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Herpetologists' League Comparative Anatomy and Phylogeny of the Cloacae of Salamanders (Amphibia: Caudata). I. Evolution at the Family Level Author(s): David M. Sever Source: Herpetologica, Vol. 47, No. 2 (Jun., 1991), pp. 165-193 Published by: Herpetologists' League Stable URL: http://www.jstor.org/stable/3892733 Accessed: 30-06-2015 16:20 UTC REFERENCES Linked references are available on JSTOR for this article: http://www.jstor.org/stable/3892733?seq=1&cid=pdf-reference#references_tab_contents You may need to log in to JSTOR to access the linked references.

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Herpetologica, 47(2), 1991, 165-193 ? 1991 by The Herpetologists' League, Inc.

COMPARATIVE ANATOMY AND PHYLOGENY OF THE CLOACAE OF SALAMANDERS (AMPHIBIA: CAUDATA). I. EVOLUTION AT THE FAMILY LEVEL DAVID M. SEVER Department of Biology, Saint Mary's College, Notre Dame, IN 46556, USA ABSTRACT: Data on cloacal anatomy were gathered for 128 species of salamanders, representing 48 genera and the nine extant families. Twenty-five characters were recognized, but after resolution of polymorphisms and elimination of autapomorphies, only 12 characters remained for use in phylogenetic analyses at the family level. Weighting the characters equally and using branch-andbound parsimony algorithms, 15 (PAUP) or 9 (Hennig86), equally parsimonious cladograms were revealed, each with 19 steps and a consistency index of 0.63. The variation in phylogenies is due to opposing hypotheses concerning convergence or reversal in two characters: the extent of epidermal lining in the cloaca, and the presence of primary and secondary folds in the cloacal tube. The strict consensus cladogram gives the topology: Sirenidae (Hynobiidae, Cryptobranchidae (Amphiumidae (Salamandridae (Ambystomatidae, Dicamptodontinae (Rhyacotritoninae, Plethodontidae, Proteidae))))). These results and consensus analyses with other cladograms based upon morphological data support the notion that the Salamandroidea, as defined by Duellman and Trueb (1986), is a monophyletic group and that internal fertilization evolved once, and is a synapomorphy for the suborder. Male and female cryptobranchids and hynobiids possess one type of cloacal gland that is not highly dimorphic, and may be a courtship gland that functions in the production of chemical signals during reproductive activities. In the Salamandroidea, portions of the cloacal gland mass (male dorsal and vent glands, female ventral glands) retain the ancestral anatomy and presumed function, while other portions have evolved structural and functional differences relating to spermatophore formation (male pelvic and ventral glands) and storage of spermatozoa (female spermathecae). Courtship glands have been secondarily lost or reduced in some of the Salamandroidea, especially in plethodontids, in which selection apparently has led to adaptations for delivery of courtship pheromones by skin glands rather than reliance on a cloacal source.

Key words:

Cloaca; Salamanders; Phylogeny; Fertilization; Pheromones

THE presence of a cloaca is the primitive vertebrate condition, and bony fish and mammals that lack cloacae are derived (M. Wake, 1979, 1986). Exocrine glands secreting into the cloaca are known for extant amphibians and for sarcopterygian fish, with which amphibians share a common ancestor (Edwards, 1989; Forey, 1986). Among anamniotes, however, salamanders (order Caudata) possess unique complexes of cloacal glands involved in producing courtship pheromones, spermatophores, and/or the storage of spermatozoa. The "rectal glands" in the sarcopterygians, Latimeria (Crossopterygii:Latimeriidae) and Protopterus (Dipnoi: Lepidosirenidae), are cation-excreting glands in the anteriorwall of the cloacae (Lagiosand McCosker, 1977; M. Wake, 1986). These glands do not have an apparent homologue in amphibians or other fish, although anal-

ogous glands occur in Chondrichthyes(Lagios and McCosker, 1977). Female caecilians (Gymnophiona) lack cloacal glands, but in males, Mullerian glands, derived from terminal portions of the embryonic Mullerian ducts, open into the cloacae (M. Wake, 1981). Mullerian glands secrete a semen-like substance thought to provide for sperm nutrition, and these glands may be a primitive homologue of the mammalian prostate gland (M. Wake, 1981, 1982). The cloacal glands in male salamanders arise from outpocketings of the cloacal walls (Beaumont, 1933), and thus are not homologous in development to the caecilian glands. In Anura,Van Dijk (1959) described "proctodeal glands," which are acinar glands that originate from the epidermal lining of the cloacal orifice in male and female Ascaphus and Leiopelma (Leiopelmatidae), in which the cloacae are relatively specialized for anurans. Such

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glands were not noted in the more generalized cloacae of Bufo, Bombina, Rana, and Xenopus (Van Dijk, 1959), so the cloacal glands in leioplematids may be independently derived. Lissamphibiaand each of its three living orders are hypothesized to be monophyletic groups (Milner, 1988). The order Caudata consists of three extant suborders split into nine families, some 62 genera, and approximately 360 species (Frost, 1985). To date, no one has attempted a comprehensive review of the comparative anatomy and phylogeny of the cloacae of salamanders.In a series of papers, I couple an analysis of the literature with the examination of additional species to provide a comprehensive review of comparative cloacal structure in salamanders. This research is based upon anatomical data gathered from 128 species, with 87 species examined for the first time. In the current paper, an overview of cloacal evolution at the family level is presented. Subsequent papers will provide detailed anatomical descriptions and analyses for each family.

[Vol. 47, No. 2

with hematoxylin-eosin (for general cytology), and for many species, additional sections were stained or treated with

Mallory's triple stain (connective tissue), mercuric bromphenol blue or the ninhydrin-Schiff reaction/fast green (proteins), periodic acid-Schiff's reagent/fast green FCF (general carbohydrates), alcian blue/ nuclear fast red at pH 2.5 or toluidine blue (acid mucopolysaccharides), and/or osmium tetroxide (lipids). Staining procedures followed Humason (1979). Three-dimensional reconstructions of cloacae were performed on some species using PC3D software (Jandel Scientific, Corte Madera, California) and a Jandel digitizing tablet with a Zenith ZF-248 microcomputer. Depending on the species, every fourth to fifteenth section was digitized for image reconstruction. Right lateral views were reconstructed by computer software, with the sections rotated 250 clockwise. The cloacal displays were stretched appropriately in the anteriorposterior direction to help alleviate geometric distortions caused by skipping sections between each one digitized. Also, each MATERIALS AND METHODS digitized section of the cloacal glands that Literature sources for anatomical de- was emphasized was repeated 2-3 times scriptions of salamander cloacae and a list so that gaps between displayed sections of species utilized are given in Table 1. were more nearly closed. Finally, alternate Data for species examined for the firsttime digitized sections of the cloacal walls were or to supplement literaturedescriptionsare displayed in order to improve clarity. given in Appendix I. In all cases, snoutSever (1986) used a ratio of the cloacal vent length (SVL) refers to the distance tube length divided by total cloacal length from the tip of the snout to the posterior (CTL/TCL) to express the relative size of edge of the vent. Cloacal anatomy for each the cloacal tube. The cloacal tube is cylinspecies was examined following histolog- drical and extends caudally to the cavity ical preparation of the cloacae for light dorsal to the vent, the cloacal chamber microscopy. Specimens, as far as known, (Sever, 1978a). To determine lengths, the were initially preserved in 10% formalin, number of transverse sections of the cloand some were stored in isopropanol or acal tube and cloacal chamber were countethanol of varying concentrations before ed. The most anterior section of the cloacal histological preparation. Although this is tube was considered the one immediately not the best means of fixing and storing posterior to the junction of the Wolffian tissue for light microscopy, this is the status ducts with the hindgut. of older museum specimens. Phylogenetic analyses were conducted Following dehydration in ethanol, spec- with the branch-and-bound algorithms that imens were cleared in toluene or Histosol will find all equally most parsimonious trees (National Diagnostics, Inc., Manville, New using the following software for IBM-comJersey), embedded in paraffin and 10J,m patible microcomputers (specific algosections cut with a rotarymicrotome. Some rithm in parentheses): PAUP (Global sections from each species were stained Swapping; Mulpars) version 2.4 (Swofford,


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167

in the literature or examination of additional specimens (indicated by an ,X") 1.-Descriptions forming the basis of this study. Collection and locality data for the specimens used for the first time in this report are given in Appendix I.

TABLE

Taxon

Males

Females

Ambystomatidae

Ambystoma annulatum A. jeffersonianum A. gracile A. laterale A. maculatum A. opacum

X Sever (1988a)

X

X

Sever (1988a) Sever et al. (1989) Kingsbury (1895) Sever (1988a) Noble and Brady (1933) Sever (1988a)

X

A. platineum A. A. A. A.

talpoideum texanum tigrinum tremblayi

Kingsbury (1895) X X

X Sever (1988a) Sever (1988a) Sever (1981)

X X X Sever (1987) x

Amphiumidae

Amphiuma means

X

A. pholeter A. tridactylum

X Wilson (1941) X

Sever (1987) Kreeger (1942) Sever (1987)

X

Sever (1987)

Cryptobranchidae

Cryptobranchusalleganiensis Dicamptodontidae: Dicamptodontinae

Dicamptodon aterrimus D. copei D. tenebrosus Dicamptondontidae: Rhyacotritoninae Rhyacotriton olympicus

X Sever (1988a) Sever (1988a)

X X

Sever (1988a)

Sever (1987) x

Chang (1936)

X

Hynobiidae

Batrachuperuspinchonii

x

B. tibetanus Hynobius leechii

X X

X X

H. stejnegeri H. tsuensis

X X

Sever (1987) Sever (1987)

Onychodactylus japonicus

X

X

Sever (1983) Sever (1983) Sever (1983) Kingsbury (1895) Sever (1983) Sever (1983) Sever (1983) Noble and Pope (1929) Sever (1983) Sever and Houck (1985) Sever (1983) Sever (1983) Sever (1983) Sever (1983) Sever (1983) Sever (1983)

Sever and Trauth (1990) Sever and Trauth (1990) Sever and Trauth (1990) Kingsbury (1895) Sever and Trauth (1990) Sever and Trauth (1990) Sever and Trauth (1990) Noble and Pope (1929) Sever and Houck (1985) Sever and Trauth (1990) Sever and Trauth (1990) Sever and Trauth (1990) Sever and Trauth (1990) Sever and Trauth (1990) Sever and Trauth (1990) Sever and Trauth (1990)

Plethodontidae: Desmognathinae Desmognathus aeneus D. auriculatus D. brimleyorum D. fuscus D. imitator D. monticola D. ochrophaeus D. quadramaculatus D. santeetlah D. welteri D. wrighti Leurognathus marmoratus Phaeognathus hubrichti


168

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HERPETOLOGICA TABLE 1.-Continued. Taxon

Plethodontidae: Bolitoglossini Batrachoseps attenuatus B. major B. wrighti Bolitoglossa adspersa B. franklini B. platydactyla B. rufescens B. subpalmata

Males

X X X X X X X X

Females

Sever Sever Sever Sever Sever Sever Sever Sever

et et et et et et et et

al. al. al. al. al. al. al. al.

