Evolutionary Relationships in the Family Salamandridae Author(S): David B
Evolutionary Relationships in the Family Salamandridae Author(s): David B. Wake and Neclâ Özeti Reviewed work(s): Source: Copeia, Vol. 1969, No. 1 (Mar. 6, 1969), pp. 124-137 Published by: American Society of Ichthyologists and Herpetologists (ASIH) Stable URL: http://www.jstor.org/stable/1441702 . Accessed: 24/01/2012 13:21
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http://www.jstor.org Evolutionary Relationships in the Family Salamandridae
DAVID B. WAKE AND NECLA OZETI Data on 40 characters, 27 relating to feeding mechanisms, were as- sembled in order to analyze evolutionary relationships in the family Salamandridae. In most instances, primitive and derived states were identified, and in many cases, state phylogenies for each character were hypothesized. Phenetic schemes of character analysis, including single and average linkage techniques and the results of inclusion and exclusion of primitive character states, were compared. There are significant dif- ferences, and exclusion of primitive character states is recommended. We put most emphasis on a combinatorial analysis of our own, which takes into account the changes in the feeding system as a single complex unit and also makes use of the phenetic methods in which primitive character states are excluded. The result is the placement of the 14 genera in four groups: A. Salamandra, Chioglossa, Salamandrina; B. Triturus, Euproctus, Neurergus, Paramesotriton, Cynops, Hypselotriton, Pachytriton, Taricha, Notophthalmus; C. Pleurodeles; D. Tylototriton. The very primitive groups C and D are slightly modified remnants of ancient groups. Group A is the most derived group. Chioglossa and Salamandrina are the most specialized genera. Of two computer methods for deducing phylogenies, one compares well with these results, but the other does not.
INTRODUCTION which, for various reasons, appear to carry T HE family Salamandridae includes 14 useful information. Our data from feeding genera and about 43 species, distributed mechanisms do not indicate whether we broadly throughout the Holarctic region. are dealing with an integrated system under Considerable information concerning sala- a relatively simple genetic control, or whether mandrid anatomy and evolutionary relation- the parts (our 27 characters) are discrete ships appeared in the German literature of and evolving independently. Probably state the 1930's, and the monograph by Herre changes in several characters are due to re- (1935) remains the most authoritative ref- sponses to a single selection pressure, but erence on the family. The work of Herre this cannot now be determined. We think and others resulted in the inclusion in the that careful analysis of such an adaptive family Salamandridae of the genera pre- complex will provide useful information for viously placed in the family Pleurodelidae, the deduction of the phylogeny. Feeding is and the distribution of regionalized groups an extremely important activity and several of species of Triturus to several genera. Their clearly adaptive trends in the system are statements concerning salamandrid evolution associated with ecological shifts. In deducing have not been reevaluated, but von Wahlert phylogeny, knowledge of community of (1953) and others added new information descent is sought, and we feel that very that has, in general, tended to corroborate complex systems, where the chance of paral- their findings. Nevertheless, many aspects of lelism and convergence is reduced, offer the evolution in the family have not been best sources for such information. Biological studied, including feeding and locomotor information for systems other than the feed- systems. Data accumulated during our study ing system has been added, for we wish to on feeding mechanisms (Ozeti and Wake, make this study as comprehensive as our 1969) are used in this paper to reinvestigate present knowledge of the group permits. salamandrid relationships and to attempt to Our working hypothesis is that information deduce the phylogeny of the group. concerning relationship in primary groups Descriptive portions of our comparative (e.g., the family Salamandridae) is contained morphological paper are condensed here to only in derived character states. Resem- 27 characters. To these we add an additional blance that results from characters shared 13 that either have been used by others or in states that are primitive for the primary 124 WAKE AND OZETI-SALAMANDRID RELATIONSHIPS 125 group has no phylogenetic information. We salamander groups other than salamandrids. are interested in community of descent with Nevertheless, presence of the arch is con- change, and retention of primitive conditions sidered primitive (0), partial development a is essentially non-descent and provides no derived state (1), and absence a more de- information. Derived states which occur rived state (2). only in single taxa similarly have no infor- 3. Maxillary length. The toothed portion mation concerning relationships, but they of the maxillary bone of amphibians is do provide information concerning degree primitively very long. In the most primitive of derivation of a group; five of our 40 char- salamandrid state the maxillary extends vir- acters fall into this category. tually to the quadrate, or falls just short of Analysis of the 40 characters has been that bone (0). In a derived state the max- based on the premise that a character state illary extends past the eye but falls far of universal occurrence in related, primitive short of the quadrate (1). A more derived families, or in early fossil ancestors, is primi- state finds the maxillary falling short of the tive for the group under consideration. We posterior margin of the eye (2). have rigorously applied this standard, and 4. Nasal bone contact. In hynobiid and feel that the following analysis is conserva- cryptobranchid salamanders the nasals are tive in this regard. Where there is doubt, we in broad median contact. Such a condition is have not identified a primitive state, except considered to represent the primitive state where an apparently clear evolutionary trend in salamandrids (0). Narrow contact is con- exists within the primary group. To facili- sidered a derived condition (1), and no con- tate computer analysis we have coded the tact is a more derived state (2). characters in the following manner (Table 5. Operculum. Opercula are ossified in 1): primitive state (0), derived states (1, 2, primitive salamanders. In salamandrids os- etc.), character not present or inapplicable sification or mineralization is considered or no information (9). Reference to primi- primitive (0), and unmineralized cartilage is tive salamander families applies to the derived (1). families Hynobiidae, Cryptobranchidae, and 6. Caudosacral ribs. There is a general evo- Ambystomatidae, unless specified. lutionary trend in amphibians for reduc- In some instances data have been obtained tion and loss of postsacral ribs, borne on from the literature, especially in regard to caudosacral vertebrae. Accordingly, caudo- osteology (data from Bolkay, 1928; Herre, sacral ribs are considered to represent a 1932, 1933, 1935, 1939; Wolterstorff and primitive state (0) and absence is derived (1). Herre, 1935). 