Short Notes Taxonomy of the Plethodontid Salamander Genus

Short Notes

Taxonomy of the Plethodontid Salamander Genus Hydromantes (Caudata: Plethodontidae)

David B. Wake1, Alfredo Salvador2, Miguel A. Alonso-Zarazaga3

The plethodontid salamanders that occur in Eu- mantes, for the European species. His sugges- rope are included in the taxon Speleomantes tion for the taxonomy of the group was to recog- Dubois 1984, which is treated either as a genus nize a single genus, Hydromantoides, with two (e.g., Lanza, 1999), or as one of two subgen- subgenera, Hydromantoides and Speleomantes. era of Hydromantes Gistel 1848 (e.g., Jack- Lanza (1986) subsequently raised Speleomantes man et al., 1997). In the latter case, the sub- to generic level. genus Hydromantes includes only North Amer- The name Hydromantes had been widely ican (i.e., Californian) species. The taxonomic used, and the demonstration by Dubois (1984) history of Hydromantes (sensu lato) is compli- that it was a substitute name for a taxon cated. The species currently assigned to Hydro- whose type species is a member of the Sala- mantes and/or Speleomantes were placed in var- mandridae had serious implications. Dubois re- ious genera (e.g., Geotriton, Spelerpes)prior duced Hydromantes to the synonymy of Trit- to 1923, when Dunn made a proposal that sta- urus Rafinesque, 1815, which of course made bilized taxonomy (all species placed in Hy- it unavailable for plethodontids. This led Smith dromantes) for over 60 years, until Lanza and Vanni (1981) assigned the American species and Wake (1993) to offer a possible solution (by this time, three in number) to a new genus to the International Commission on Zoologi- Hydromantoides on the basis of morphological Nomenclature. They suggested that Sala- cal and genetic data (see also Lanza et al., mandra genei Temminck & Schlegel, 1838 be 1995). Dubois (1984) showed that Dunn had designated as the type species of Hydromantes, erred in technical but significant details of tax- thereby preserving the name for species of the onomic procedure in using the name Hydro- Plethodontidae. Discussion followed (Dubois, mantes, and proposed a new name, Speleo- 1995; Salvidio, 1995; Smith et al., 1995, 1996), and a modification of the proposal was offered that would retain Speleomantes for European 1 - Museum of Vertebrate Zoology and Department of Inte- grative Biology, University of California, Berkeley, CA species and restore Hydromantes for Amer- 94720-3160 ican species (Dubois, 1995). This proposal e-mail: [email protected] 2 - Departamento de Ecología Evolutiva, Museo Nacional was accepted, and the International Commis- de Ciencias Naturales, CSIC, José Gutiérrez Abascal, 2, sion on Zoological Nomenclature issued Opin- 28006 Madrid, Spain ion 1866 (1997) designating Spelerpes platy- 3 - Departamento de Biodiversidad y Biología Evolutiva, Museo Nacional de Ciencias Naturales, CSIC, José cephalus Camp, 1916 as the type species of Hy- Gutiérrez Abascal, 2, 28006 Madrid, Spain dromantes Gistel, 1848.