(1990a) (1990a) (1990a) (1990a) (1990a) (1990a) (1990a) (1990a)

Chiropterotritonchiropterus

X

Sever et al. (1990a)

C. multidentatus Dendrotriton bromeliacia Hydromantes italicus H. shastae Lineatriton lineola Nototriton picadoi Oedipina poelzi Pseudoeurycea belli P. goebeli

X X _t X X

Sever Sever Sever Sever Sever Sever Sever Sever Sever

P. leprosa

X

P. rex Thorius macdougalli

X X

Sever et al. (1990a) Sever et al. (1990a)

Kingsbury (1895) Sever (1980) Sever (1980, 1981) Sever (1980) Williams et al. (1985) Williams et al. (1985) Sever (1980) Sever (1985) Sever (1985) Sever (1980) Sever (1980) Sever (1980) Sever (1985)

Kingsbury (1895) Kohering (1925) Sever (1988b)

X X

et et et et et et et et et

al. al. al. al. al. al. al. al. al.

(1990a) (1990a) (1990a) (1990a) (1990a) (1990a) (1990a) (1990a) (1990a)

Plethodontidae: Hemidactyliini

Eurycea bislineata E. cirrigera E. junaluska E. longicauda E. lucifuga

E. multiplicata E. nana E. neotenes E. quadridigitata E. tynerensis E. wilderae Typhlomolge rathbuni

Hemidactylium scutatum Gyrinophilus palleucus G. porphyriticus Pseudotriton montanus P. ruber Stereochilus marginatus Typhlotriton spelaeus

X Sever Sever Sever Sever Sever

Sever (1985) Sever (1985) Trauth (1983) Sever (1985)

Sever (1987) (1986) (1986) (1986) (1986) (1986)

X

Sever Sever Sever Sever Sever

(1986) (1986) (1986) (1986) (1986) Sever (1987)

Plethodontidae: Plethodontini

Aneides aeneus A. ferreus A. lugubris Ensatina eschscholtzi Pethodon cinereus

X X X X

X X X X

Sever (1978a)

Kingsbury (1895)

X P. dorsalis

Sever (1978a) x

P. elongatus P. glutinosus

X X

P. jordani

X

P. larselli

P. ouachitae P. richmondi P. serratus

X X X

Sever (1978b) Sever (1978b)

X Trauth (1984) x

X Davitt and Larsen (1988)

X X X


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169

TABLE 1.-Continued. Taxon

P. teyahalee P. vehiculum P. websteri P. wehrlei P. yonahlossee

Males

Females

X X X X X

X X X X X

Necturus beyeri N. lewisi

X

Sever (1987)

X

X

N. maculosus

Dawson (1922) x

Kingsbury (1895) x

N. punctatus Proteus anguinus

X X

X

Salamandridae Chioglossa lusitanica

X

Wahlert (1953) x Wahlert (1953)

X X X

X X X

E. asper E. montanus

X

X X

Mertensiella luschani

X

Wahlert (1953) x Wahlert (1953)

Notophthalmus perstriatus

X

X

N. viridescens

Kingsbury (1895) Sever (1981)

Kingsbury (1895) Wahlert (1953) Dent (1970) Hardy and Dent (1986) x

Pachytriton brevipes Paramesotriton chinensis P. hongkongensis

X X X

X X X

Pleurodeles waltl

Lemaitre-Lutz (1968) X

Salamandra species

Zeller (1905)

Wahlert (1953) Lemaitre-Lutz (1986) x Wahlert (1953)

S. atra S. salamandra

X X

X X

Salamandrina terdigitata Taricha species

Brizzi et al. (1986)

Brizzi et al. (1989) Wahlert (1953)

T. rivularis T. torosa Triturus

X X

Proteidae

Cynops species

C. orientalis C. pyrrhogaster C. wolterstorffi Euproctus species

Wahlert (1953)

Neuregus crocatus

T. alpestris

Zeller (1905) Heidenhain (1890) x

X Wahlert (1953) X

X

X X

T. helveticus T. vulgaris

Heidenhain (1890) Sacerdote (1958) Fasolo and Grosso (1969) x Heidenhain (1890) Sever et al. (1990b)

Tylototriton verrucosus

X

X

T. boscai T. cristatus

Verrell and Sever (1988)

Sirenidae

Pseudobranchusstriatus

X

Sever (1987)

Siren intermedia S. lacertina

X X

Sever (1987) Vaillant (1863)


170

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1985), PHYLIP (Penny) version 2.8 (Felsenstein, 1986), and Hennig86 (bb option) version 1.5 (Farris, 1988). Characterswere weighted evenly. Other Lissamphibiawere used to determine ancestral states for the Caudata, and cladograms were rooted to a hypothetical ancestor that was plesiomorphic for all characters (Watrous and Wheeler, 1981). To resolve some polarities at the family level, characterswere mapped on published phylogenies using the methodology of Platnick (1977) and Maddison et al. (1984). Consensus trees were constructed using the CONTREE program supplied with PAUP and the nelsen option provided in Hennig86.

[Vol. 47, No. 2

2). The autapomorphies,of course, cannot help resolve character evolution among families. When the polymorphic characters are coded as such for phylogenetic analyses using PHYLIP, 93 equally parsimonious cladograms (requiring 51 steps) are produced using the Penny algorithm that finds all possible trees of minimum length. Resolution of the polymorphisms, therefore, is necessary to limit the number of topologies such a "messy" data set creates. The ancestralstate of characterP cannot be resolved for Salamandridae, but resolution of polymorphisms for the other charactersleads to a matrix in which characters D, G, N, V, and X are autapomorphic at the family level, and charactersA, RESULTS B, F, I, J, K, and Y show no change in any Cloacal Characters family from the ancestralcondition (Table Character states and their polarities are 2). This leaves 12 characters, C, E, H, L, considered separately for each sex. Cloacal M, 0, Q, R, S, T, U, and W, useful for evolution in males and females of a species phylogenetic analysis. Below, the 25 charcould be subject, in part, to different se- acters and their resolutions are discussed. lective pressures,and the patterns of variCharacters A-K: Anatomy of ation between male and female pairs may Cloacal Linings be disparate in a lineage (Sever, 1986). Thus, male salamanders in the family CharactersA-B: CTL/TCL quotient in Plethodontidae possessciliated epithelium females (A) and males (B).-Van Dijk in the cloaca (the ancestral state) while (1959) recognized a three-part cloaca in female plethodontids lack cilia in the clo- anurans, using the terminology developed aca (the derived condition). Thus, any ho- by Gadow (1887) for amniotes. The ar.mology between male and female cloacal uran urodaeum and coprodaeum are anstructures, including cloacal glands, is a terior tubular portions, and the proctomoot point in determining character po- daeum is the area surrounding the more larities. posterior cloacal orifice. From Van Dijk's In the family Dicamptodontidae, the (1959) work, it is apparent that the cloaca monotypic subfamily Rhyacotritoninae in anuransis largely tubular,and a "cloacal (containing Rhyacotrition olympicus) is chamber," as defined for urodeles, does coded separately from the subfamily Di- not exist. From M. Wake's (1972) work on camptodontinae (Dicamptodon aterri- caecilians, it is apparent that gymnomus, D. copei, D. ensatus, and D. tene- phiones have a well-defined cylindrical brosus). No clear evidence exists for portion of the cloaca anteriorto the cloacal monophyly of the family, and recent work orifice. Thus, I infer that the ancestralconsuggests that Rhyacotriton and Dicamp- dition is the presence of a definite cloacal todon are not closest relatives (Duellman tube. and Trueb, 1986; Good et al., 1987; Milner, Following Sever et al. (1990a), coding 1983). for this character indicates whether or not Twenty-five characters, A-Y, are rec- a discrete cloacal tube exists, and CTL/ ognized (Table 2). All but seven (H, M, N, TCL = 0.05 was used to partition the anQ, S, T, X) are polymorphic within one or cestral state, presence of a definitive clomore families and five are autapomorphies acal tube (CTL/TCL > 0.05) from the (I, N, V, X, Y) at the family level (Table derived condition, lack of definite cloacal


2.-Character polarities for cloacal characters in salamanders. Characters A-Y are defined in the Results sec "O", the derived condition by "1", "B" indicates polymorphisms (both ancestral and derived character states occur the ancestral state cannot be resolved. Following resolution of polymorphisms, characters C, E, H, L, M, 0, Q, R, S, T analyses shown in Fig. 7. TABLE

Characters Taxon

A

With polymorphisms included 0 Ancestor Ambystomatidae B 0 Amphiumidae 0 Cryptobranchidae 0 Dicamptodontinae 0 Rhyacotritoninae 0 Hynobiidae Plethodontidae B Proteidae O Salamandridae B Sirenidae B With polymorphisms resolved 0 Ambystomatidae 0 Amphiumidae 0 Cryptobranchidae 0 Dicamptodontinae 0 Rhyacotritoninae 0 Hynobiidae 0 Plethodontidae 0 Proteidae 0 Salamandridae Sirenidae 0

B

C

D

E

F

G

H

I

I

K

L

M

N

0

p

Q

0 0 0 0 0 0 B B 0 0 0

0 0 0 0 0 1 0 1 1 B 1

0 0 0 0 0 0 B B 0 0 1

0 0 B 0 0 1 B 1 1 B 1

0 0 0 0 0 0 0 B 0 0 0

0 0 0 0 B 0 0 B 1 0 0

0 1 0 0 1 1 0 0 0 0 0

0 0 0 0 0 0 0 B 0 0 0

0 0 0 0 0 0 0 B 0 0 0

0 0 0 0 0 0 0 0 0 B 0

0 1 0 1 1 0 1 B 1 B 0

0 1 1 0 1 1 0 1 1 1 0

0 0 0 0 0 0 0 1 0 0 0

0 1 0 0 0 0 0 B 0 0 0

0 0 1 0 0 0 0 0 0 B 0

0 1 1 1 1 1 1 1 1 1 0

0 0 0 0 0 0 0 0 0 0

0 0 0 0 1 0 1 1 0 1

0 0 0 0 0 0 0 0 0 1

0 0 0 0 1 1 1 1 0 1

0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 1 0 0

1 0 0 1 1 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0

0 0 0 0 0 0 0 0 0 0

1 0 1 1 0 1 1 1 1 0

1 1 0 1 1 0 1 1 1 0

0 0 0 0 0 0 1 0 0 0

1 0 0 0 0 0 1 0 0 0

0 1 0 0 0 0 0 0 ? 0

1 1 1 1 1 1 1 1 1 0


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tube (CTL/TCL < 0.05). This division negates analysis at this time of the considerable variation that occurs among salamanders in the CTL/TCL range of 0.060.96. Except in Amphiumidae, Cryptobranchidae, and Hynobiidae, the CTL/TCL quotient is generally larger in males than females. Among males, the quotient varies from 0 (Leurognathus, Pseudotriton) to 0.69 (Necturus). In females, the quotient ranges from 0 (many genera) to 0.49 (Amphiuma), except for Euproctus, in which the cloacal tubes are highly specialized, and CTL/TCL = 0.64 in Euproctus montanus and 0.96 in E. asper. Considerable homoplasy occurs in this character, as resolution at the family level infers the ancestral condition of CTL/TCL > 0.05 for both sexes in each family. Resolution of polymorphisms.-In the Sirenidae, the urogenital ducts open directly into the cloacal chamber in one female Siren intermedia, indicating the derived condition, while another individual sectioned possesses a well-formed cloacal tube, although the sections for the latter specimen are not complete enough to calculate the CTL/TCL ratio. In a female Pseudobranchus striatus, however, the cloacal tube is longer than the cloacal chamber, and CTL/TCL = 0.62. Male sirenids have relatively long cloacal tubes, with CTL/TCL = 0.33 in S. intermedia and 0.40 in P. striatus. I infer that both sexes of sirenids should be coded for the ancestral condition, but further data on this character in sirenids would be welcome. In the Hynobiidae, the derived condition occurs in male Batrachuperus tibetanus and Hynobius leechii but not male B. pinchonii, H. steinegeri, H. tsuensis, or Onychodactylus japonicus. Thus, based upon data currently available, homoplasy is apparent for the character in Batrachuperus and Hynobius, and the ancestral condition is most parsimoniousfor the Hynobiidae as a whole. In the Salamandridae, the derived condition is found only in female Pleurodeles waltl, and in the Ambystomatidae, only in female A. annulatum, indicating an independently evolved