7. Fifth toe. Loss of the fifth toe and fifth distal tarsal is clearly a derived con- CHARACTER ANALYSIS dition (1), since all generalized salamanders 1. Premaxillary fusion. Premaxillary bones have five toes (0). are paired in primitive tetrapods and in 8. Lung reduction. Well developed lungs primitive salamanders. Two premaxillaries are primitively present in salamanders (0). are considered primitive (0) and fused pre- Lung reduction and loss is considered to be maxillaries derived (1). derived (1; see Liidike, 1955). 2. Frontosquamosal arch. Frontosquamosal 9. Skin 'texture. It is not possible to ascer- arches are found only in the "family Sala- tain whether or not rough skin such as mandridae. There are many fossil sala- that encountered in the terrestrial newts is mandrids, but most are represented only by primitive or derived. However, since it seems vertebral fragments. Some are known from to be associated with a primitive way?:of complete skulls and the earliest of these life and is absent only in those groups that (Tylototriton weigelti, Middle Eocene; Paleo- have diverged from that pattern, we con- taricha oligocenia, Upper Oligocene; Oligo- sider roughened, keratinized skin to be semia spinosa, Oligocene; Heliarchon fur- primitive (0) and smooth skin to be derived cillatus, Lower Miocene) have well developed in one direction in terrestrial environments arches. The general trend is for bone re- (1) and in another in aquatic habitats (2). duction in salamanders, and the arches are 10. Egg size. Primitively salamanders lay undergoing apparent reduction in certain large numbers of small eggs. Such a pattern genera (e.g., Triturus). However, fronto- is considered primitive (0), and the laying squamosal arches do not occur in primitive of medium-sized eggs is considered to be de- 126 COPEIA, 1969, NO. 1 rived (1). Large eggs constitute the most 19. Second ceratobranchial. There is evi- derived state (2) (some data from Wolter- dence that the last three elements have sepa- storff and Herre, 1935). rate histories in the family. Since all are 11. Courtship pattern. Salthe (1967) has subjected to unique mechanical pressures, described three courtship patterns in the it is likely that different selective pressures family Salamandridae. He considers that are also operative. Primitively the element found in Euproctus to be primitive (0), and is ossified (0). A derived state finds the we have followed him. He recognizes two element partially mineralized (1), and the derived states (1 and 2). element is unmineralized cartilage in the 12. Reproductive pattern. Oviparity is more derived state (2). primitive in amphibians (0). Ovoviviparity 20. Ceratohyal. This element is partially or viviparity are considered derived (1). ossified primitively (0). It is entirely un- 13. Second basibranchial. The second basi- mineralized cartilage in the derived state (1). branchial is present primitively in salaman- 21. Length of first ceratobranchial. This ders and its presence here is considered element primitively extends about to the primitive (0). Presence of occasional rudi- posterior tip of the second ceratobranchial ments is considered derived (1) and total (0). It is very much longer in the derived absence is a more derived state (2). state (1). 14. Epibranchial. Presence of an epibran- 22. Form of rectus cervicis profundus. The chial is a primitive state in salamanders (0). derived condition is characterized by the Fusion or loss is considered derived (1). presence of a distinct lengthening loop (1), 15. Radii. Since the first pair of radii which is not present primitively (0). represents an apparent remnant of the hypo- 23. Insertion of rectus cervicis profundus. hyals, elements present in more primitive In primitive salamanders this muscle has salamanders and in larvae, we consider two several heads (0). In certain salamandrids pairs of radii to represent a primitive state a derived condition is found that is char- (0). Loss of the anterior pair is a derived acterized by a single insertion (1). state (1). 24. Myocommata in rectus cervicis pro- 16. Interradial cartilage. The interradial fundus. Primitively many myocommata are cartilage is a functionally significant element present in salamander muscles. The most found only in forms that have lost the first primitive state in salamandrids finds three pair of radii. Thus absence of the element myocommata between the sternum and in- may be considered primitive (0). We recog- sertion (0). A derived state finds but one nize three derivative states. The least de- (1), and in a more derived state there are rived finds the element very well developed none (2). (1). The intermediate state is an element 25. Hebosteoypsiloideus. We consider the of reduced size (2). The most advanced less differentiated state to represent the state is presumed loss of the element in a primitive state (0), and the more differenti- single genus (Notophthalmus) that is a mem- itted to represent a derived state (1). ber of the group in which the element is 26. Inter-ossa-quadrata. Primitive salaman- otherwise found (3). ders have a well developed muscle (0). One 17. First basibranchial. The first basibran- derived state is represented by a distinct chial is primitively ossified (0). A derived reduction of the muscle with only a few state finds a cartilaginous element that is muscle fibers extending to the medial raphe mineralized (1), and in the most derived (1). A more derived state finds all fibers state the element is unmineralized carti- falling short of the raphe (2). lage (2). The first basibranchials of Chio- 27. Tongue. Tongues of four general types glossa and Salamandrina are probably can be recognized in salamandrids. The secondarily ossified in response to pressures most primitive type is similar to that found exerted by the enlarged basiradialis muscles in primitive hynobiids and ambystomatids, during tongue flipping, but in the absence and has a well developed tongue pad but of conclusive evidence they are called primi- lacks a free posterior flap (0). One derived tive. state (1) is found in Pachytriton, an aquatic 18. First ceratobranchial. This element is form that lacks a differentiated tongue pad. primitively bony (0) in salamanders. It is In another direction, evolutionarily, is a cartilaginous in the derived state (1). tongue pad with somewhat free posterior WAKE AND OZETI-SALAMANDRID RELATIONSHIPS 127 margins (2). The most derived state of this slips that attach to the posterior part of the trend is a tongue pad with a large, free first basibranchial(2)i to that part and to posteriorflap (3). the radii (3), or to neither part (1). We are 28. Basiradialis. Primitively this muscle is not certain which, if any, is the primitive rather small and weak to relatively well de- state; states 1 and 2 are found in other veloped (0). In the derived state the muscle primitivesalamanders. is verywell developedand strong(1). 