Amphibia-Reptilia 34 (2013): 323-336

The enigmatic history of the European, Asian and Americanplethodontid salamanders

David B. Wake∗

Abstract. Recently published research addressing the question of relationships and biogeography of European plethodontidsalamanders has refined time estimates for divergence from American relatives. The recently discovered Korean plethodontidKarsenia is either the sister-taxon of Hydromantes (which has members in Europe and California), or a close relative andco-member of a larger clade that originated in western North America, not eastern North America as formerly thought. Thenew information strengthens the biogeographical hypothesis that Hydromantes entered Eurasia via the Bering Land Bridge.Arguments are made favoring the placement of European and American relatives in a genus Hydromantes, with an Americanclade (subgenus Hydromantes) and a European clade (subgenera Atylodes and Speleomantes).

Keywords: Atylodes, biogeography, Hydromantes, morphology, paleogeography, phylogeny, Speleomantes, taxonomy.

Introduction

When the clade of salamanders today bearingthe name Plethodontidae was first recognizedand named by Gray (1850), it contained speciesin both Europe and North America. With thepassage of time, more and more plethodontidswere found in North America, and then theAmerican tropics. The European species, al-ways few in number in comparison to Americanrelatives, were characterized as having a freelyprojectile tongue and five toes. They were as-signed to Geotriton by Gray (1850) (Geotritonlater was shown by Dunn, 1923, to be based on asalamandrid and, hence, invalid), and Americanspecies with similar traits were placed in Speler-pes (later found to be a junior synonym of Eu-rycea; Stejneger and Barbour, 1917). A periodof taxonomic instability ensued until Strauch(1870) placed European species and Americanspecies that had five toes and a projectile tonguein Spelerpes. This taxonomy was adopted in theinfluential catalogue of Boulenger (1882), butsome workers, including Cope (1889), placedspecies with five toes, partially webbed hands

Department of Integrative Biology and Museum of Ver-tebrate Zoology, University of California, Berkeley, CA,USA 94720-3160∗Corresponding author; e-mail: wakelab@berkeley.edu

and feet, a projectile tongue, and two premaxil-lary bones back into Geotriton. Cope remarkedon the curious fact that his Geotriton was theonly member of a very distinctive and well-marked family that occurred in Europe.

A big change occurred when Camp (1916)described a new species of Spelerpes from thehigh Sierra Nevada (10 800 ft [3292 m]) ofCalifornia. Dunn (1923) coined Hydromantesas a replacement name for Geotriton, assignedCamp’s species as the only American repre-sentative, and thereby established the fact thatthat genus had a remarkable distribution, twospecies in the central Mediterranean region ofEurope and one at the heights of the SierraNevada of California.

Dunn (1926) thought that Hydromantes itali-cus was the “most primitive” species of thegenus, and that Hydromantes genei was “per-haps closer” to H. platycephalus (see fig. 1) thanto H. italicus. He hypothesized that the genushad once been more widely distributed in Eu-rope, and that it had recently become extinct onCorsica. Dunn proposed that continental glacia-tion and the development of “east-west moun-tain systems” together were the cause of Euro-pean extinctions. Furthermore, he hypothesizedthat Hydromantes had come to Europe throughthe north, by way of Greenland and Iceland.

© Koninklijke Brill NV, Leiden, 2013. DOI:10.1163/15685381-00002893

324 D.B. Wake

Figure 1. Adult cave salamander from California (Hydromantes platycephalus). Photo by Sean Rovito. This figure ispublished in colour in the online version.

Early in my career I noted the followingstatement in the then new book by Darlington(1957, p. 163): “The Hydromantes in Europeis presumably a relict, surviving from a timewhen plethodontids were widely distributed inEurasia”. Darlington also noted that herpetolo-gists “apparently agreed” that the European andAmerican species were congeneric. This stimu-lated me to investigate the zoogeography of thePlethodontidae, a topic that continues to be a fo-cus of research in my laboratory.