[Vol. 47, No. 2

character within each of these two families. In the Plethodontidae, all males in species of the subfamily Plethodontinae possess the ancestral condition, and among males in the Desmognathinae, the derived condition is found only in Leurognathus marmoratus (Sever, 1983). Among female plethodontids, only in the tribe Plethodontini do all species possess the ancestral condition. In the tribe Hemidactyliini, the derived condition occurs in female Gyrinophilus porphyriticus, Pseudotriton ruber, and Typhlomolge rathbuni, but not in the other eight species examined. In the Bolitoglossini,the derived condition occurs in Bolitoglossa, Dendrotriton, Oedipina, and Thorius, and Sever et al. (1990a) considered this homoplasy. Within the Desmognathinae, female Desmognathus quadramaculatus, Leurognathus marmoratus, and Phaeognathus hubrichti possess the derived condition, but the remaining 10 species that have been examined possess the ancestral state (Sever and Trauth, 1990). Mapping this character using the method of Platnick (1977) on the phylogeny of plethodontid genera from Larson (1984) combined with the phylogeny of salamander families from Duellman and Trueb (1986), I infer the ancestral condition for the Plethodontidae is CTL/ TCL > 0.05. Thus, homoplasy in this character is prevalent in female plethodontids. CharactersC-D: Ciliated epithelium in the cloacal tube and/or anterior cloacal chamber of females (C) and males (D).Duellman and Trueb (1986) stated that the cloacal mucosa of amphibians is ciliated. Based upon this, I consider the ancestral condition in both sexes is presence of cilia (Fig. IA), and absence of cilia is derived. I am unaware, however, of any primary literature describing cilia in the cloacae of anurans. Also, M. Wake (1972) reported cilia in the cloacae of male caecilians but not of females. Reproductive condition must be considered when checking for this character, for Sever (1980) and Brizzi et al. (1989) have noted some species in which cloacal cilia are apparent only during the breeding season. Resolution of polymorphisms.-The


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only hynobiid of either sex in which cilia are lacking is male Onychodactylus japonicus, so this is considered an independent loss in males of that species. In female Salamandridae,cilia occur in Mertensiella luschani and Pleurodeles waltl, and Brizzi et al. (1989) reported the occurrence of cilia in female Salamandrina terdigitata. Although I did not find cilia in females from the other nine genera examined, these remaining genera, with the exception of Tylototriton, form a monophyletic unit that is more apomorphic than clades involving Mertensiella-Salamandrina and Pleurodeles (D. Wake and Ozeti, 1969). Thus, I infer that the ancestral condition in female salamandrids is presence of cilia. Cilia have been reported from females of two species of plethodontids, Eurycea quadridigitata (Pool and Hoage, 1973; Trauth, 1983) and Plethodon glutinosus (Kingsbury,1895; Trauth, 1984), but I have never found cilia in these or other female plethodontids. If cilia do occur in some female plethodontids, I view this as a reversal to the plesiomorphic state for salamanders. In male plethodontids, I found cilia lacking in male Bolitoglossa and Lineatriton; because cilia occur in male specimens of every other plethodontid examined, this loss must be secondary. Character E: The extent of epidermis in the female cloacal chamber.-The pseudostratifiedepithelium of the anterior cloacal tube gradually grades into an epidermal lining (stratified cuboidal epithelium with a superficial cornified layer) in the cloacal chamber. Duellman and Trueb (1986) stated that the lining of the amphibian cloaca is simple columnar epithelium. Van Dijk (1959) reported that the proctodaeum of anurans is lined with epidermis, and that the junction with the coprodaeum and urodaeum is marked by transitional epithelium. In male salamanders, except for some hynobiids, the extent of epidermis into the cloacal chamber is restricted to the medial lips of the cloacal orifice. Therefore, I infer that the ancestral condition in female salamandersis that the epidermal lining does not extend into the anterior one-half of the cloacal chamber,

173

and the derived condition is that the epidermal lining does extend into the anterior one-half of the cloacal chamber (Fig. 1B,C). Resolution of polymorphisms.-In the Amphiumidae, the exception to the ancestral condition, as seen in A. means and A. tridactylum, is Amphiuma pholeter, a specialized species in which selection for miniaturization and a switch from an aquatic to a fossoriallifestyle has occurred. In the Salamandridae, only female Euproctus possess the derived condition, but these species have specialized, elongate cloacal tubes and relatively short cloacal chambers (see character A). Thus, the character coding for these two families is possessionof the ancestral state. Character F: Cloacal recess in females.-A cloacal recess is an anterior extension of the female cloacal chamber dorsal to the posterior end of the cloacal tube (Sever, 1978b). Such structures have not been reported in female anurans,in which a definite cloacal chamber does not exist (see charactersA,B). The cloacae of female caecilians possesscharacteristicridges, but "blind sacs"do not occur (M. Wake, 1972). Thus, the ancestral condition in urodeles is absence of a recess, derived is presence of a recess. This character occurs only in the Plethodontidae. Resolution of polymorphisms.-Cloacal recesses occur only in Phaeognathus hubrichti of the Desmognathinae; Batrachoseps pacificus, Hydromantes italicus, and Thorius macdougalli of the Bolitoglossini; Gyrinophilus porphyriticus and Stereochilus marginatus of the Hemidactyliini; and eastern small and large species of Plethodon. I infer that a cloacal recess has evolved independently in a number of plethodontid lineages, and that the ancestral condition for the family as a whole is absence of a cloacal recess. Character G: Number of pairs of rugae in the male cloaca.-Transverse sections through the cloacae of male anuransshow 4-5 pairs of rugae (Van Dijk, 1959). No data exist for caecilians. The cloacae of male caecilians have muscular ridges associated with eversion of the cloaca, and these may be confused with rugae of con-


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174

Cc

D

E~~~~~~~~E

FIG. 1. Characters associated with the anatomy of the cloacal cavities in salamanders. Transverse sections stained in hematoxylin-eosin except (F) was stained with PAS-fast green. (A) Ciliated mucosa in the cloacal tube of a female Hynobius tsuensis (specimen from Sever, 1987). Scale bar = 10,um. (B) Same specimen as (A), showing epidermal lining of the cloacal chamber. Scale bar = 50 ,um. (C) Epithelial linings in the posterior cloacal chamber of a female Triturus boscai (BMNH 1973.3470). The epidermal lining does not cover the dorsal walls of the chamber. Scale bar = 50 ,um. (D) Primary and secondary folds of the cloacal tube in a male Ambystoma opacum (specimen from Sever, 1988a). Scale bar = 200 ,m. (E) Same as (D), in a male Dicamptodon tenebrosus (specimen from Sever, 1988a). Scale bar = 200,um. (F) Same as (D), in a male Rhyacotriton olympicus (specimen from Sever, 1988a). Scale bar = 100 tm. Av = anterior ventral gland; Cc = cloacal chamber; Ce = ciliated epithelium; Cm = cloacal mucosa; Dp = dorsal pelvic gland; Ep = epidermis; Kg = Kingsbury's gland; Lp = lateral pelvic gland; Pf = primary folds; and Sf = secondary folds.

nective tissue without contractile properties (M. Wake, 1972). For salamanders, coding is meant to indicate extreme folding of the cloacal wall, which is surely derived. Therefore, the ancestral condition is < 10, derived is > 10 pairs of rugae. the Resolution of polymorphisms.-In Dicamptodontinae, two specimens of D. tenebrosus possess 12 pairs of rugae each,

and two D. copei possess seven pairs of rugae each. Male Ambystomatidae, morphologically similar to dicamptodontids, have < 10 pairs of rugae. Thus, I infer that it is more likely that the number of rugae in D. tenebrosus is an independently derived feature, perhaps relating to the large body size of this species (122-148 mm SVL in specimens examined by Sever, 1988a).


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In the Plethodontinae, the derived character is found in the eastern large Plethodon; because it does not occur in other plethodontids, the ancestral condition prevails for the family as a whole. Character H: Primary and secondary folds in the male cloacal tube.-These are conspicuous evaginations from the dorsolateral walls of the cloacal tube that serve as the site for secretion of Kingsbury's glands (primary folds) and lateral pelvic glands (secondary folds) in Ambystoma, Dicamptodon, and Rhyacotriton (Sever, 1981, 1988a). The folds are better developed in Ambystoma than in Dicamptodon or Rhyacotriton (Fig. 1D-F). The folds and associated glands are lacking in other Lissamphibia, so the ancestral condition is absence of primary and secondary folds, and their presence is derived. Character I: Middorsal evagination of the male cloacal chamber.-This character indicates the presence of a prominent middorsal depression of the roof of the cloacal chamber, in the form of a cone, that fills the dorsal one-half of the cavity. Based upon available data, this character is lacking in amphibians other than some Plethodontidae. Thus, I infer that the ancestral condition is absence of the cloacal chamber depression, and the derived condition is presence of the depression. Resolutionof polymorphisms.-The derived state is found in eastern Plethodon, except for members of the P. cinereus group, of the Plethodontini' and in Bolitoglossa of the Bolitoglossini. Homoplasy occurs with this character in Plethodon and Bolitoglossa, and the ancestral condition for the Plethodontidae as a whole is absence of a middorsal evagination of the male cloacal chamber. CharacterJ:Dorsolateralrecesses in the male cloacal chamber.-Again, this is a character found only in some plethodontids. Thus, the ancestral condition is absence of such recesses,and the derived condition is presence of dorsolateral recesses. Resolution of polymorphisms.-This characteris found in Desmognathus of the Desmognathinae and only in Chiropterotriton of the Bolitoglossini. Thus, homoplasy is likely in these two genera, and the

175

ancestral condition for the family as a whole is absence of the dorsolateralrecesses. Character K: Pseudopenis in the male cloaca.-The pseudopenis is an evagination from the dorsal wall of an anterior extension of the cloacal chamber, ventral to the posterior cloacal tube (Sever et al., 1990b). A pseudopenis is known only in certain male salamandrids. Thus, the ancestral condition in amphibians is lack of a pseudopenis, derived is presence of a pseudopenis. Resolution of polymorphisms.-A pseudopenis occurs in male Cynops, Euproctus, Pachytriton, Paramesotriton, Taricha, and Triturus. Following the phylogeny proposed by D. Wake and Ozeti (1969), this character is clearly derived within the Salamandridae,and the ancestral state for the family is absence of a pseudopenis. Clocal Glands As noted previously, the anatomy of exocrine glands secreting into the cloacae of sarcopterygianfish, anuransand male caecilians contraindicates homology with salamander cloacal glands. The ancestral condition for salamanders, therefore, is considered to be the absence of cloacal glands, and the presence of cloacal glands in all salamanders except Sirenidae is a derived condition. Characters L-P: Female Clocal Glands Character L: Female anterior ventral glands.-Anterior ventral glands secrete onto the epidermis lining the cloacal orifice and/or onto the ventrolateral walls of the cloacal chamber (Fig. 2). In most species, the region of the secretion is limited to the anterior portion of the cloacal orifice/chamber. Depending on species, these glands can be basophilic or eosinophilic in females. Resolution of polymorphisms.-In the Salamandridae,female ventral glands are absent in Chioglossa, Cynops, Paramesotriton, and Triturus, but are present in the other genera that are more basal according to the phylogeny of D. Wake and Ozeti (1969). Thus, I infer that the ancestralcon-