35. Radioglossusand hyoglossus. The prim- 29. Rib protrusion. Rib processes either itive state has but a single, undifferentiated protrude (1) or do not (2) from the body and unpaired muscle (0). In one direction wall. The processes occur in many fossil the muscle differentiates and both parts, salamandridsand may be primitive features but particularly the radioglossus, are well of the family, but we are unsure of this. Pro- developed (1). In another direction the trusion is not found in other families of muscle is differentiated and a single hyo- salamanders,and we prefer not to identify glossus and a paired radioglossusare found one or the other of these states as primitive (2). The radioglossalsare not well developed. at this time. In a third derived state (3) the muscles are 30. Rectus abdominis profundus. Maurer greatlyreduced. (1892) first demonstrateddifferences in the 36. Depressormandibulae. This musclemay degree of differentiation of the trunk mus- have a single part (3), two skeletal heads cles of salamanders,but he emphasizedonly (2), or a skeletal head and a cutaneous head Triturus and Salamandraamong the sala- (1). We cannot identify a primitivestate. mandrids. From our dissections and analy- 37. Subhyoideus. The muscle is either not sis of histologicalsections, we have been able attached to the mandible (3), attached by to extend these observationssomewhat. In muscle fibers to the mandible (2), or at- primitive salamandersthis muscle is not dis- tached to the mandible by a tendon (1). tinct from the rectus abdominis superficialis The state that lacks mandibular attach- (0). In the derived state the two muscles ment is probablythe primitiveone, since the are differentiatedand separate(1). muscle is derived from hyoidean constrictors, 31. Medial superficial fibers of genioglos- but we cannot be certain. sus. Primitively the superficial fibers are 38. Interradialis. Primitively the muscle is extensive and include medial fibers that in- present (0), but it may be very well de- sert in the vicinity of the tips of the cera- veloped (1) or absent (2). tohyals (0). The medial fibers are absent, 39. Ratio of epibranchialto ceratobranchial. but the lateral ones are relatively well de- The epibranchial is either shorter (1) or veloped in the derivedstate (1). longer (2) than the ceratobranchial. The 32. Relation of geniohyoideusto genioglos- short epibranchial is likely the primitive sus. Primitively the geniohyoideus muscles state, since lengthening of the epibranchial are attached to well differentiated genio- in other groups is associatedwith derivative glossal muscles by dense beds of connective features of tongue protrusion. However, we tissue lying at the anterior ends of the cera- have not identified either state as primitive. tohyals (0). In one derived state the con- 40. Maxillary-pterygoidjoint. A maxillary- nection is absent (1). In an entirely different pterygoid joint is either present (1) or trend the connectionis presentbut the genio- absent (2). Primitive salamanderslack such glossusis not differentiated(2). joints and state 2 may be primitive; in the 33. Insertion of the rectus cervicis super- absence of good evidence we have not iden- ficialis. Two states are found. In the first tified either state as primitive. (1) the muscleinserts primarily in the vicinity Distributionof characterstates in the sala- of the attachmentof the first ceratobranchial mandrid genera is summarizedin Table 1. to the first basibranchial,and in the second Table 2 summarizesthe characterstate trees, (2) a well developed slip extends far an- or the presumeddirection of change or evo- teriorly to insert near the tip of the first lutionary trends for each character. Infor- basibranchial.The simpler state (1) is prob- mation in these tables is used below to aid ably primitive, but we have no good evi- in outlining major patterns of phenetic re- dence. lationships, and, in the following section, 34. Insertion of the rectus cervicis pro- in elucidating phyletic patterns. Our data fundus. The rectus cervicis profundus has are mainly from systemsrelated to feeding 00
TABLE 1. DISTRIBUTIONOF CHARACTERSTATES IN SALAMANDRIDGENERA. See text for coding. Character 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 Salamandra 0 2 0 0 1 1 0 0 1 2 1 1 0 1 0 0 2 1 2 1 0 0 1 2 1 2 2 0 2 1 1 1 2 1 3 2 3 2 9 2 z,, Chioglossa 0 2 2 0 1 1 0 1 1 2 9 0 0 1 1 0 0 1 2 1 1 0 1 1 1 1 3 1 2 1 0 1 1 1 3 2 1 0 9 2 Salamafdrina 0 0 0 2 1 0 1 1 0 9 9 0 2 1 1 0 0 1 2 1 0 1 1 2 1 2 3 1 1 1 0 1 1 1 1 1 2 1 9 2
Pleurodeles 0 0 0 0 0 0 0 0 0 0 1 0 2 0 0 0 2 0 2 0 0 0 1 1 0 0 0 0 1 1 0 0 1 1 3 3 3 0 2 2 0 ItI Tylototriton- 0 0 0 0 0 0 0 0 0 1 0 1 000 1 020 0 0 0 0 0 0 0 0 1 1 00 1 20 3 302 2 Euproctus 1 0 2 2 1 1 0 1 0 2 0 0 1 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 1 3 3 3 3 0 2 1 Triturus 1 1 2 2 1 1 0 0 0 1 2 0 2 0 1 1 0 0 2 0 0 0 0 0 0 0 0 0 2 0 0 0 1 3 2 3 2 0 2 2
Neurergus 1 1 2 2 1 1 0 0 0 2 9 0 2 0 1 1 0 0 1 0 0 0 0 0 0 1 0 0 2 9 0 0 1 3 3 3 3 0 1 2
Notophthalmus 1 0 1 1 1 1 0 0 0 1 2 0 2 0 1 3 1 0 1 0 0 0 0 0 0 0 0 0 2 9 0 0 1 3 2 3 3 0 1 2 Taricha 1 0 0 2 0 1 0 0 0 1 2 0 2 0 1 2 1 0 1 0 0 0 0 0 0 0 0 0 2 9 0 0 1 3 3 3 3 0 1 2
Cynops 1 0 2 0 0 1 0 0 0 2 2 0 2 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 2 0 0 0 1 3 3 3 2 0 2 2 Paramesotriton 1 0 0 2 1 1 0 0 0 2 9 0 2 0 1 1 0 0 2 0 0 0 0 0 0 0 0 0 2 9 0 0 1 3 2 3 3 0 1 2
Hypselotriton 1 0 2 1 0 0 0 0 2 9 9 0 2 0 1 1 0 0 0 0 0 0 0 0 0 0 0 0 2 9 0 0 1 3 3 3 3 0 2 2
Pachytriton 1 0 2 2 1 1 0 0 2 2 9 0 2 0 1 1 0 0 0 0 0 0 0 0 0 0 1 0 2 0 9 2 1 3 3 3 3 0 2 1 WAKE AND OZETI-SALAMANDRID RELATIONSHIPS 129
TABLE 2. CHARACTERSTATE TREES.