It did not take me long to encounter the workof Benedetto Lanza, whose work on Hydro-mantes first started to appear in the mid-1940s.Through the years Dr. Lanza produced manypapers dealing with European Hydromantes,culminating in such works as the monographdealing with morphological and genetic studies(Lanza et al., 1995) and the masterful summaryof virtually everything known up to the timeof publication on the European species (Lanzaet al., 2006 [2005]). However, at the time ofthe latter publication, the first Asian plethodon-tid, Karsenia koreana, had just been described(Min et al., 2005), and the subsequent studies ofthat species and Hydromantes, especially new

molecular work, were not available. Here I in-corporate new information concerning Califor-nian and Asian species, summarize informationpublished since 2006, and present my views ontopics ranging from phylogeny and morphologyto taxonomy and biogeography.

Phylogenetics

When Gray (1850) named the Plethodontidae heincluded within it species currently consideredplethodontids from the Americas, Hydromantes(then Geotriton) from Europe, but also somepresent-day ambystomatids and hynobiids. Var-ious familial arrangements were proposed, butfollowing Dunn (1926), the current taxon-omy has held, with his Hydromantes includ-ing two European species as well as the rela-tively recently described and still poorly known(only from two specimens at that time) Hydro-mantes platycephalus. Cope (1889) recognizedtwo main divisions of plethodontids, Plethodon-tae (Plethodon, Hemidactylium, Batrachoseps,Stereochilus, and Autodax [= present-day Anei-des]) and Spelerpae (Geotriton [= present-day Hydromantes], Gyrinophilus, Manculus

Plethodontid salamander history 325

[= present-day Eurycea, in part], Spelerpes[= most species of present-day Eurycea,Pseudotriton and some tropical species,mainly present-day Pseudoeurycea], Oedipus[= present-day tropical salamanders in severalgenera], and Oedipina). This suggested rela-tionship of Hydromantes was based principallyon the presence in all species of a freely pro-jectile tongue. Dunn (1926) placed all tropi-cal plethodontids in Oedipus, and it and Hy-dromantes were included in his free-tonguedEurycea group. Oedipus was shown to be apreoccupied name by Taylor (1940), who sub-stituted Bolitoglossa, and later Taylor (1944)began the dismantling of Bolitoglossa into anumber of genera (currently 12; Wake, 2012).Tanner (1952) undertook a comparative studyof the hyobranchial musculature of tropicalsalamanders and compared them with Hydro-mantes. One conclusion was that Hydromantesseemed to be a close relative of Bolitoglossa andMagnadigita (the latter today recognized as asubgenus of Bolitoglossa; Wake, 2012). In myfirst contribution to this question (Wake, 1966),Hydromantes was considered to be a relative ofthe tropical clade and of Batrachoseps (fromwestern North America), with Hydromantes en-visioned as a sister-taxon of the other two taxa.These relationships appeared to be well sup-ported by morphological data, and the same re-lationship was found by Lombard and Wake(1986). However, this hypothesis required ex-tensive homoplasy, and even the freely projec-tile tongue and the partially to fully webbeddigits, previously the main reasons for associat-ing Hydromantes and the tropical genera, werefound to be convergently evolved.

No one seemed to question that the Amer-ican species and the European species of Hy-dromantes were close relatives. For example,Adams (1942) made detailed comparisons ofthe cranial osteology and head region muscula-ture of H. genei and H. platycephalus. He con-cluded that the two species were “alike” in oste-ology (but see below), and that while there weregreat similarities in musculature, there were suf-

ficient differences to indicate that species sta-tus was warranted. This was the first detaileddemonstration of the close similarity of the Eu-ropean and American species of Hydromantes.With respect to morphology, the species of Hy-dromantes possessed many unique features thatstrongly suggested that they were phylogenti-cally close relatives.

Subsequent studies only served to substan-tiate Adams’ conclusions. My doctoral disser-tation (see Wake, 1966) treated the compara-tive osteology of Plethodontidae, sampling H.brunus, H. genei, H. italicus, H. platycephalus,and H. shastae. While noting a few differ-ences between the American and Europeanspecies, those species shared many derived fea-tures and they were placed in a supergenusHydromantes, together with a supergenus Ba-trachoseps and a supergenus Bolitoglossa (forthe then-recognized seven genera of neotropicalplethodontids), with Hydromantes as the sister-taxon to a clade constituted of the other two.A detailed assessment of the tongue and as-sociated structures (Lombard and Wake, 1977,1986) showed the species of Hydromantes todiffer dramatically from all other plethodon-tids in many aspects of tongue morphology. So,on abundant morphological grounds, Europeanspecies of Hydromantes are not only plethodon-tids (they have all of the diagnostic charactersof the family, including lunglessness), but areclose phylogenetic relatives of the three Ameri-can species.