176

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Ct

E4~~~~

.1

~

~

A

"M I

~

~


177

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June 1991]

Ct

Dg 00

C

*

D~C

FIG. 3.-The dorsal gland in female salamanders. Transverse sections stained with hematoxylin-eosin are shown in (A) and (C), and scale bars = 100 ,um in (A) and 50 ,um in (C). Three-dimensional reconstructions of lateral views of the cloacae with the anterior end (towards the right) rotated 250 clockwise are illustrated in (B) and (D). (A), (B) Ambystoma opacum (UMMZ 187373). (B), (D) Typhlotriton spelaeus (specimen from Sever, 1987). Labels same as for Figs. 1 and 2 plus Dg = dorsal gland.

dition for the family Salamandridae is presence of female ventral glands. In the Plethodontidae, female ventral glands are lacking in some Desmognathus (Sever and Trauth, 1990), all Bolitoglossini examined except B. pacificus, Hydro-

mantes shastae, and Pseudoeurycea goebeli (Sever et al., 1990a), and in Aneides and all Plethodon examined except P.

ouachitae and P. vehiculum. Ventral

glands are found in all female Hemidactyliini that have been examined. Thus, female ventral glands are known in at least some species in each subfamily and tribe of Plethodontidae. Following Watrous and Wheeler (1981), the plesiomorphic state for plethodontids is the state occurring in related groups as determined by other characters. This criterion and mapping occurrence of ventral glands using the meth-

FIG. 2.-The anterior ventral gland in female salamanders. Transverse sections through the anterior cloacal chamber are shown in (A), (C), (E), and (G), and scale bars = 200 lim except (G) in which the scale bar = 100 Am. Sections were stained with hematoxylin-eosin except (G) was stained with mercuric bromphenol blue. Three-dimensional reconstructions of lateral views of the cloacae with the anterior end (towards the right) rotated 250 clockwise are illustrated in (B), (D), (F), and (H). (A) Batrachuperus pinchonii (FMNH 232844). (B) Hynobius tsuensis (specimen from Sever, 1987). (C), (D) Pleurodeles waltl (FMNH 84877). (E) Ambystoma gracile (UMMZ 133156.1). (F) A. opacum (UMMZ 187373). (G) Eurycea cirrigera (specimen from Sever, 1988b), (H) Typhlotriton spelaeus (specimen from Sever, 1987). Labels same as for Fig. 1 plus Ct = cloacal tube and St = spermathecae.


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Av

Kg

*

0Q

Av


tune 19911

HERPETOLOGICA

odology of Platnick (1977) on the phylogeny of salamander families provided by Duellman and Trueb (1986) indicate that the ancestral condition for the family Plethodontidae is presence of female ventral glands. Character M: Spermathecae. -Spermathecae are glands in which sperm are stored, usually found in the dorsal walls of the posterior cloacal tube and/or anterior cloacal chamber. In many species of salamandrids, amphiumids, and proteids, however, spermathecae also occur along the dorsolateral walls of all but the most posterior portion of the cloacal chamber. CharacterN: Common tube to the spermathecae.-This is an autapomorphy for the Plethodontidae, in which all of the spermathecae are joined by a single duct of pseudostratifiedor stratified epithelium to the dorsal wall of the cloacal tube or anterior cloacal chamber (Sever, 1987). Character 0: Female dorsal glands.These are glands that secrete into the dorsal walls of the cloaca, anteriorand/or posterior to the spermathecae or in the vicinity of the spermathecalcommon tube (Fig. 3). Female dorsal glands often appear rudimentary, especially in the Plethodontidae (Sever, 1987). Resolution of polymorphisms.-In the Desmognathinae, dorsalglands are lacking in D. aeneus and D. wrighti, and in some populations of other Desmognathus species (Sever and Trauth, 1990). In the Bolitoglossini, dorsal glands occur in Hydromantes italicus, Lineatriton lineola, and Pseudoeurycea goebeli (Sever et al., 1990a). In the Hemidactyliini, dorsal glands are present in all species except paedomorphic Eurycea and Typhlomolge rathbuni (Sever, 1980, 1987). In the Plethodontini, dorsal glands occur in Ensatina, Plethodon ouachitae, and P. yonahlossee. Thus, dorsal glands are known from all

179

subfamilies and tribes of the Plethodontidae. Using the same criteria for polarity determination by outgroup comparison employed for female anterior ventral glands (see Character L), I infer that the ancestral condition for the Plethodontidae is presence of dorsal glands. Character P: Other female cloacal glands.-The salamandrids Pleurodeles and Typhlotriton and female amphiumids have well-developed tubular glands secreting into the posterior angle of the cloaca, similar in some respectsto male dorsal or vent glands. Based upon available anatomical data, however, I cannot determine whether these glands in female salamandrids and amphiumids are homologous to one another. Resolution of polymorphisms.-In the Salamandridae,these glands occur only in Pleurodeles and Typhlotriton. Mapping this characterusing the method of Platnick (1977) on the phylogeny of salamandrids from D. Wake and Ozeti (1969) combined with the phylogeny of salamanderfamilies from Duellman and Trueb (1986), an ancestral state of presence of such glands could be inferred for the Salamandridae. These glands may be independently derived in salamandrids and amphiumids, however, and I feel that more anatomical data are necessary to support a hypothesis of homology. Thus, I believe that it is best to consider the origin of these glands in salamandridsas unresolved for the present and not use this character in phyletic analyses (Table 2). Characters Q-Y: Male Cloacal Glands Character Q: Male anterior ventral glands.-As in females, anterior ventral glands in males generally secrete onto the epidermis surrounding the cloacal orifice and/or onto the ventrolateral walls of the anterior cloacal chamber (Fig. 4). Male

FIG. 4. -The anterior ventral gland and Kingsbury's gland in male salamanders. Transverse sections through the cloacal tube stained with hematoxylin-eosin are shown in (A), (C), (E), and (G), and scale bars = 200,um except (G) in which the scale bar = 275 gm. Three-dimensional reconstructions of lateral views of the cloacae with the anterior end (towards the right) rotated 250 clockwise are illustrated in (B), (D), (F), and (H). (A) Hynobius leechii (FMNH 25248). (B) H. tsuensis (BMNH 1911.2.24.6). (C), (D) Pleurodeles waltl (FMNH 84879). (E), (F) Amphiuma pholeter (UF 62411). (G), (H) Necturus lewisi (NCSM 22338). Labels same as for Fig. 1.


*

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180

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June 1991]

HERPETOLOGICA

anterior ventral glands are generally basophilic except in some hynobiids. CharacterR: Posteriorventral glands. Generally, these are glands similar to anterior ventral glands but differing by having larger gland tubules, a lighter-staining secretory product, and by secreting into the posteriorone-half of the cloacal chamber (Fig. 5). Resolution of polymorphisms.-In the Salamandridae, definitive posterior ventral gland clusters are not found in Pachytriton and Tylototriton, two species that are not closely related within the family (D. Wake and Ozeti, 1969). The absence of posterior ventral glands in Pachytriton and Tylototriton therefore are considered independent reversals. In the Plethodontidae, posterior ventral glands are absent only in Typhlomolge rathbuni (Sever, 1985) and Pseudotriton montanus (Sever, 1986), certain reversalsto the ancestralstate as determined by outgroup analysis (Maddison et al., 1984; Platnick, 1977; Watrous and Wheeler, 1981). Character S: Kingsbury's glands. These form a small cluster of basophilic glands that secretes into the dorsal and dorsolateralwalls of the most anterior end of the cloaca (Fig. 4). Character T: Dorsal pelvic glands.These compose a group of glands, often containing eosinophilic globules in a matrix of basophilic granules, that secretes into the dorsalroof of the cloacal tube and/ or anterior cloacal chamber (Fig. 6). Distal ends generally pass anteriorly. Character U: Lateral pelvic glands.In some species, lateral pelvic glands exist that secrete into the dorsolateral walls of the cloaca between dorsalpelvic gland and anterior ventral gland clusters (Fig. 6). These glands have been called "dorsolateral pelvic glands"in plethodontids (Sever,

181

1980, 1981, 1983; Williams et al., 1985). As noted by Sever (1981) and Williams et al. (1985), lateral pelvic glands are distinguished from the dorsal pelvic glands by cytological features (more luminal globular material, staining intensities) and relationshipsto the cloacal chamber (usually lateral pelvic glands persist caudal to the dorsal pelvic glands). Resolution of polymorphisms.-In the Plethodontidae, lateral pelvic glands are absent in Phaeognathus hubrichti of the Desmognathinae (Sever, 1983) and in Pseudotriton ruber, P. montanus, and Typhlomolge rathbuni of the Hemidactyliini (Sever, 1985, 1986). Mapping this character on phylogenies of the Desmognathinae and Hemidactyliini (Larson, 1984; D. Wake, 1966) indicates that these absences are likely reversals.Thus, the ancestral state for plethodontids is possession of lateral pelvic glands. Character V: Caudal pelvic glands.An autapomorphy for plethodontids, caudal pelvic glands secrete into the dorsal roof of the cloacal chamber posterior to the dorsal pelvic glands (Sever, 1978a, 1980, 1981; Fig. 6G). Distal ends of caudal pelvic glands generally pass posteriorly. Often, the luminal secretion lacks the basophilic component found in dorsal pelvic glands. Resolution of polymorphisms. -All plethodontids that have been examined possess a caudal pelvic gland except for Phaeognathus hubrichti (Sever, 1983). Reversal is the most parsimonious explanation for absence of this gland in P. hubrichti. Character W: Male dorsal or vent glands.-The name vent gland is used for all families except Salamandridae,in which the name "dorsal gland" or "abdominal" gland has enjoyed long usage. The inap-

FIG. 5.-The dorsal gland, vent gland, and posterior ventral gland in male salamanders. Transverse sections stained with hematoxylin-eosin are shown in (A), (C), (E), and (G), and scale bars = 200 ,tm except (G) in which the scale bar = 150 ,um. Sections are through the posterior cloacal chamber except (E) which is through the anterior end of the cloacal chamber. Three-dimensional reconstructions of lateral views of the cloacae with the anterior end (towards the right) rotated 25? clockwise are illustrated in (B), (D), (F), and (H). (A), (B) Pleurodeles waltl (FMNH 84879). (C), (D) Amphiuma pholeter (UF 62411). (E), (F) Necturus lewisi (NCSM 22338). (G), (H) Hemidactylium scutatum (DMS 3983). Labels same as for Fig. 3 plus Pi = pit gland and Pv = posterior ventral gland.


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B

U...."t

fr5

9t'tL

fol~~~~~~


June 1991]

HERPETOLOGICA

propriate nature of the term "abdominal gland" for this structure was discussed by Sever et al. (1990b) and Wahlert (1953). The name "dorsal gland" is retained for male salamandrids, but the dorsal glands in male salamandrids are homologous to the vent glands in other male salamanders and not to female "dorsal glands," which are found only in ambystomatidsand some salamandrids(see above, character0). Male dorsal and vent glands show considerable variation. These are eosinophilic glands that secrete into the cloacal orifice, with the secretion site limited to the caudal angle of the vent in most species. In Rhyacotriton, however, vent glands secrete onto skin lobes dorsolateral to the caudal angle of the vent. The glands are often restricted to the posterior portion of the cloaca, although in some salamandrids, distal ends of dorsal glands may pass anteriorly to lie cranial of the pelvic girdle. Resolution of polymorphisms.-Vent glands are lacking in the hemidactyliines Eurycea tynerensis (Sever, 1980) and Typhlomolge rathbuni (Sever, 1985), and reversalsare the most parsimoniousexplanation for this condition. Character X: Amphiumid pit glands. An autapomorphy for male Amphiumidae, the pit glands are eosinophilic glands in the dorsal and lateral walls of the posterior cloacal chamber, occupying the area where posterior ventral glands (lacking in amphiumids) are found in many other species (Fig. 5). Character Y: Other male cloacal glands.-Onychodactylus japonicus possesses three distinct glands clusters. One of these secretes onto the epidermis lining the cloacal orifice and can be homologized with the anterior ventral glands. The other two glands do not have a structuralhomologue in other salamanders.These glands will be described in a future paper.