State relation Character(see text) 0 - 1 1,5,6,7,8,12,14,15,18,20,21,22,23,25,28,30,31
0 - 1 - 2 2,3,4,10,11,13,17,19,24,26 0 --+1 - 2 -+ 3 16
0 9,32,38
0 27,35 2 3 -- 1 - 2 29,33,39,40 1 - 2 - 3 34,37 1,2,3 36 and this, of course, places limitations on whether the states are primitive or derived, our interpretation. The body of data is Hypselotriton and Cynops have the greatest relatively large and is derived from an ex- phenetic similarity (89%). The lowest simi- amination of all genera. We have therefore larity among genera of group B is 68% prepared an analysis of evolutionary rela- between Pachytriton and Notophthalmus. In tionships. contrast, the highest similarity in group A is Similarity matrices are presented in Table 63% (Chioglossa-Salamandra) and the lowest 3. Total similarity (in roman type) and sim- is 46% (Salamandrina-Salamandra). The ilarity based on characters shared in other highest similarity between members of groups than known primitive states (in italics) are A and B is 43% (Chioglossa-Neurergus) and presented. In addition, on the diagonal (in the lowest is 25% (Pachytriton-Salaman- bold face) is presented the percentage of drina). Pleurodeles is most similar to Sala- characters for each genus that are in other mandra (49%) and least to Chioglossa (42%) than known primitive states; this is at least among genera of group A, and to Hypselo- a rough approximation of the relative degree triton (68%) and Pachytriton (50%) respec- of divergence from a presumed common an- tively among group B. Tylototriton is most cestor. Genera are listed from top to bottom similar to Salamandra (39%) and least to in increasing degree of primitiveness. From Chioglossa (32%) among genera of group A, the data in this table, we may select four and to Hypselotriton and Taricha (68%), and generic groups for discussion: A. Chioglossa, to Pachytriton (50%) respectively among Salamandrina, Salamandra; B. Neurergus, group B. Pleurodeles and Tylototriton share Pachytriton, Notophthalmus, Triturus, Ta- 85% of their characters in the same state. richa, Euproctus, Paramesotriton, Hypselo- As discussed earlier, we believe that more triton, Cynops; C. Pleurodeles; D. Tyloto- information concerning phylogeny is to be triton. derived from an analysis in which character Chioglossa, Salamandrina, and Salamandra states known to be primitive for the primary are about equally derived (by our gross esti- group as a whole are excluded (such as mation, Table 3, diagonal) from a presumed italicized matrix in Table 3), than one in familial ancestor. These genera are con- which these states are included. When states siderably more derived in the characters known to be primitive are excluded, the analyzed than the remaining genera. Among similarity matrix is considerably modified, the remainder, Neurergus and Pachytriton especially among those genera which retain are the most derived, and Tylototriton is the many primitive characters. The highest de- most primitive. gree of similarity now is 47% (Chioglossa- Based on the percentage of total char- Salamandra) and occurs within group A acters shared in the same state, regardless of rather than group B. The lowest similarity 130 COPEIA, 1969, NO. 1
TABLE 3. SIMILARITYMATRICES1 FOR SALAMANDRIDGENERA. Genus 1 2 3 4 5 6 7 8 9 10 11 12 13 14 1 Chioglossa 74 57 63 43 35 30 37 30 40 38 36 40 42 32 2 Salamandrina 43 73 46 31 25 28 35 31 30 39 28 30 46 38 3 Salamandra 47 35 72 32 30 26 27 29 26 35 28 28 49 39 4 Neurergus 27 17 19 53 78 79 84 82 82 87 78 82 55 55 5 Pachytriton 22 14 16 41 53 68 76 70 87 78 81 82 50 50 6 Notophthalmus 16 14 13 34 27 51 80 87 69 84 76 74 56 62 7 Triturus 21 22 13 37 34 33 50 77 78 87 78 85 55 58 8 Taricha 16 14 13 37 30 39 31 46 72 84 78 80 64 68 9 Euproctus 24 14 15 37 42 23 30 26 45 82 81 83 53 58 10 Paramesotriton 22 19 19 40 35 34 37 32 32 45 78 82 63 66 11 Hypselotriton 19 11 14 32 33 27 30 27 30 27 41 89 68 68 12 Cynops 21 14 13 34 34 26 35 28 30 29 32 40 63 63 13 Pleurodeles 21 22 23 16 16 13 15 15 13 16 19 15 38 85 14 Tylototriton 11 14 13 11 11 113 3 13 13 13 13 14 10 23 30 1 Roman type--total similarity (per cent); italics--similarity (per cent) in characters shared in other than known primitive states; bold face-percentage of characters that occur in states other than known primitive states. among genera of group A (35%, Salamandra- phylogenetic relationships within the family Salamandrina) is high relative to the family Salamandridae. The family is represented as a whole. The highest degree of similarity by a rather good fossil record (for list of among genera of group B is 42% (Euproc- currently recognized species see Brame, 1967). tus-Pachytriton) and the lowest is 23% Most of the fossils are represented only by (Euproctus-Notophthalmus). The average vertebrae, however, and these are currently similarity within group B is now 30%, which being studied by several workers. In addition, contrasts strikingly with the average of 77% studies are being conducted on vertebral when primitive states are included (Figs. 3, morphology of recent forms in the laboratory 4). By contrast, average similarity within of the senior author and these indicate that group A has dropped only from 51% with modern salamanders are so poorly known primitives included to 39%. The highest in terms of vertebral variation that mean- similarity between members of groups A and ingful interpretation of fossil vertebrae is B is 27% (Chioglossa-Neurergus) and the not possible at this time. For these reasons lowest is 11% (Salamandrina-Hypselotriton). and because very little information concern- Pleurodeles is almost equally similar to all ing those anatomical features that we have members of group A (21-23%), but is most studied is available from the fossils, we have similar to Hypselotriton (19%) and least chosen to use a deductive approach, utiliz- similar to Euproctus and Notophthalmus ing