The era of biochemical systematics beganin earnest in the 1970s, when such methodsas electrophoretic analysis of allozyme vari-ation and immunological approaches such asmicro-complement fixation came into generaluse. Both of these methods were used by Wakeet al. (1978) to study Hydromantes. The al-lozyme data showed small genetic distancesamong American species (maximum Nei D of0.553) but the two European species studied,H. genei and H. italicus, differed greatly (NeiD = 1.135). The difference between the Euro-pean and American species was even greater,

326 D.B. Wake

between 1.276 and 1.399. Immunological dis-tances among the American species were low,between 0 and 9, whereas distances to the Euro-pean species were 47 and 48. In contrast, im-munological distances to outgroup taxa (twospecies of Batrachoseps and three neotropicalplethodontids) were from 75 to 105. In com-bination, these data supported the inferences ofrelationships from morphology. However, a sur-prise was the discovery that the Sardinean H.genei was greatly differentiated from the main-land H. italicus. Subsequent studies by Italianworkers (Lanza et al., 1986, 1995; Nascetti etal., 1996) using more allozymes and refinedmethods revealed even higher levels of varia-tion between European and American salaman-ders, and Lanza et al. (1986) showed large dif-ferences between H. genei and the other Eu-ropean species. Furthermore, they showed thatSardinean forms other than H. genei were closerrelatives of the mainland species than to H.genei. In addition to describing a new Sardineanspecies, they raised former subspecies of H.genei to full species rank.

With the advent of DNA sequencing, the rela-tionships of Hydromantes were re-investigated,always with the goal of determining whetherthe European species and American speciesof the genus were truly more closely relatedto each other than to members of other taxa.Jackman et al. (1997) obtained 555 basepairsof the mitochondrial gene cytochrome b fromsamples of Hydromantes (one sample each offour European species, three from Sardinia andH. italicus; five samples of the three Ameri-can species) and Batrachoseps (five samples ofthree species of subgenus Batrachoseps; threesamples of three species of subgenus Plethop-sis), as well as samples of Bolitoglossa, Anei-des, Plethodon, and Aneides. The most im-portant result is that European and Ameri-can species of Hydromantes were each other’sclosest relatives. Furthermore, and surprisingly,the differences between the two groups wereless than between the two subgenera of Ba-trachoseps (which occur in Oregon, Califor-

nia, and Baja California Norte in western NorthAmerica). But another unremarked result wasthat Batrachoseps and Bolitoglossa did notform the sister taxon of Hydromantes. With re-spect to genetic distances (Kimura 2 parameter),Hydromantes and either Batrachoseps (0.178-0.252) or Bolitoglossa (0.191-0.242) tended tobe more differentiated than members of thetribe Plethodontini (0.142-0.222), and the phy-logenetic analysis found ambiguity with respectto the closest relative of Hydromantes. Theseresults served notice that the long-maintainedview that Hydromantes, Batrachoseps and thetropical species (supergenus Bolitoglossa) forma clade should be tested.

The first strong evidence that Hydromanteswas not a bolitoglossine came from analysisof complete mitochondrial genes (Mueller etal., 2004). While the two species of Hydro-mantes studied (the American H. brunus andthe European H. italicus) formed a stronglysupported clade, it was nested within a cladecontaining Aneides, Desmognathus, Ensatina,Phaeognathus, and Plethodon. There were threemajor surprises in this result: 1. The long-standing view that desmognathines formed asister-taxon to other plethodontids was rejected(a result confirmed by Chippindale et al. [2004]using a nuclear gene [Rag1], portions of twomitochondrial genes, and traditional morpho-logical characters; they did not study Hydro-mantes); 2. Desmognathus and Phaeognathuswere nested within the plethodonines (mem-bers of the tribe Plethodontini – Aneides, En-satina and Plethodon); 3. Hydromantes was alsonested within the plethodonines with high sta-tistical confidence, and its closest relative wasAneides (although this result had low statisticalconfidence).

When Min et al. (2005) announced the dis-covery of the first Asian plethodontid, Karse-nia from Korea, they included the new formin a phylogenetic analysis based on the nu-clear gene Rag1. Both were members of aclade that included Aneides, Desmognathus,Ensatina, Phaeognathus and Plethodon, with

Plethodontid salamander history 327

high statistical support; Hydromantes was foundto be sister to Ensatina, but with low statisticalsupport.