183

Phylogenetic Analyses As noted previously, 12 characters (C, E, H, L, M, 0, Q, R, S, T, U, and W) were found useful for phylogenetic analysis after resolving polymorphisms. With PHYLIP and PAUP, which do not account for trees with zero branch-lengths, the same 15 equally parsimonious cladograms are generated by the branch-and-bound algorithms. With Hennig86, which does account for zero branch-lengths,nine cladograms are generated. The cladograms all have 19 steps and a consistency index of 0.63. Two topologies, showing the variation in phylogenetic hypotheses, are illustrated in Fig. 7. Constant features of all cladogramsare (1) the sister-grouprelation between Sirenidaeand the remaining families, (2) the sister-group relation between Amphiumidae, Salamandridae, and other Salamandroidea, and (3) the sister-group relation between Ambystomatidaeand Dicamptodontidae. In all cladograms produced by the software used, convergence is hypothesized to account for C' in Sirenidae and in Proteidae + Plethodontidae + Rhyacotritoninae and for O' in Ambystomatidae and in Plethodontidae. Variation in cladograms generated is due entirely to characters E and H, and whether the occurrenceof these characters can be explained best by convergence (Fig. 7A) or reversal (Fig. 7B). In Fig. 7B, E' is the ancestral state for extant salamanders,and a reversalto E has occurred in the ancestor for all families except Sirenidae and Hynobiidae, with E' later re-evolving in Proteidae+Plethodontidae. Also, H' evolved in the ancestor to Ambystomatidae + Dicamptodontinae (Rhyacotritoninae(Plethodontidae + Proteidae)), and reversed to H in Plethodontidae+Proteidae (Fig. 7B). Obviously, other equally parsimonious cladograms are

FIG. 6.-The dorsal and lateral pelvic glands in male salamanders. Transverse sections stained with hematoxylin-eosin are shown in (A), (C), (E), and (G), and scale bars = 200 gm except (G) in which the scale bar = 150 ,um. Sections are through the anterior end of the cloacal chamber except (F) which is through the middle cloacal tube. Three-dimensional reconstructions of lateral views of the cloacae with the anterior end (towards the right) rotated 250 clockwise are illustrated in (B), (D), (F) and (H). (A), (B) Pleurodeles waltl (FMNH 84879). (C), (D) Amphiuma pholeter (UF 62411). (E), (F) Necturus lewisi (NCSM 22338). (G), (H) Hemidactylium scutatum (DMS 3983). Labels same as for Fig. 1 plus Cp = caudal pelvic gland.


8

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characters in salamanders.Each cladogram has 19 steps and a consistency index of 0.63. Charactersare taken from Table 2. An "X" indicates a reversal to the ancestralstate, and a prime sign (') indicates the derived state. Equally parsimoniouscladogramsdiffered in the frequency of convergence or reversalin charactersE and H. (A) Cladogramshowing the most convergence and least reversalsin characterstatesof any cladogramgenerated. (B) Alternativecladogram, which contains the most reversalsand least convergence.

possible in which the reversal of E occurs, but not H, and vice-versa.

If E' is convergent in Sirenidae and Hy-

nobiidae, then Hynobiidae and Cryptobranchidae are sister-groups,and together they form the sister-group for the Salamandroidea (Fig. 7A). If E' is reversed in the ancestor to Cryptobranchidae, then Hynobiidae

is the sister-group

for all fam-

ilies except Sirenidae (Fig. 71B). If H' is convergent in Ambystomatidae and in Rhyacotriton+Dicamptodontinae inae, then Proteidae + Plethodontidae

+pRhyacotritoninae form a trichotomy that

is the sister-group of Ambystomatidae+ Dicamptodontinae (Fig. 7A). If H' is found in their ancestor but reversed in Plethodontidae+Proteidae, Rhyacotritoninae is the sister-taxonto Proteidae+Plethodontidae as well as Ambystomatidae+Dicamptodontinae (Fig. 7B). Consensus Trees A strict (Nelson) consensus tree (Funk and Brooks, 1990) was generated based upon the nine cladograms produced by Hennig86. This consensus tree (Fig. 8A) is not identical to any of the inputted cladograms and shows two differences from the tree showing the least reversals (Fig. 7A). One difference is that Fig. 7A shows Ambystomatidae+Dicamptodontinae as the sister-group to Rhyacotritoninae+ Plethodontidae+Proteidae while the consensus tree shows a trichotomous relationship among Ambystomatidae, Dicamptodontinae, and Rhyacotritoninae + Plethodontidae+Proteidae. The other difference is that in Fig. 7A, the ancestor to Cryptobranchidae+ Hynobiidae is the sistertaxon of the Salamandroideawhile in Fig. 8A, a trichotomy exists among Cryptobranchidae, Hynobiidae, and the ancestor to the Salamandroidea. Another strict consensus tree was obtained using the consensus tree from the cloacal data (Fig. 8A) and cladogramsfrom Duellman and Trueb (1986), Hecht and Edwards (1977), and Milner (1983). The results (Fig. 8B) again are not identical with any of the inputted topologies. A common element of all of the inputted cladograms, which, of course, is present in the consensustree, is the monophyly of the Salamandroidea. This consensus tree also affirms, however, that problems still exist in resolving the relationships of families within the Salamandroidea (Fig. 8B). DISCUSSION

Characters involving cloacal anatomy have been used in previous parsimony analyses of character evolution in salamanders. Hecht and Edwards (1977) and Duellman and Trueb (1986) used type of fertilization as a character, with the ancestral condition being external fertiliza-


June 1991]

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tion. Milner (1983) used the number and types of cloacal glands (absent, one type, three types) as characters. Other characters used by these authors involved osteology, skeletal muscles, spinal nerves, and chromosome data. Larson and Wilson (1989) used patternsof ribosomalRNA and morphological data from Duellman and Trueb (1986) to construct a phylogenetic hypothesis, but only seven families of salamanderswere represented.Duellman and Trueb (1986) noted that Milner (1983) misinterpreted polarities of some characters in his analyses. I cannot passjudgement on the accuracy of assessment of non-cloacal characters in any of the published phylogenies mentioned above. I leave that to others who are expert on such characters. My data, however, are now available for incorporation into new phylogenies as differences of interpretation of polarities of non-cloacal characters are resolved. My results, however, are of interest in comparison to past phylogenetic hypotheses based primarily on non-cloacal characters. The cloacal data support the arrangement of extant salamander families into the three suborders provisionally recognized by Duellman and Trueb (1986). The suborderSirenoideacontains only the family Sirenidae which is composed of three paedomorphic species in the genera Siren and Pseudobranchus in the southeastern United States. These amphibians were placed in their own order (Trachystoma) by Goin and Goin (1962). Although ordinal status has not been generally accepted, the species of Sirenidae variously have been considered early offshoots from the urodelan lineage, one of the most derived salamander families, or not even salamanders at all (Estes, 1981; Hecht and Edwards, 1977). Mostrecent workers,however, place sirenids near the base of salamander phylogeny, which is supported by my results. The suborder Cryptobranchoidea consists of the families Cryptobranchidaeand Hynobiidae. The extant members of the Cryptobranchidae are aquatic paedomorphs and consist of Andrias, with two species in Japan and central China, and Cryptobranchus, with one species in the

185

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0 Z 0 (0

0~~~~ OR~

B FIG. 8. -Strict consensus trees. (A) Consensus tree derived from the nine equally parsimonious cladograms for cloacal data found by Hennig86. (B) Consensus tree based upon that in (A) and cladograms published by Duellman and Trueb (1986), Hecht and Edwards (1977), and Milner (1983).

Appalachian/Ozarkian highlands of eastern United States. The Hynobiidae consist of 33 species in nine genera that occur in Asia. Hynobius with 17 species and Batrachuperus with six species are the largest genera. Virtually all salamander systematists have agreed that the Hynobiidae has many plesiomorphic morphological features, and that differences with cryptobranchids are largely due to paedomorphosis in the latter group (Duellman and Trueb, 1986; Estes, 1981; Hecht and Edwards, 1977; Milner, 1983). The consensus analysis for cloacal characterssupportsthe close relationshipof the Cryptobranchidae and Hynobiidae and their placement out-


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[Vol. 47, No. 2

side of the clade of salamanderswith in- subordinalstatus for amphiumids. The reternalfertilization. lationship between the Amphiumidae and In their phylogenyincorporatingdata Salamandridae is a constant one in my from comparisonsof ribosomalRNA seg- analyses (Fig. 7), although the two families ments, Larsonand Wilson (1989) found are quite differentin cloacal anatomy.Male that the Plethodontidaeis the sister-group amphiumids lack the posterior ventral of all other salamanderfamiliesand that gland that is found in salamandrids (and amongthe non-plethodontids, the tree to- all other salamanderfamilies with internal pology is: Amphiuma(Andrias(Rhyaco- fertilization),but they possessa unique "pit triton (Notophthalmus(Necturus (Am- gland" in the posterior wall of the cloacal bystoma))))).The positionof Andrias is chamber that clearly has no structuralhomost intriguing.AlthoughI did not ex- mologue in any other family (Fig. 5C). amine Andrias,the speciesis well known The detailed histology of the amphiumid to have externalfertilizationas in Cryp- pit gland will be discussed in a forthcomtobranchus(Nussbaum,1985), and one ing paper. could hypothesize that the only glands The Proteidae contains five species in present in either sex would be ventral the genus Necturus occurring in eastern glands. By its placement in Larsonand North America, and one species, Proteus Wilson'stree, one would need to hypoth- anguinus, in the CarniolaAlps of Italy and esize that internalfertilizationevolved at Yugoslavia. Hecht and Edwards (1977) least twice, or that a reversalto external placed Necturus in a separatefamily, Necfertilizationoccurredin Andrias. turidae, and Estes (1981) placed the ProThe morphologicalcloacaldata are un- teidae and extinct Batrachosauroididaein equivocalin promotingthe view that in- their own suborder, Proteoidea. The cloternalfertilization,and the cloacalglands acal data show a sister-group relation beresponsiblefor this process,evolvedonce. tween the Proteidae and Plethodontidae The presenceof spermathecaefor sperm in some of the trees and in others, a tristoragein females and of spermatophore chotomy of Proteidae+ Plethodontidae+ forming glandsin males is a synapomor- Rhyacotritoninae. Parsimony analysis on phy for the suborderSalamandroidea. The other morphological data sets has placed relationshipsamongthesefamilies,andin- the Proteidae as the sister-groupof all othdeed the actualnumberof families,forms er families in the Salamandroidea (Hecht the substanceof the discrepanciesamong and Edwards, 1977; Milner, 1983), except recent attemptsat phylogeneticanalyses that Duellman and Trueb (1986) noted that of familial relationships(Duellman and positions of Proteidae, Amphiumidae, and Trueb, 1986; Hecht and Edwards,1977; Dicamptodontidae are interchangeable in Milner, 1983). Traditionally,the main their cladograms. Larson and Wilson problemsin constructingphylogeniesre- (1989) found a sister-group relation bevolve aroundpaedomorphosis and the re- tween Necturus and Ambystoma, and that sultant heterochronyand/or reversalof these two genera are more highly derived characters. than others analyzed. Clearly, problems Two families, Amphiumidaeand Pro- still exist with the placement of the Proteidae, consist wholly of aquatic paedo- teidae. Although proteids are most similar morphs.The three living species of the to plethodontidsin cloacal anatomy, plethAmphiumidaeare in the genus Amphi- odontids possess autapomorphies (comuma and occurin the southeasternUnited mon tube to the spermathecae in females, States.Estes (1981)followeda numberof caudal pelvic gland in males) that allow previous workers who placed the am- the cloacae to be easily distinguished. phiumidsin their own suborder,AmphiThe Salamandridae, composed of 15 umoidea. Because my results place the genera and some 53 species, occupies the Amphiumidaeas the sister-groupof other widest range of any extant salamander salamanderfamilies with internalfertil- family, with the greatest diversity in Asia ization,thiscouldbe viewedas supportfor and Europe. Hecht and Edwards (1977) This content downloaded from 147.174.85.132 on Tue, 30 Jun 2015 16:20:16 UTC All use subject to JSTOR Terms and Conditions