as the primary data those presented in (13%) among genera of group B. Tyloto- our previous paper (Ozeti and Wake, 1969). triton and Pleurodeles share only 23% of We have sought character correlations and their characters in states other than those in this search we have been greatly aided by known to be primitive. This is a figure computer programs prepared by Joseph Felsenstein and Glenn both of equivalent to the lowest similarity within Sharrock, the of These group B. Tylototriton has so few non- University Chicago. procedures have enabled us to view our data from primitive states that further comparisons are several standpoints, and the result of this relatively meaningless (range from 10-14%). analysis is the cladogram, discussed below, in 7. Four EVOLUTIONARY PATTERNS AND RELATIONSHIPS presented Fig. phenograms (Figs. 1-4), prepared by single and average link- From the data in the presented compara- age clustering methods (Sokal and Sneath, tive of this from our parts paper, analysis 1963) are useful in illustrating phenetic re- of functional morphology, and from the lationships. Two cladograms (Figs. 5, 6) character analysis presented above we have have been generated by electronic digital formulated an hypothesis concerning the computers. One (Fig. 5) was prepared by WAKE AND OZETI--SALAMANDRID RELATIONSHIPS 131
------CHIOGLOSSA L------SALAMANDRA
------SALAMANDRINA
------CYNOPS
L-----HYPSELOTRITON
------TRITURUS
I IS--•------NEURERGUS I I - -I I L------PARAMESOTRITON NOTOPHTHALMUS iL-r.------L------TARICHA -----EUPROCTUS ------I I ------PACHYTRITON ------PLEURODELES
------I L------TYLOTOTRITON
I I I I I 55 65 75 85 95 Fig. 1. Relationshipsof salamandridgenera. Phenogram constructed by single linkage method with primitive statesincluded. utilizing the minimum evolutionary steps placed as close together as possible. It method of Camin and Sokal (1965). The utilized the character state trees and is a other (Fig. 6) is based on a computer pro- phylogenetic method (cf. Inger, 1967). gram prepared by Joseph Felsenstein. This Comparison of phenograms constructed by method attempts to minimize the number of the same method, but with primitive states convergences in the tree. Where convergence included in one case and excluded in the cannot be avoided, the convergent taxa are other, is instructive. In Figs. 1 and 3 primi-
------CHIOGLOSSA I- ---7 I------SALAMANDRA ------SALAMANDRINA ------CYNOPS
-- --TRITURUS I -I --II
S------EUPROCTUS I I I------PACHYTRITON
IL---I ------NEURERGUS I. . . . .II - l LI------PARAMESOTRITON ------NOTOPHTHALMUS II r~--I --- S------TARICHA
------HYPSELOTRITON L------PLEURODELES
------TYLOTOTRITON
15 25 35 45 55 Fig. 2. Relationships of salamandridgenera. Phenogram constructed by single linkage method with known primitive states excluded. 132 COPEIA, 1969, NO. 1
------CIIIOGLOSSA I------I I------L------SALAMANDRA
------SALAMANDRINA ..----CYNOPS ['; - -- I S-----HYPSELOTRITON
------EUPROCTUS
_------PACHYTRITOINI-..--TRITURUS
PARAMESOTRITON? ------.. L------NEURERGUS - L------I ---..NOTOPHTI!ALMUS I...[. L------TARICHA ------I------PLEURODELES S------TYLOTOTRITON
35 45 55 65 75 85 95 Fig. 3. Relationships of salamandridgenera. Phenogram constructedby average linkage method with primitive states included. tive states have been included. In both two resemblances based on shared primitive states very distinct phenetic groups are evident. are excluded (Figs. 2, 4) the pattern is rather Similarities are low in the Chioglossa-Sala- drastically changed. Pleurodeles and Tyloto- mandra-Salamandrina group. The remain- triton are joined at a very low level, and the ing genera fall into two groups, a Triturus average similarity within the Triturus group group in which similarities are very high, is also low. The Salamandra group is at the and a Tylototriton-Pleurodeles group with relatively highest level of the three. The the similarity at a very high level. When similarities of genera within the Salamandra
------CHIOGLOSSA
------SALAMANDRA
------F ------SALAMANDRINA
------CYNOPS
I------TRITURUS _jJ .. .I i II ------NEURERGUS
I II --- L ------r------EUPOCTUSPARAMESOTRITON SI III
------PACHYTRITON '--i------I IL------HYPSELOTRITON ------NOTOPHTHALMUS L------TARICHA
------PLEURODELES ------TYLOTRITON
15 25 35 4 5 . .I Fig. 4. Relationships of salamandridgenera. Phenogramconstructed by average linkage method with known primitive states excluded. WAKE AND OZETI-SALAMANDRID RELATIONSHIPS 133
also character Thus r----CHIOGLOSSA emphasized complexes. r- trends L-- --SALAMANDRA we have tried to consider not only the in the unit characters(i.e., as outlined in -L------SALAMANDRINA Table but also those in the entire func- - 2) I tional unit associated with feeeding r----PLEURODELES (Ozeti L----TYLOTOTRITON and Wake, 1969).This approachis less opera- tional than those of Felsenstein and Camin S----CYNOPS ----I and Sokal,and is rather How------1 -- group-specific. L----HYPSELOTRITON ever, several premises are shared, especially with the Felsenstein method (e.g., exclusion L ---IEUPROCTUS ---I of primitivestates, considerationof character r. L----.PACHYTRITON state We our method,four -- trees). recognizeby --TRITURUS groupswithin the family Salamandridae(Fig. L..