Although Gistel (1848) had used Hydro- 1868). In later years, this taxon and Gistel’s mantes originally as a replacement name for book were mentioned by Mertens and cowork- Geotriton (i.e., Triturus), twenty years later ers in two checklists of the European herpeto- (Gistel, 1868) he reverted to use of Geotri- fauna (Mertens & Müller, 1940; Mertens & ton and the name Hydromantes did not ap- Wermuth, 1960), and more recently, Arnold pear. The two species he assigned to Geotri- (1973) transferred Lacerta wagleriana to Po- ton in 1868 were identified as “fuscus Bonap.” darcis wagleriana and again cited Gistel’s book. and “cinereus? Merr.”. The intention of Gis- Mertens (1936) explicitly lists Atylodes among tel (1868) is clear, because following the en- the new taxa in Gistel (1868), as follows: “Cau- try “Geotriton Bonap.” the vernacular name is data. S. 158 Atylodes, Typus: Salamandra genei given: “Höhlenmolch”, or Cave Salamander, the SCHLEGEL:—Hydromantes GISTEL 1848”. widely used term for the biological entity that he The latest edition of the International Code referred to Geotriton fuscus and that currently of Zoological Nomenclature (1999) protects is known as either Hydromantes (Speleomantes) Speleomantes, which has been cited extensively italicus or Speleomantes italicus. since it was first proposed. Our proposal is that Gistel (1868) listed a number of genera un- the name Atylodes also should be preserved and der the general heading “Salamandrini (Sala- herein we present our argument. manderartige Lurche)”. The first genus listed Molecular and morphological studies of Hy- is “LIII Atylodes Gistel (Ohndrüser)”, and its dromantes (sensu lato) have shown that the only species is “103 Genei”, from “Sardinien”. genus is monophyletic and that it includes The brief description of Atylodes, in German, three, not two, subclades (Wake et al., 1978; is accurate for the taxon today known as Hy- Lanza et al., 1995; Jackman et al., 1997). Wake dromantes (Speleomantes) genei, which occurs (1966) presented morphological evidence of only on the southwestern part of the island of monophyly for the genus, and those charac- Sardinia. The next genus listed is “LIV, Sala- ters have not been challenged. Especially com- mandra”, and from context it is apparent that pelling is the unique hyobranchial apparatus Gistel was distinguishing Atylodes from Sala- and tongue (see also Lombard and Wake, 1977, mandra. The vernacular name he chose for Aty- 1986; Lanza et al., 1995; Jackman et al., 1997). lodes translates into English as the glandless Molecular data (sequences of the mitochondrial salamander, and Gistel explicitly emphasized gene cytochrome b) also support monophyly, as the lack of parotoid glands (“Keine Parotiden”). does a combined analysis of morphological and Geotriton appears later in the list, as genus num- molecular data (Jackman et al., 1997). ber LVIII. Within Hydromantes Wake (1966) showed Had the work of Gistel (1868) been known that the European and American species dif- to Dubois (1984), we believe that he would fered in some osteological features (shape of have adopted the name Atylodes rather than facial process of maxilla, most ribs bicipital proposing the new name Speleomantes.Gis- in American species but unicipital in European tel’s work has been cited rarely in the herpeto- species), and there are also some other morphological literature and the name Atylodes, men- logical and behavioural differences (Lanza and tioned by Neave (1939) in his list of generic Vanni, 1981; Lanza et al., 1995). Wake et al. and subgeneric taxa, remained unnoticed un- (1978) measured albumin immunological dis- til now. Mertens (1936) was the first to men- tances between the two groups and obtained dis- tion Gistel’s book when he revalidated the taxon tances of 47 and 48. They suggested on the ba- Podarcis muralis var. wagleriana Gistel, 1868 sis of these and allozymic data that the Euro- and elevated it to species rank in combina- pean and American lineages had been diverg- tion with Lacerta, Lacerta wagleriana (Gistel, ing for about 28 million years (using a molecu- Short Notes 545 lar evolutionary clock calibration of 1.7 albumin mosomes, and this is generally thought to be immunological distance units equals roughly an ancestral feature in the Plethodontidae (Ses- one million years). Immunological distances be- sions and Kezer, 1991). The 14th pair of chro- tween species within the American group were mosomes of the American species is metacen- from 1-9, but distances between the European tric (presumed to be the ancestral state) whereas species were not measured because antiserum that of H. genei and the other European species was available only for the American species Hy- is subtelocentric. Nardi (1991) also reported dif- dromantes shastae. ferences between H. genei and the other Euro- Wake et al. (1978) presented a limited study pean species with respect to the distribution of of allozymes (18 loci in 70 specimens, including centromeric