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and Milner (1983) found the Salamandridae to be the most apomorphic family, while Duellman and Trueb (1986) found that the Salamandridae is the sister-group of the Ambystomatidae and Plethodontidae. The position of the Salamandridaein my cladograms relative to other Salamandroidea is due to the presence of three ancestral traits: cilia in the female cloaca, the lack of epidermal lining in the dorsolateral walls of the anterior one-half of the cloacal chamber, and the lack of lateral pelvic glands (Fig. 7). Thus, althoughmuch diversity in cloacal structuresoccurs within the Salamandridae,salamandridseasily can be distinguished from all other families of salamanders by their cloacal anatomy. The Ambystomatidae, containing the genera Ambystoma (27 species) and Rhyacosiredon (four species), is endemic to North America, and a number of species are facultative or obligatory aquatic paedomorphs.The Dicamptodontidae consists of four species of Dicamptodon in the subfamily Dicamptodontinae and the monotypic Rhyacotriton olympicus in the subfamily Rhyacotritoninae,all of which occur in the Pacific northwestof the United States (Good, 1989; Good et al., 1987). In Dicamptodon, one species (D. copei) is a branchiated, aquatic paedomorph while both metamorphosed and aquatic paedomorphic populations are known from other species (D. aterrimus, D. ensatus, and D. tenebrosus). Until Edwards (1976) and Estes (1981), the Dicamptodontidae was usually given subfamilial status in Ambystomatidae (Tihen, 1958). More recently, questions have been raised as to whether Rhyacotriton merits separate familial status. Milner (1983) considered Rhyacotriton more closely related to plethodontids and amphiumids than to dicamptodontines, although he did not find this conclusion wholly satisfactory. Duellman and Trueb (1986) noted that the similarities between Rhyacotriton and plethodontidsare the result of convergence of paedomorphiccharacters, but that synapomorphies linking Rhyacotriton and Dicamptodon are weak, and that Dicamptodontidae may be poly-

187

phyletic. Good et al. (1987) noted that neither Ambystoma nor Dicamptodon is similar enough in its allozymes to make outgroup comparison with Rhyacotriton feasible. My results place Ambystomatidae and Dicamptodontinaeas sister-groups,and the ancestor of clades involving Rhyacotritoninae is the sister-taxonof the ancestor for Ambystomatidae + Dicamptodontinae (Fig. 7). If character H' is considered convergent in Ambystomatidae + Dicamptodontinae and Rhyacotritoninae,then the Dicamptodontidae is polyphyletic (Fig. 7A). If H' is symplesiomorphic for these taxa and Proteidae+Plethodontidae, but reversed in the latter, then Dicamptodontidae is paraphyletic (Fig. 7B). In either case, my results lend support to elevation of Rhyacotritoninaeto full familial status. The Plethodontidae is the largest family of salamanders with 28 genera and in excess of 220 species. Although two species occur in Europeand othersare known from South America, centers of diversity are in mountainous areas of North America and Central America. Plethodontids are usually considered most closely related phylogenetically to ambystomatids(Duellman and Trueb, 1986; Hecht and Edwards, 1977; Ruben and Boucot, 1989), although Milner (1983) found a sister-grouprelation with the Amphiumidae, and Larson and Wilson (1989) proposed that the Plethodontidae is the sister-groupto all other salamanders. As stated previously, both male and female plethodontids possess cloacal gland autapomorphiesthat allow their cloacae to be readily distinguished from those of other salamanders. Male plethodontids have the most highly specialized pelvic gland clustersof any salamanders,but vent glands are reduced in most forms. Although female ventral and dorsal glands are found in some members of both subfamilies and each tribe, these glands appear rudimentary or are lost in most female plethodontids except certain desmognathines (Sever and Trauth, 1990) and hemidactyliines (Sever, 1987, 1988b). The range of interspecific variation in cloacal anatomy encountered in some groups that are conservative in other mor-


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phological characters, such as Plethodon, is somewhat surprising. Perhaps more sampling will reveal that some of the variation detected is intraspecific. Studies in which relatively large samples (n > 10) of cloacal tissue have been examined, however, have noted little intraspecific variation (Sever, 1978a,b, 1988a; Sever et al., 1990b; Trauth, 1983, 1984; Williams et al., 1985). Also, Sever (1978a,b) firstnoted that P. cinereus and P. dorsalis are quite distinct in cloacal anatomy, and additional data now present suggest that the cloacal variation in Plethodon may correlate with species groups proposed by Highton and Larson (1979). The homology of the anterior ventral glands of male and female salamandersis apparent from an examination of species in which these are the only glands that exist, Cryptobranchus and the hynobiids (except for male Onychodactylus in which other cloacal glands also are present). Indeed, the ventral glands of male and female Hynobius and Batrachuperus are so similar in appearance that what sexual dimorphism exists in the cloacae is due to the cloacal conformation, and the sex of the specimen cannot be determined by cytology of the ventral glands. Because these glands are not involved in spermatophore formation or sperm storage in salamanders with external fertilization, Sever (1988b) postulated that the glands secrete a courtship pheromone, although this has not been confirmed in hynobiids or cryptobranchids. The ventral glands of female Eurycea cirrigera, however, have been found to be actively secreting a substance only during the preovipository mating season (Sever, 1988b). In the Salamandroidea, portions of the ancestral ventral gland mass have been modified for production of spermatophores (male pelvic, ventral, and Kingsbury's glands) and for storage of sperm (female spermathecae) with some other portions apparently retaining the putative ancestralfunction of mate attraction (male dorsal and vent glands, female ventral glands). This presumed specialization of male and female cloacal glands occurred concurrently with the divergence of the

[Vol. 47, No. 2

Salamandroidea. Thus, the search for homologies between male and female cloacal glands in the Salamandroidea(Beaumont, 1928; Lemaitre-Lutz, 1968; Noble and Pope, 1929) is largely a barren exercise. Male and female cloacal glands in the Salamandroidea have been under different, but linked, selective pressures since the evolution of internal fertilization in the common ancestor of the suborder. For example, the female spermathecae and male pelvic glands both represent modifications of the dorsal or anterior portion of the ancestral ventral gland. The most likely homology of the spermathecae and pelvic glands, therefore, is not to each other but to a similar area of the ancestral ventral gland. The pelvic and ventral glands presumably function in spermatophore production in all members of the Salamandroidea, although direct experimental evidence for this exists only for Desmognathus in the Plethodontidae (Sever and Houck, 1985). The dorsal gland in the Salamandridae is a known source of courtship pheromones (Malacarneand Vellano, 1987; Malacarne et al., 1984), and presumably the vent glands have a similarfunction in male Ambystomatidae, Amphiumidae, Dicamptodontidae, Plethodontidae, and Proteidae (Sever, 1980, 1981). Evidence for courtship pheromone production by male cloacal glands, however, is lacking in all families except Salamandridae. If the relation between spermatophore producing glands and courtship glands supposed above is correct within the Salamandroidea, the spermatophore producing (pelvic and ventral) glands are quite similar in cytology and arrangementwhile the putative courtship (dorsal and vent) glands vary greatly, as one might expect if the latter are sexually selected characters (Arnold and Houck, 1982). Courtshippheromone producing glands other than the dorsal and vent glands in salamandersare limited, as far as currently known, to the Salamandridae and Plethodontidae. In the Salamandridae, genial glands on the lateral surface of the head occur in Notophthalamus viridescens (Rogoff, 1927) and submandibular courtship


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1989. Female cloacal anatomy in the spectacled salamander, Salamandrina terdigitata (Amphibia: Salamandridae). Herpetologica 45:310-322. CHANG, M. L. Y. 1936. Contribution a l'tude morphologique, biologique et syst6matique des amphibiens urodeles de la Chine. Librairie Picart, Paris. DAVITT, C. M., AND J. H. LARSEN, JR. 1988. Scanning electron microscopy of the spermatheca of Plethodon larselli (Amphibia: Plethodontidae): Changes in the surface morphology of the spermathecal tubule prior to ovulation. Scan. Microscop. 2:1805-1812. DAWSON, A. B. 1922. The cloaca and cloacal glands of the male Necturus. J. Morphol. 36:447-465. DENT, J. N. 1970. The ultrastructure of the spermatheca in the red spotted newt. J. Morphol. 132: 397-424. DUELLMAN, W. E., AND L. TRUEB. 1986. Biology of Amphibians. McGraw-Hill, New York. EDWARDS, J. L. 1976. Spinal nerves and their bearing on salamander phylogeny. J. Morphol. 148:305327. . 1989. Two perspectives on the evolution of the tetrapod limb. Am. Zool. 29:235-254. ESTES, R. 1981. Handbuch der Palioherpetologie. Teil 2. Gymnophiona, Caudata. G. Fischer, Stuttgart. FARRIS, J. S. 1988. Hennig86 Reference, Version 1.5. State University of New York, Stony Brook, New York. FASOLO, A., AND A. GROSSO. 1969. Cloaca e ghianAcknowledgments. -This work was supported by dole annesse nel maschio di Triturus cristatus carBSR-8715341 from the National Science Foundation. nifex Laur. Boll. Zool. 36:121-180. For the loan or gift of specimens and/or aid in colFELSENSTEIN, J. 1986. PHYLIP, Version 2.7, Comlecting, I thank E. N. Arnold, S. N. Arnold, A. L. piled by G. D. F. Wilson. University of WashingBraswell, R. C. Bruce, B. Clarke, D. Duff, R. F. Inger, ton, Seattle, Washington. C. J. McCoy, P. Molar, R. A. Nussbaum, K. Ovaska, FOREY, P. L. 1986. Relationships of lungfishes. J. S. Perrill, C. D. Sullivan, W. VanDevender, and R. Morphol. Suppl. 1:75-91. Vogt. I also thank the undergraduate students at Saint FROST, D. R. (Ed.). 1985. Amphibian Species of the Mary's College who worked on this project: J. Darrow, World: A Taxonomic and Geographic Reference. P. Falaschetti, E. Heinz, P. Lempart, C. Mansfield, Allen Press, Inc. and The Association of Systematic and M. Taghon. Collections, Lawrence, Kansas. FUNK, V. A., AND D. R. BROOKS. 1990. Phylogenetic LITERATURE CITED systematics as the basis of comparative biology. Smithsonian Contrib. Botany 73:1-45. ARNOLD,S. J., AND L. D. HOUCK. 1982. Courtship GADOW, H. 1887. Remarks on the cloaca and coppheromones: Evolution by natural and sexual seulatory organs of Amniota. Philos. Trans. 178 (Ser. lection. Pp. 173-211. In M. H. Nitecki (Ed.), BioB):5-37. chemical Aspects of Evolutionary Biology. UniverGOIN, C. J., AND 0. B. GOIN. 1962. Introductionto sity of Chicago Press, Chicago. Herpetology. W. H. Freeman, San Francisco. BEAUMONT,J. DE. 1928. Modifications de l'appareil GOOD, D. A. 1989. Hybridization and cryptic speurogenital du Triton cristatus femelle apres greffe cies in Dicamptodon (Caudata: Dicamptodontide testicules. Compt. rend. Soc. Biol. 98:563-564. dae). Evolution 43:728-744. 1933. La diff6renciation sexuelle dans l'apGOOD, D. A., G. Z. WURST, AND D. B. WAKE. 1987. pareil uro-genital du Triton et son d6terminisme. Patterns of geographic variation in allozymes of W. Roux' Archiv. f. Entwicklungsmechanik 129: the olympic salamander, Rhyacotriton olympicus 120-178. (Caudata: Dicamptodontidae). Fieldiana Zool. New BRIZZI,R., C. CALLONI, AND G. DELFINO. 1986. Ser. (32):1-15. Accessory structures in the genital apparatus of Salamandra terdigitata (Amphibia: Salamandridae). HARDY, M. P., AND J. N. DENT. 1986. Transport of I. Ultrastructural patterns of the male abdominal sperm within the cloaca of the female red-spotted gland. Z. Mikrosk.-Anat. Forsch., Leipzig 100:397newt. J. Morphol. 190:259-270. 409. HECHT, M. K., AND J. L. EDWARDS. 1977. The