----NEURERGUS 7). These are: A. Salamandra,Chioglossa, Salamandrina;B. Triturus, Neur- -L------PARAMESOTRITON Euproctus, ergus, Paramesotriton, Cynops, Hypselotri------NOTOPHTHALMUS ton, Pachytriton,Taricha, Notophthalmus; C. L----TARICHA Pleurodeles; D. Tylototriton. We do not Fig. 5. Relationships of salamandrid genera. assign these genera to different subfamilies Cladogram constructed according to method of at this time, nor do we consider subfamilial and Sokal Camin (1965). recognitionwarranted. Perhapsa lower level taxonomicstatus (tribe?) might be warranted. Our conclusions identifi- group are mostly based on derived states, concerning group cation are identical while those elsewhere in the family are to the results obtained by based on primitive states. For example, the Felsenstein method (Fig. 6), but differ Cynops and Hypselotriton share 89% of from results obtained by the Camin and their characters in the same state, but only Sokal method (Fig. 5). The latter finds es- 32% of the total similarity is based on sentially two groups, with Pleurodeles and shared, non-primitive states. By contrast, Tylototriton being included in a Salamandra Chioglossa and Salamandra share 63% of group. Pleurodeles and Tylototriton have so their characters in the same state, and 47% of few derived characters that it is difficult if their non-primitive characters. not impossible to discuss meaningfully possi- In our phylogenetic analysis we have taken ble relationships. We feel that the best course into account phenetic relationships based on of action is to recognize that each forms a correlation of unit characters, but we have separate group that has probably been dis-
.----.CHIOGLOSSA SL___SALAMANDRA ------SALAMANDRINA
------NEURERGUS I I r------PACHYTRITON I . L----EUPROCTUS F----'
I L------rI.-----HYPSELOTRITON SL....----CYNOPS ------NOTOPHTHALMUS L------TARICHA L~ ---Tl-nu..TRITURUS - L----PARAMESOTRITON
L ------PLEURODELES
L------TYLOTOTRITON Fig. 6. Relationships of salamandridgenera. Cladogramgenerated by electronic computer utiliz- ing program developed by J. Felsenstein. 134 COPEIA, 1969, NO. 1
F----CHIOGLOSSA r.---- L----SALAMANDRA
,------I I------SALAMANDRINA
------EUPROCTUS
---NOTOPHTHALMUS S---I ---I --I
.----TARICHA -----NEURERGUS
SL----L----TRITURUS
7----? ----- PARAMESOTRITON
S------CYNOPS ------I .----HYPSELOTRITON
L-----PACHYTRITON
------PLEURODELES L------TYLOTOTRITON Fig. 7. Relationships of salamandridgenera. Cladogrambased on analysis of feeding mechanisms in the family Salamandridae. See text for explanation. tinct for a very long time. They share many works are concerned, and effectively negates character states with their common ancestor the recognition of two families or subfamilies (possibly the common ancestor of the family), for the salamandrid genera. and they have survived relatively little The Triturus group has a very high degree changed for a very long time. To include of similarity (77% based on average linkage them in the same group or to speak of them analysis, Fig. 3), but most characters are in as being closely related would be quite mis- primitive states and are thus of no use in leading. They are similar because they re- deducing phylogeny. As can be seen from semble an ancient ancestor, not because they Figs. 1-7 there is little congruence among have shared community of descent. the phenograms and cladograms in regard Pleurodeles is probably somewhat more to this group. Notophthalmus and Taricha closely related to the Salamandra group than are closely connected in all methods of analy- to the Triturus group, but Tylototriton is sis, but agreement ends there. We think in a very isolated position within the family. Triturus, Paramesotriton, and Neurergus Tylototriton is more closely related to Pleuro- might form a subgroup, but our evidence is deles than to any other genus but the not strong. Cynops, Hypselotriton, and similarity is at a low level in terms of de- Pachytriton seem to form another group, rived states. The reality of the Pleurodeles- with Pachytriton being closer to Hypselo- Tylototriton-Salamandrina group of Herre triton than to any other genus. In this we (1935) and von Wahlert (1953) is thus called are in disagreement with the Felsenstein and into question. This group seemingly is Camin and Sokal cladograms and with the based on the retention of certain primitive linkage phenograms. We do not think that characters that have been lost or modified Euproctus and Pachytriton are closely re- in the other salamandrids. We reject this lated, as is indicated by the phenograms and as a criterion of evolutionary relationship other cladograms, but that the similarity of and thus reject the group. the two genera in certain features is the Salamandra, Salamandrina, and Chioglossa result of convergence in two groups which form a well defined group. The closest re- entered similar habitats (mountain streams) lationship is between Chioglossa and Sala- in different parts of the world. The two have mandra. Salamandrina apparently diverged arisen from rather generalized ancestors and from the ancestral stock at an early stage. have so few derived characters (mostly of It presents a most peculiar mosaic of char- a convergent nature) that they tend to fall acters in primitive and highly derived states together in most analyses. This is true, for and is in a rather isolated position. Its place- example, of the Felsenstein method where ment by us close to Salamandra and Chio- convergent groups are kept together by de- glossa is unique, at least as far as recent sign. Euproctus has been considered to be WAKE AND diZETI-SALAMANDRID RELATIONSHIPS 135 a close relative of Pachytriton by some au- the basis of our analysis, we conclude that thors (Herre, 1935; Steiner, 1950), but von Tylototriton is the most primitive genus. In Wahlert (1953) and Freytag and Petzold terms of feeding mechanisms, Tylototriton (1962) have emphasized the closer relation- is distinctly primitive. If it had a second ship of Pachytriton to other east Asian basibranchial (some individuals apparently genera, especially Paramesotriton. Based on have, Noble, 1928), it would have a hyo- overall similarity and especially on similar branchial apparatus that would correspond evolutionary trends in feeding mechanisms, precisely with our concept of that which was we consider Pachytriton to be most closely present in ancestral salamandrids. We sug- related to Hypselotriton. The two may have gest that a group of salamanders more arisen from an ancestral stock close to that primitive