satellites on chromosomes, and fur- all American species plus one population each thermore found that H. genei differed from the of H. genei and H. italicus) and reported large others in having more pericentric heterochro- genetic distances between the European and matin and more restriction sites for a particu- American species (averaging DNei of about 1). lar marker in ribosomal genes. In a later study, Surprisingly, Wake et al. (1978) also found a Nardi et al. (1999) report a number of differ- genetic distance of about 1 between the two ences between H. shastae, H. genei, and the European species studied (Hydromantes genei other European species with respect to repeti- and Hydromantes italicus). tive DNA. The results, too technical to be easily Extensive allozymic investigations of the Eu- summarized here, suggest that H. genei retains ropean species by Lanza et al. (1995) and some ancestral elements, and it consistently dif- Nascetti et al. (1996) using 33 loci in nearly fers from other European species as well as 500 specimens reported genetic distances be- from H. shastae. tween European and American species so great Lanza and Leo (2001) reported that one pop- as to be essentially unmeasureable. The three ulation of Hydromantes imperialis gives birth to species from eastern Sardinia (H. flavus, H. im- living young, but the data, although based on in- perialis, H. supramontis) are more closely re- dependent observations by two observers, were lated to the species on the European mainland scanty. Early reports of live-bearing in continen- (H. ambrosii, H. italicus, H. strinatii) than they tal species are suspect, and although reproduc- are to H. genei, which is limited in distribu- tive habits of the different species of European tion to the southwestern part of the island. Ge- plethodontids are not fully known, the Ameri- netic distances between H. genei and the other can species are all oviparous, as is H. genei, and European species are greater than 1.47 (Wake clutches of eggs are known for some but not et al., 1978, reported a distance of 1.135 with all of the remaining European species (Lanza, their limited sample). Nascetti et al. (1996) also 1999). Thus, all of the provocative accounts of reported substantial geographic differentiation live-bearing are for mainland or eastern Sar- within the limited range of H. genei (DNei as dinian species (Lanza, 1999; Lanza and Leo, great as 0.25), raising the possibility that more 2001). than a single species should be recognized and Studies of sequences of the mitochondrial suggesting that the taxon is relatively old. gene cytochrome b (Jackman et al., 1997) Nardi (1991) showed that morphologically showed that the European and American species differentiated sex chromosomes of the XX/XY group were well differentiated from each other, type occur in the continental species, as well as with each forming a clade. A basal polytomy in the eastern Sardinian species. However, sex in the European clade left relationships between chromosomal dimorphism is absent in H. genei. H. italicus, H. genei, and two species from The American species of Hydromantes also eastern Sardinia unresolved (however H. supra- lack morphologically differentiated sex chro- montis and H. flavus were close relatives with 546 Short Notes high support). The Kimura 2-parameter dis- native, the new molecular data (Jackman et al., tance between H. genei and the other European 1997, not cited by Nascetti et al.) and the analy- species was the highest recorded in the Euro- sis of Larson et al. (2003) are more compatible pean clade (13.7-15%). More extensive studies with the scenario of Lanza et al. (1995). of DNA sequence evolution in Hydromantes are All available data agree that H. genei is in progress. widely divergent from the other European Larson et al. (2003) summarized available species in proteins, mitochondrial DNA, sex data for Hydromantes and suggested an approx- chromosomes, and perhaps even in reproduc- imate early Eocene divergence of the American tion, and to a minor extent in morphology. Ac- and European lineages and an Oligocene diver- cordingly, because we think that the phyloge- gence of the two European lineages from each netic information is most readily reflected taxo- other. In turn, they suggest an Early Miocene di- nomically through the use of subgenera (see ar- vergence of the eastern Sardinian and mainland guments in Jackman et al., 1997, and Parra-Olea lineages. The weight of all available evidence et al., 2004), we propose the following taxon- (as hypothesized by Lanza et al., 1995, and crit- omy: ically evaluated by Delfino et al., in press) is that Genus Hydromantes Gistel, 1848 the European and American lineages separated Subgenus Hydromantes Gistel, 1848 very long ago, possibly associated with the sep- Included species: Hydromantes (Hydro- aration of the continental masses that gave rise mantes) platycephalus (Camp, 1916); Hy- to North America and Europe around 50 ma. dromantes (Hydromantes) brunus Gor- Lanza (1983), Nardi (1991), Lanza et al. man, 1954; Hydromantes (Hydromantes) (1995), Nascetti et al. (1996) and Delfino et al. shastae Gorman et Camp, 1953 (in press) all discuss historical biogeography of Subgenus Atylodes Gistel, 1868 the European species. Progenitors of H. genei Included species: Hydromantes (Atylodes) are thought to have separated from a continental genei (Temminck et Schlegel, 1838) ancestral stock (fossil Hydromantes are known Subgenus Speleomantes Dubois, 1984 from the Middle Miocene of Slovakia; Venczel Included species: Hydromantes (Speleo- and Sanchíz, 2005) during the late Oligocene mantes) italicus Dunn, 1923; Hydromantes (27-30 Myr) when a Sardinian-Corsican mi- (Speleomantes) ambrosii Lanza, 1955; croplate was detached from the main Euro- Hydromantes (Speleomantes) flavus Ste- pean plate (see Alvarez, 1972, and Boccaletti fani, 1969; Hydromantes (Speleomantes) et al., 1990, for detailed reconstructions). Lanza supramontis Lanza, Nascetti et Bullini, (1983; see also Lanza et al., 1995) hypothesized 1986; Hydromantes (Speleomantes) impe- that the microplate that became Sardinia may rialis Stefani, 1969; Hydromantes (Speleo- have formed from two parts, which migrated mantes) strinatii Aellen, 1958 separately with ancestors of H. genei occupy- ing a small “Iglesiente block”, a fossil island Because this is also a phylogenetic classi- that definitively joined the larger block to form fication it is readily convertable to alternative the present island of Sardinia in the Pliocene. classification systems, such as the phylocode. Ancestors of the present-day species of eastern In a phylogenetic classification the generic-level Sardinian are thought to have migrated from the clade would be Hydromantes.IfAtylodes and mainland to the larger of the two parts of the mi- Speleomantes are sister taxa, as all available croplate during the latest Miocene (Messinian, morphological and biochemical evidence sug- about 6 Myr), when desiccation restored a land gests, the name of the subordinate clade would connection to the continent. Although Nascetti be Atylodes, which has priority over Speleo- et al. (1996) also considered a more recent alter- mantes. Short Notes 547

Acknowledgements. Gistel (1868) is a rare book, and Lanza, B. (1986): I Rettili e gli Anfibi. In: L’ambiente natu- after many enquiries, one of us (M. A. A.-Z.) was able rale in Sardegna (Elementi di base per la conoscenza e la to locate one copy at the Senckenberg Museum (Frankfurt gestione del territorio, p. 289-321 + 549-550. Camarda, am Main, Germany) library. We thank Dr. Damir Kovac I., Falchi, S., Nudda, G., Eds, Sassari, Carlo Delfino Ed- (Senckenberg Museum, Frankfurt am Main, Germany) for itore. making available to us a xerox copy of this book. We thank Lanza, B. (1999): Plethodontidae — Lungenlose Salaman- Matthias Stöck for linguistic and bibliographic assistance ders. In: Handbuch der Reptilien und Amphibien Eu- and Hobart M. Smith for discussion. We appreciate the ropas, Band 4/1, Schwanzlurche (Urodela), I, p. 77-204, constructive review of the manuscript by Massimo Delfino Wiesbelshein, ALUA Verlag. and Benedetto Lanza. Lanza, B., Leo, P. 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Salvidio, S. (1995): Comments on the proposed conserva- Gistel, 1848 (Amphibia, Cuadaa) by the designation of tion of Hydromantes Gistel, 1848 (Amphibia, Caudata) Salamandra genei Temminck & Schlegel, 1838 as the by the designation of Salamandra genei Temminck & type species. Bull. Zool. Nomencl. 53: 48. Schlegel, 1838 as the type species. Bull. Zool. Nomencl. Venczel, M., Sanchíz, B. (2005): A fossil plethodontid sala- 52: 339-340. mander from the Middle Miocene of Slovakia (Caudata, Sessions, S.K., Kezer, J. (1991): Evolutionary cytogenetics Plethodontidae). Amphibia-Reptilia 26, in press. of bolitoglossine salamanders (Family Plethodontidae). Wake, D.B. (1966): Comparative osteology and evolution of In: Amphibian Cytogenetics and Evolution, p. 89-130, the lungless salamanders, family Plethodontidae. Mem- Green, D., Sessions, S.K., Eds, San Diego, Academic oirs, South. Calif. Acad. Sci. 4: 1-111. Press. Wake, D.B., Maxson, L.R., Wurst, G.Z. (1978): Genetic dif- Smith, H.M., Wake, D.B. (1993): Case 2868. Hydromantes ferentiation, albumin evolution, and their biogeographic Gistel, 1848 (Amphibia, Caudata): proposed designation implications in plethodontid salamanders of California of Salamandra genei Temminck & Schlegel, 1838 as the and southern Europe. Evolution 32: 529-539. type species. Bull. Zool. Nomencl. 50: 219-223. Smith, H.M., Wake, D.B., Jennings, M.R. (1995): Comment on the proposed conservation of Hydromantes Gistel, Received: March 27, 2004. Accepted: July 12, 2004. 1848 (Amphibia, Caudata) by the designation of Sala- mandra genei Temminck & Schlegel, 1838 as the type species. Bull. Zool. Nomencl. 52: 267-269. Smith, H.M., Wake, D.B., Jennings, M.R. (1996): Com- ments on the proposed conservation of Hydromantes