glands have been reported from Taricha torosa (Smith, 1941). In the Plethodontidae, mental hedonic glands on the chin occur in most species that have been examined (Sever, 1976), and caudal hedonic glands on the dorsaltail base have recently been described in the hemidactyliine genus Eurycea and may occur widely in the family (Sever, 1989). The vent gland is relatively small in most male plethodontids, and perhaps selection in this family has led to adaptationsfor delivery of courtship pheromonesby skin glands ratherthan reliance on a cloacal source. In summary, cloacal characters provide phyletic hypotheses that can be tested by examining their congruence with other characters.Cloacal anatomy, however, seems no exception to the homoplasy rampant in salamandermorphology. The goals for future studies are to determine the order of character transformations that illuminate the true pathway toward phyletic resolution and to avoid miscodings that lead us astray down the gloomy road of false inference.

BRIZZI, R., G. DELFINO, AND C. CALLONI.


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methodology of phylogenetic inference. Pp. 3-51. In M. K. Hecht, P. C. Goody, and B. M. Hecht (Eds.), Major Patterns in Vertebrate Evolution. Plenum Press, New York. HEIDENHAIN, M. 1890. Beitraige zur Kenntniss der Topographie und Histologie der Kloake und ihrer driisigen Adnexa bei den einheimischen Tritonen. Arch. Mikr. Anat. 35:173-274. HIGHTON, R., AND A. LARSON. 1979. The genetic relationships of the salamanders of the genus Plethodon. Syst. Zool. 28:579-599. HUMASON, G. L. 1979. Animal Tissue Techniques, 4th ed. W. H. Freeman, San Francisco. KINGSBURY, B. F. 1895. The spermatheca and methods of fertilization in some American newts and salamanders. Trans. Am. Microscop. Soc. 17: 261-304. KOHERING, V. 1925. The spermatheca of Eurycea bislineata. Biol. Bull. 49:250-265. KREEGER, F. R. 1942. The cloaca of the female Amphiuma tridactylum. Copeia 1942:240-245. LAGIOS, M. D., AND J. E. MCCOSKER. 1977. A cloacal excretory gland in the lungfish Protopterus. Copeia 1977:176-178. LARSON, A. 1984. Neontological inferences of evolutionary pattern and process in the salamander family Plethodontidae. Pp. 119-217. In M. K. Hecht, B. Wallace, and G. T. Prance (Eds.), Evolutionary Biology, Vol. 17. Plenum Press, New York. LARSON, A., AND A. C. WILSON. 1989. Patterns of ribosomal RNA evolution in salamanders. Mol. Biol. Evol. 6:131-154. LEMAITRE-LUTZ, F. 1968. Anatomie des glandes pelviennes de la femelle de Pleurodeles waltlii Michah: Leur role de receptacle seminal. Ann. Embryol. Morphol. 1:409-416. MADDISON, W. P., M. J. DONOGHUE AND D. R. MADDISON. 1984. Outgroup analysis and parsimony. Syst. Zool. 33:83-103. MALACARNE, G., L. BOTTONI, R. MASSA, AND C. VELLANO. 1984. The abdominal gland of the crested newt: A possible source of courtship pheromones. Preliminary ethological and biochemical data. Monitore Zool. Ital. (N. S.) 18:33-39. MALACARNE, G., AND C. VELLANO. 1987. Behavioral evidence of a courtship pheromone in the crested newt, Triturus cristatus carnifex Laurenti. Copeia 1987:245-247. MILNER, A. R. 1983. The biogeography of salamanders in the Mesozoic and early Cenozoic: A cladistic-vicariance model. Pp. 431-468. In R. W. Sims, J. H. Price, and P. E. S. Whalley (Eds.), Evolution, Time and Space: The Emergence of the Biosphere. Academic Press, London. 1988. The relationships and origin of living amphibians. Pp. 59-102. In M. J. Benton (Ed.), The Phylogeny and Classification of the Tetrapods, Vol. 1: Amphibians, Reptiles, Birds. Systematics Association Special Vol. 35A, Clarendon Press, Oxford, UK. NOBLE, G. K., AND M. K. BRADY. 1933. Observations on the life history of the marbled salamander, Ambystoma opacum Gravenhorst. Zoologica 11: 89-132.

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1929. The modification of the cloaca and teeth of the adult salamander, Desmognathus, by testicular transplants and castration. J. Exp. Biol. 6:399-411. NUSSBAUM, R. A. 1985. The evolution of parental care in salamanders. Univ. Michigan Misc. Publ. Mus. Zool. 169:1-50. PLATNICK, N. I. 1977. Paraphyletic and polyphyletic groups. Syst. Zool. 26:195-200. POOL, T. B., AND T. R. HOAGE. 1973. The ultrastructure of secretion in the spermatheca of the salamander, Manculus quadridigitatus (Holbrook). Tissue Cell 5:303-313. ROGOFF, J. L. 1927. The hedonic glandsof Triturus viridescens; a structural and functional study. Anat. Rec. (Abst.) 34:132-133. RUBEN,

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lucifuga and Eurycea longicauda (Amphibia: Plethodontidae). Herpetologica 41:272-281. 1941. The cloaca in the male Amphiuma tridactylum. Anat. Rec. (Suppl. Abst.) 81: 63. ZELLER, E. 1905. Untersuchungen iuber die Samentraiger und den Kloakenwulst der Tritonen. Zeitsch. wissen. Zool. 74:171-221.

WILSON, F. H.

Accepted: 19 July 1990 Associate Editor: David Cannatella APPENDIX I Sex, SVL, collection dates, and locality data are given for specimens described for the first time in this paper. Where not indicated, SVL's, collection dates, and localities are unknown. The female Necturus punctatus from Scotland County, North Carolina, one female Taricha torosa, and male and female Paramesotriton hongkongensis are held by S. J. Arnold (SJA), University of Chicago. The remaining specimens are in the British Museum of Natural History (BMNH), Carnegie Museum (CM), Field Museum of Natural History (FMNH), Florida State Museum (UF), North Carolina State Museum (NCSM), The University of Michigan Museum of Zoology (UMMZ), or my possession (DMS). Microscope slides will be placed in the UMMZ. Ambystomatidae: Ambystoma annulatum -9 UMMZ 187374, 89.0 mm. A. gracile-a UMMZ 133156.2, 97.8 mm, and 9 UMMZ 133156.1, 95.6 mm, 17 March 1969, Polk County, Oregon. A. lateraleQUMMZ 187371,57.1 mm, 13 September 1975, Manitowoc County, Wisconsin. A. maculatum-9 UMMZ 187377, 89.5 mm, 11 April 1980, Cass County, Michigan. A. opacum-9 UMMZ 187373, 68.3 mm, fall 1983, Missouri. A. platineum-99 UMMZ 122856, 78.4 mm, UMMZ 122857, 79.0 mm, UMMZ 122859, 85.0 mm, and UMMZ 122860, 79.1 mm, 1961, Franklin County, Massachusetts. A. talpoideum-9 UMMZ 187378, 55.9 mm, 22 February 1982, Henderson County, North Carolina. A. texanum-9 UMMZ 187376,83.5 mm, 22 February 1970, Hamilton County, Ohio. A. tigrinum-9 UMMZ 187375, 110.7 mm, 18 March 1980, St. Joseph County, Indiana. A. tremblayi-99 UMMZ 122736, 64.8 mm, 15 April 1960, Kent County, Michigan; UMMZ 122783.1, 74.2 mm, UMMZ 122783.2, 80.0 mm, and UMMZ 122783.3, 81.3 mm, 23 February 1961, Delaware County, Indiana. Amphiumidae: Amphiuma means - UMMZ 187365, 520 mm, 14 April 1987, Marion County, Florida. A. pholeter-e UF 62411, 160 mm, 12 May 1985, Levy County, Florida. A. tridactylum-&i UMMZ 187363, 421 mm, and UMMZ 187366, 481 mm, no other data; DMS 4103, 725 mm, 29 May 1974 [sacrificed 17 November 1980], Orleans Parish, Lou-