and generalized than modern which gave rise to Cynops. Cynops is the Tylototriton was widely distributed in Eur- most generalized and Pachytriton the most asia during late Mesozoic times. Modern specialized of these three genera. Euproctus Tylototriton of southeast Asia has remained was probably derived relatively early from relatively close to this group in terms of the stock that gave rise to the Notophthal- morphological similarity, but the similarity mus-Taricha and the Triturus-Neurergus- is based on the very conservative, primitive Paramesotriton subgroups. Euproctus con- nature of most features of Tylototriton. tains three very distinct species and our Primitive salamandrids that were morpho- generalizations concerning the genus are logically similar to modern Tylototriton based on very scanty material. We have existed in Europe as late as Late Miocene been unable to analyze interspecific varia- (Noble, 1928; Herre, 1935), but no longer tion and our statements concerning its re- occur there. The ancestral stock of Pleuro- lationships must be considered tentative. deles probably diverged rather early; mod- Notophthalmus and Taricha are very dis- ern Pleurodeles has many primitive and tinct genera, but evidence for their close re- generalized features. Today, Pleurodeles lationship is fairly good. They have been and Tylototriton represent separate, con- separated from each other for a very long servative stocks derived with relatively little time, for the Oligocene genus Paleotaricha change from the Mesozoic ancestors of the is very similar to modern Taricha in most family. The two genera have doubtless had details. very long, separate histories. We agree with Bolkay (1928), Herre (1932, Salamandra, Chioglossa, and Salamandrina 1935), von Wahlert (1953), and Steiner are the descendents of a third branch of the (1950) in considering Neurergus and Triturus ancestral salamandrid stock. This branch to be very closely related. diverged very early. The major trend Paramesotriton presents several problems. within this group has been in the direction The genus contains three species, P. de- of terrestriality, with the extreme being loustali, a very distinctive species from Viet found in the viviparous Salamandra atra. Nam, and the closely related P. hongkong. Of the three extant genera, ancestors of ensis and P. chinensis. The last two species Salamandrina probably represented the first were included until recently in the genus derivative stock. Salamandrina has become Trituroides (see Freytag, 1962). We have highly specialized, but within the framework studied only P. hongkongensis which we con- of a primitive, generalized morphology (e.g., sider to be more closely related to Triturus separated premaxillary bones, frontosqua- than to any other genus, but there is also mosal arch, rough skin, etc.). Salamandra evidence of relatively close relationship to has also retained a number of primitive other east Asian genera, especially Cynops. characters, but it has become specialized Freytag and Petzold (1961), on the basis of in several ways and a minor adaptive radia- their studies on P. deloustali, suggested that tion has occurred within the relatively wide- the genus is closely related to Cynops. In spread genus (Ozeti, 1967). Chioglossa is the terms of the feeding apparatus, however, the most derived of the three genera, and it has relationship of P. hongkongensis, at least, many specializations. Chioglossa and Sala- to Triturus seems closer than that to Cynops. mandrina are both highly specialized forms Several authors (e.g., Herre, 1935; von that have relict distributions in southern Wahlert, 1953) have considered Salamandra and western Europe. In general body form, to be the most primitive salamandrid. On in the relative mobility of the tongue, in its 136 COPEIA, 1969, NO. 1 coloration, and in its smooth skin and long western Eurasia and its success may have led tail, Chioglossa is remarkably convergent to the extinction of the Tylototriton-like with plethodontids. The distinctly salaman- populations that occurred in that region at drid skeleton and the tongue propulsion least as late as Late Miocene times. This mechanism, which is very different from that stock may have become almost world-wide in of plethodontids, clearly demonstrates that distribution relatively early, perhaps by the convergence, rather than common ancestry, beginning of Tertiary times. Disruption of accounts for the similarity. In Salamandrina this widespread group and subsequent dif- and Chioglossa tongue pad movements are ferentiation of the isolated stock led to the dominant in feeding. In the adetoglossal present evolutionary patterns. Ancestors of plethodontids, the entire hyobranchial ap- Euproctus were probably derived relatively paratus is projected, and tongue pads are early; species of Euproctus today occupy neither as elaborated nor as mobile as in montane streams, specialized environments, the salamandrids. but they have retained some primitive fea- The remaining genera (Euproctus, Tri- tures, notably the most primitive pattern of turus, Neurergus, Paramesotriton, Cynops, breeding behavior in the family (Salthe, Hypselotriton, Pachytriton, Notophthalmus, 1967), that suggest very early derivation. In and Taricha) have probably been derived east Asia, descendants of a somewhat more from an ancestral stock that may have been derived stock than that which gave rise more similar to Tylototriton than to any to Euproctus also invaded montane stream other modern salamandrid. Within this environments. From this were derived the group of nine genera (our Triturus group) a specialized genera Hypselotriton and Pachy- clear trend in the direction of aquatic feed- triton, the latter the most extremely spe- ing specializations is apparent. However, cialized member of the Triturus group. The more than simple aquatic habitation is in- remaining