passed before the prey even length, the force of jaw closure is began to move. Since the posterior teeth experienced approximately equally by are the first teeth of the maxilla to engage each individual tooth. But, when a few the prey, the snake is able to take full ad- teeth (e.g., posterior maxillary teeth) proj- THE Ei.OLCTIOS OF SSAKE F.4SGS 43 7 ect beyond the even tooth row, this per- nodon) and viperid snakes. Ancestral to mits the force of jaw closure to be locally both these colubrid genera and to viperids concentrated upon these long teeth. Thus, is an hypothesized "protoviper" presumed a few long, projection teeth not only sink very heterodon- or senodon- like in jaw deeper but also concentrate forces to aid anatomy (Weaver, 1965). Some evidence their penetration. As a consequence, the in support of this phylogenetic relation- elongated projecting posterior maxillan ship comes from serological work (Minton teeth gain secure purchase on the prey. and Salanitro, 1972), but most of this pro- The specific kinds of special mechanical posed Heterodon-ayenodon to viperid af- problems favoring tooth enlargement are finity is based on the viper-like construc- not known. Perhaps the prey may be tion of the maxilla and associated features moist (e.g., amphibians), smooth skinned (Anthony, 1955; Mosauer, 1935; Weaver, (e.g., skinks), or inflated (e.g., toads) and 1965). However, many structures of Xe- thus offer only a slippery or uncertain sur- nodon and Heterodon tire !ikely special face to an even row of teeth. In non-con- adaptations for swallowing, not venom in- stricting snakes, the prey may continue to jection, and upon closer look do not re- struggle even as swallowing proceeds.

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