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isiana. Cryptobranchidae: Cryptobranchusalleganiensis-88 UMMZ 187361, 292 mm, and DMS 6729 [gross dissection only], 28 cm, 27 July 1984, Dallas County, Missouri, and immature a DMS, 125 mm, no other data. Dicamptodontidae (Dicamptodontinae): Dicamptodon aterrimus -9 metamorph UMMZ 134671, 135 mm, 10 May 1967, Benewah County, Idaho. D. copei -2 UMMZ 134960.1, 101.5 mm, and UMMZ 134960.2, 110.0 mm, 24 August 1969, Skamania County, Washington. D. tenebrosus-99 paedomorphs UMMZ 137462.1, 130 mm, and UMMZ 137462.2, 123 mm, 13 September 1975, Linn County, Oregon. Dicamptodontidae (Rhyacotritoninae): Rhyacotriton olympicus-99 UMMZ 135501.1, 52.2 mm, and UMMZ 135501.2, 54.2 mm, 29 May 1983, Multnomah County, Oregon. Hynobiidae: Batrachuperus pinchonii-a FMNH 232840,103.0 mm, and 9 FMNH 232844, 106.3 mm, 31 May 1987, Sichuan, China. B. tibetanus-a FMNH 15153, 74.8 mm, and 9 FMNH 15154, 62.2 mm, 15 April 1929, Szechwan, China. Hynobius leechii-a FMNH 25248, 58.0 mm, 19 December 1934, Songdo, Korea, and 2 FMNH 21060.6, 71.5 mm, 1934, Chosen, Korea. H. stejnegeri-a BMNH 1932.7.18.1, 57.7 mm, April, 1932, Kummamoto-Ken, Japan. H. tsuensis -a BMNH 1911.2.24.6, 74.1 mm, 1911, Tsu Shima, Japan. Onychodactylus japonicus-8 UMMZ 70212, 69.0 mm, Yamanashi, Japan, and 9 UMMZ 131037, 80.0 mm, 1971, Tochigi, Japan. Plethodontidae (Plethodontinae: Bolitoglossini): Batrachoseps attenuatus-a8 UMMZ 187388, 36.3 mm, and UMMZ 187390, 37.0 mm, 27 June 1981, Humboldt County, California. B. pacificus-a UMMZ 86794.2, 43.4 mm, 7 January 1934, Los Angeles County, California. B. wrighti a UMMZ 135737.3, 41.4 mm, 7 June 1974, Lane County, Oregon. Bolitoglossa adspersa-a UMMZ 126381.4, 49.6 mm, 26 July 1965, Cundinamarca, Columbia. B. franklini-d UMMZ 137343.2,70.4 mm, 21 May 1975, between San Marcos and San Rafael, Guatemala. B. platydactyla-d UMMZ 85440.2, 70.4 mm, 9 January 1939, Paraje San Rafael, Veracruz, Mexico. B. rufescens-aa CM 93732, 36 mm, 30 June 1983, Playa Escondida, Veracruz, Mexico, and UMMZ 85444.1, 28.4 mm, 28 May 1975, Paraje Nuevo San Rafael, Veracruz, Mexico. B. subpalmata-aa UMMZ 187392, 41.2 mm, and UMMZ 187395, 46.5 mm, 24 June 1973, Alajuela Province, Costa Rica. Chiropterotriton chiropterus-a UMMZ 115111.2, 31.2 mm, 18 June 1956, Morelos, Mexico. C. multidentatus a UMMZ 105115.2, 38.9 mm, 2 September 1951, Hidalgo, Mexico. Dendrotriton bromeliacia-a UMMZ 137115, 31.9 mm, 14 July 1973, near San Marcos, Guatemala. Hydromantesshastae-a UMMZ 142820, 62.4 mm, 21 March 1966, Shasta County, California. H. italicus-a BMNH 1928.12.20.420, 56 mm, 15 February 1928, Val di Castello, Switzerland [locale according to catalogue, perhaps erroneous]. Lineatriton lineola-a UMMZ 89242, 35.3 mm, 21 January 1940, Metlac, Veracruz. Oedipina poelzi-d UMMZ 136989.1, 60.7 mm, 1 July 1973, Heredia Province, Costa Rica. P. goebeli-a UMMZ 137365.3, 58.6 mm, 21 May 1975, between San Marcos and San Rafael, Guatemala. P. leprosa-aM CM 93724, 39 mm, and CM 93723, 42 mm, 6 July 1983, Cohuacan, Mexico. P. rex-a UMMZ 120068.1, 45.3 mm, 20 May 1955,

[Vol. 47, No. 2

Huehuetenango, Guatemala. Thorius macdougalliy6 UMMZ 119705.3, 19.2 mm, and UMMZ 119705.4,

20.5 mm, 2 April 1959, Oaxaca, Mexico. Plethodontidae (Plethodontinae: Hemidactyliini): Hemidactylium scutatum-88 no voucher specimen, 31.0 mm, DMS 3409, 16 April 1978, DMS 3850, 26 May 1979, DMS 3983-3984, 11 April 1980, and DMS 5635, 16 September 1982, Cass County, Michigan. Typhlotriton spelaeus-6 UMMZ 187449, 42.7 mm, 14 April, 1974, Pulaski County, Missouri. Plethodontidae (Plethodontinae: Plethodontini): Aneides aeneus-&M UMMZ 187379, 27 July 1973, Macon County, North Carolina, and UMMZ 187381, 54.0 mm, 25 October 1983, Etowah County, Alabama, and 2 UMMZ 187382, 58.0 mm, 25 April 1970, Monongalia County, West Virginia. A. ferreus-e UMMZ 187383, 58.5 mm, 23 June 1981, and 2 UMMZ 187384, 62.8 mm, 24 June 1981, Benton County, Oregon. A. lugubris-6 UMMZ 119015, 64.4 mm, 7 May 1955, Marin County, California, and 9 UMMZ 117097, 83.1 mm, 23 February 1957, Orange County, California. Ensatina eschscholtzii-&M UMMZ 130671, 60.4 mm, January 1970, Contra Costa County, California, and UMMZ 130677.3, 56.0 mm, and QQUMMZ 130677.1, 72.9 mm, and UMMZ 130677.2, 65.2 mm, Contra Costa County, California. Plethodon cinereus-6 UMMZ 187495, 40.8 mm, 25 October 1983, Montgomery County, Indiana. P. dorsalis - UMMZ 187497, 38.0 mm, 29 October 1983, Montgomery County, Indiana. P. elongatus-&d UMMZ 135822.2, 61.8 mm, and UMMZ 135822.3, 66.2 mm, and 2Q UMMZ 135822.1, 72.2 mm, 16 April 1974, and UMMZ 135823, 65.8 mm, 25 April 1974, Josephine County, Oregon. P. glutinosus-6 UMMZ 187501, 69.3 mm, 25 April 1970, Monongalia County, West Virginia, and 2 UMMZ 187507, 61.8 mm, 10 April 1976, Parke County, Indiana. P. jordani-&i UMMZ 187509, 23 July 1973, and no voucher specimen, 8 August 1982, Macon County, North Carolina, and 2 UMMZ 187510, 58.6 mm, 11 August 1982, Watuga County, North Carolina. P. ouachitae-6 UMMZ 187370, 60.7 mm, and 2 UMMZ 187367, 71.0 mm, 11 April 1974, Polk County, Arkansas. P. richmondi-a UMMZ 187514, 47.7 mm, and 9 UMMZ 187513, 45.9 mm, 3 November 1982, Watuga County, North Carolina. P. serratus- UMMZ 187517, 40.8 mm, 14 March 1982, Monroe County, Tennessee, and Q UMMZ 187520, 44.8 mm, 21 October 1982, Graham County, North Carolina. P. teyahalee-, UMMZ 187499, 57.1 mm, and 2 UMMZ 187500, 60.6 mm, 15 March 1982, Monroe County, Tennessee. P. vehiculum-6 UMMZ 187524, 49 mm, and 2 UMMZ 187523, 55 mm, October 1986, Vancouver, British Columbia. P. websteri-6 UMMZ 187528, 35.0 mm, and 2 UMMZ 187527, 38.4 mm, 25 October 1983, Etowah County, Alabama. P. wehrlei-a UMMZ 85731, 42.5 mm, and 2 UMMZ 87530, 36.7 mm, 11 August 1982, Avery County, North Carolina. P. yonahlossee-e UMMZ 120668, 81.9 mm, 1958, Grayson County, Virginia, and 2 UMMZ 120670, 77.1 mm, 1958, Smyth County, Virginia. Proteidae: Necturus beyeri-6 UMMZ 187488,114.4 mm, 10 November 1971, St. Tammany Parish, Louisiana. N. lewisi-a NCSM 22338, 147.2 mm, 21 March 1980, and 2 NCSM 22333, 136.3 mm, 17 March 1980, Warren County, North Carolina. N.


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maculosus-6 DMS, 185 mm, and 2 DMS, 184 mm, from Carolina Biological Supply Co., Burlington, North Carolina. N. punctatus -8 NCSM 22433, 117.2 mm, and 2 NCSM 22434, 109.5 mm, 11 January 1980, Pitt County, North Carolina; d SJA, 67.9 mm, and 9 SJA, 88.5 mm, 22 February 1988, Scotland County, North Carolina. Proteus anguinus-9 UMMZ 187489 134.9 mm, August 1931, Regensburg, Germany [locale according to old tag, probably erroneous]. SalChioglossa lusitanica -6 BMNH amandridae: 1936.10.6.3, 50 mm, and 2 BMNH 1936.10.6.4, 50 mm, near Posto, Portugal. Cynops orientalis-6 UMMZ 187450, 65.4 mm, and 22 UMMZ 187451, 76.5 mm, and SJA, 52.4 mm. C. pyrrhogaster-d UMMZ 187452, 53.0 mm, and 2 UMMZ 187453, 58.1 mm, no other data; d FMNH 204767, 57.0 mm, 7 June 1970, and 2 FMNH 204686, 68.7 mm, 15 May 1970, Kanagawa Prefecture, Japan. C. wolterstorffi6 BMNH 1907.5.4.40, 66.1 mm, 4 May 1907, and 2 BMNH 1908.2.27.5, 84.6 mm, 27 February 1908, Yunnam, China. Euproctus asper -6 BMNH 1976.1246, 76 mm, and 9 BMNH 1976.1247, 74 mm, Harpea, East Pyrenees, France. E. montanus-9 BMNH 1928.12.20.378,48.7 mm, 20 December 1928, Vizzavona, Corsica. Mertensiella luschani-6 BMNH 1964.355, 60.5 mm, and 2 BMNH 1964.354, 63.5 mm, 14 April 1962, Dodunga, Mugla Province, Turkey. Notophthalmus perstriatus-6 UMMZ 187454, 34.2 mm, and 9 UMMZ 187455, 33.3 mm, 26 April 1987, UMMZ Putnam County, Florida. N. viridescens-9 187456, 55.2 mm, 10 May 1979, Monroe County, Indiana. Pachytriton brevipes-9 DMS, 72.1 mm, no other data; 6 FMNH 24394, 71.2 mm, and 2 FMNH

193

24393, 79.0 mm, 24 August-5 October 1925, Fukien Province, China. Paramesotriton chinensis-.a UMMZ 187457, 76.7 mm, and 22 UMMZ 187458, 75.1 mm, and DMS 76 mm. P. hongkongensis-e SJA, 72.4 mm and 9 SJA, 67.7 mm, October 1973, Hong Kong. Pleurodeles waltl-a FMNH 84879, 95.9 mm, and 9 FMNH 84877, 91.2 mm, 1950, Spain. Salamandra atra-6 BMNH 1970.1818, 54.7 mm, 17 August 1970, Mt. Zlebeh, Yugoslavia, and 2 BMNH 1970.1821, 72.4 mm, 19 August 1970, Trenta Valley, Yugoslavia. S. UMMZ 187461, 87.5 mm, and salamandra-68 UMMZ 187460, 99.5 mm, and 2 UMMZ 187459 111.1 mm. Taricha rivularis-8 UMMZ 187462, 70.6 mm. T. torosa-a UMMZ 187463, 71.7 mm, and 29 UMMZ 187464, 69.5 mm, and SJA, 69.4 mm. Triturus alpestris-8 BMNH 1983.637, 47.5 mm, and 9 BMNH 1983.638, 54.2 mm, 7 June 1983, near Nismes, BelBMNH 1973.3467, 33.4 mm, and gium. T. boscai9 BMNH 1973.3470, 39.2 mm, 1973, Oviedo, Spain. T. cristatus-&6 UMMZ 187465,55.4 mm, and UMMZ 187466, 72.3 mm, and 9 UMMZ 187467, 79.7 mm, March 1981, Bucks, England. Tylototriton verrucosus-&- UMMZ 187468,70.1 mm, and FMNH 215480, 76.4 mm, and 22 UMMZ 187469,76.4 mm, and FMNH 212344, 91.6 mm. Sirenidae: Pseudobranchusstriatus-a UMMZ 187482, 63.3 mm, 17 April 1986, Columbia County, Florida, and 2 UMMZ 187481, 84.2 mm, 10 April 1987, Marion County, Florida. Siren intermedia-6M UMMZ 187483, 116.4 mm, 30 August 1969, and UMMZ 187484, 135.1 mm, 1 November 1969, Jones County, North Carolina. S. lacertinaUMMZ 187362, 354 mm, 13 April 1987, Hernando County, Florida.