genera have rather similar ways volved, for the generalized Pleurodeles is of life and they represent, in a sense, de- more aquatic than many members of the scendants of a common stock which have Triturus group, which are structurally and evolved partially in parallel. Each has its functionally more specialized. The ancestors own unique features which have evolved in of the Triturus group were perhaps derived response to the selective pressures character- later and from a less generalized and less istic of the diverse region they have in- conservative stock than the ancestors of the habited. Triturus today occupies most of Pleurodeles and Tylototriton groups. How- Europe and Asia Minor, extending as far ever, even within the Triturus group, very southeast as Israel. Its close relative, Neurer- generalized salamanders (e.g., Cynops) have gus, occupies Kurdistan and neighboring survived, and the relatively extremely spe- areas in the Middle East, regions peripheral cialized forms such as Pachytriton are to the south and east of the main Triturus specialized within a framework that is prim- range. The ranges of Paramesotriton and itive relative to such derived salamandrids Cynops overlap in east-central China, but as Chioglossa. generally Paramesotriton ranges to the south Differentiation within the Triturus group and west (to North Viet Nam) and Cynops has been relatively extensive and has re- to the north and east (to Japan). Taricha sulted in many more discrete phyletic lines inhabits western North America and Notoph- (as reflected in the number of genera) than thalmus ranges throughout eastern North in the other three generic groups combined. America and into Mexico. Thus today the In species diversity, too, the Triturus group more generalized but discrete lines derived is dominant. Of the 43 species of living sala- from the generalized ancestral stock of the mandrids recognized by Brame (1967), 28 are Triturus group tend to occupy distinct, sizable in the Triturus group and 9 are species of geographic regions, and these ranges Triturus. Yet the range of differentiation may reflect the ancient disruption of the is not great, and, at least in terms of feeding once widespread ancestral stock. mechanisms, the differences separating any ACKNOWLEDGMENTS two of the three genera in the Salamandra group are greater than those within the We are grateful to many colleagues for entire Triturus group. The ancestral stock their generosity in providing materials for of the Triturus group probably arose in the present study (cited in previous paper). WAKE AND OZETI-SALAMANDRID RELATIONSHIPS 137
In addition we wish to thank Joseph Felsen- INGER,R. F. 1967. The development of a phy- stein and Glenn Sharrock for assistance with logeny of frogs. Evolution 21:369-384. used in data LijDICKE,R. 1955. tVber den Respirationsapparat computer programs analysis. verscheidener Urodelen und seine Beziehungen of this work have been aided a Aspects by zum Herzen. Z. Morph. Okol. Tiere 43:578- Grant-in-Aid of Research from the Society 615. of Xi, NSF GB-3868 and GB- MAURER, F. 1892. Der Aufbau und die Ent- Sigma grants der ventralen bei 6423X, AEC and the wicklung Rumpfmuskulatur grant AT(11-1)-1437, den urodelen Amphibien und deren Bezie- Dr. Wallace C. and Clara A. Abbott Fund hung zu den gleichen Muskeln bei Selachiern of the University of Chicago. u. Teleostiern. Morph.Jahrb. 18:76-179. NOBLE,G. K. 1928. Two new fossil Amphibia of from the Mio- LITERATURECITED zoogeographic importance cene of Europe. Am. Mus. Novit. No. 303, BOLKAY,ST. J. 1928. Die Schlidel der Sala- 13 pp. mandriden mit besonderer Riicksicht auf ihre OZETI, N. 1967. The morphology of the sala- systematische Bedeutung. Z. Anat. Entw. 86: mander Mertensiella luschani (Steindachner) 259-319. and the relationships of Mertensiella and Sala- BRAME,A. H., JR. 1967. A list of the World's mandra. Copeia 1967(2):287-298. recent and fossil salamanders. Herpeton, J. AND D. B. WAKE. 1969. The mor- Southwest. Herpetol. Soc. 2(1):1-26. phology and evolution of the tongue and as- CAMIN, J. H. ANDR. R. SOKAL.1965. A method sociated structures in salamandersand newts for deducing branching sequences in phylog- (family Salamandridae).Copeia 1969(1):91-123. eny. Evolution 19:311-326. SALTHE,S. N. 1967. Courtship patterns and the FREYTAG, G. E. 1962. Ober die Wassermolch- phylogeny of the urodeles. Copeia 1967(1): gattungen Paramesotriton Chang 1935, Pingia 100-117. Wolterstorff Chang 1935 und Hypselotriton SOKAL, R. R. AND P. H. A. SNEATH. 1963. The Mitt. Zool. Mus. Berlin 1934 (Salamandridae). principles of numerical taxonomy. Freeman, 38(2):451-459. San Francisco. ANDH-G. PETZOLD.1961. Beitraige zur Paramesotriton STEINER, H. 1950. Die Differenzierung der Okologie und Anatomie von Salamandrinen wqihrend des deloustali nebst palliarktischen (Bourret 1934) Bemerkungen Rev. SuisseZool. 57:590-603. tiber Pachytriton brevipes (Sauvage 1875). Sitz. Pleistozlns. Ges. Naturf. Freunde Berlin (N.F.) 1:143-162. WAHLERT, G. voN. 1953. Eileiter, Laich und HERRE,W. 1932. Zur Anatomie von Neurergus Kloake der Salamandriden. Zool. Jahrb. Anat. crocatus. Zool. Anz. 100:317-326. 73:276-324. . 1933. Zur Anatomie und systemat- WOLTERSTORFF,W. AND W. HERRE. 1935. Die ischen Stellung von Pachytriton brevipes Sau- Gattungen der Wassermolche der Familie Sala- vage. Z. Anat. Entw. 101:511-524. mandridae. Arch. Naturgesch. N.F. 4:217-229. . 1935. Die Schwanzlurche der mittel- Braunkohle des eoclnen (oberlutetischen) DEPARTMENT OF ANATOMY, THE UNIVERSITY Geiseltales und die Phylogenie der Urodelen unter Einschluss der fossilen Formen. Zoolog- OF CHICAGO,CHICAGO, ILLINOIS 60637. Pres- ica, Stuttgart 87:1-85. ent address of junior author: DEPARTMENT 1939. Studien an asiatischen und EGE BORNOVA- nordamericanischen Salamandriden. Abh. Ber. OF ZOOLOGY, UNIVERSITY, Mus. Naturk. Vorgesch. Magdeburg 7:79-97. IZMIR, TURKEY.