Roelants et al. (2007) studied one mito-chondrial and four nuclear genes in a subsetof plethodontids that included both American(H. platycephalus) and European (H. italicus)species. Among relevant taxa they had onlyEnsatina, Desmognathus, and Plethodon, butagain Hydromantes was found to be mono-phyletic and to be nested within the plethodo-nine + desmognathine clade, as a sister-taxon ofa Desmognathus + Ensatina clade (with weakstatistical support for both relationships).

This study was followed by that of Vieiteset al. (2007), which used three nuclear genes;they again found that Hydromantes and Karse-nia were nested within the plethodonines +desmognathines, with high statistical support.Hydromantes and Karsenia were found to besister-taxa, and in turn to form a sister-taxonrelationship with a clade including Aneides,Desmognathus, and Ensatina. Plethodon wasthe sister to the combined clade of the otherspecies.

A complete mitochondrial genome of Karse-nia and data for three nuclear genes were addedby Vieites et al. (2011). The results supportthe earlier molecular work in finding a mono-phyletic Hydromantes, two major clades ofplethodontids, and inclusion of Hydromantes inthe subfamily Plethodontinae. There is also sta-tistical support for a sister-taxon relationship ofHydromantes and Karsenia, and this clade issister to a clade including Aneides, Desmog-nathus, Ensatina and Phaeognathus. Plethodonis the sister-taxon of all other plethodontines.

Pyron and Wiens (2011) added no new datafor plethodontids, but included data from Gen-Bank for nine nuclear and three mitochondrialgenes and included all taxa for which datawere available. However, complete data werenot available for any taxon, and some taxa wererepresented by as little as 3% of the possible to-tal of 12 712 basepairs. The mitochondrial gene16S was available, at least in part, for 90%

of the taxa, but 10 of the genes were avail-able, in part, from as many as 43% of the taxato as few as 6%. Despite its limitations, thiswork contains the most comprehensive analy-sis of amphibian relationships. Important find-ings include: 1. Hydromantes is monophyletic;2. Hydromantes is the sister-taxon of a cladethat includes Aneides, Ensatina, Desmognathus,Karsenia, Phaeognathus and Plethodon. Thesetaxa constitute the subfamily Plethodontinae.However, it must be kept in mind that they didnot include the majority of available data for themitochondrial genome (Mueller et al., 2004).

Some questions remain concerning the rela-tionships of Hydromantes to other plethodon-tines, but the closest relationship with the bestsupport to date is with Karsenia. These ques-tions doubtless will be pursued using rapidly de-veloping next generation sequencing methods toobtain enlarged databases.

Morphological, ecological and behavioralcomparisons

Lanza et al. (2006 [2005]) usefully summarizedinformation concerning the biology of Euro-pean Hydromantes and also included referencesto the American species. I will build on thisfoundation. Vastly more information is avail-able for the European than for the Americanspecies, which remain poorly known biologi-cally, largely because they are, in general, lesscommon and more difficult to study than the Eu-ropean species.

The great morphological similarity betweenEuropean and American species was docu-mented by Adams (1942), whose work was notcited by Lanza et al. (2006 [2005]). The headmorphology, including the skull and muscula-ture, of H. platycephalus was compared withthat of H. genei. While Adams’ intent was toshow that the species differed and that speciesstatus was warranted, his main result was thedemonstration that the two species closely re-semble each other and differ only in relativelyminor details. For example, the skull is shorter

328 D.B. Wake

and flatter in male H. platycephalus than inH. genei, and there are a few minor differ-ences in the origin and insertion of muscles. Therelatively poorly developed skull of H. platy-cephalus and especially its much larger cra-nial fontanelle are illustrated but not mentioned.Furthermore, the elongated pars frontalis of themaxilla in H. platycephalus and the contrastinglow profile of the process in H. genei are illus-trated. Also shown are elongated teeth that ex-tend laterally out of the mouth and beyond themargins of the head in male H. platycephalus.These are derived morphological traits thatcharacterize the American species and distin-guish them from the European species. Sep-tomaxillary bones are always present in Amer-ican species, but may be absent in some spec-imens in some but not all of the Europeanspecies. Among the notable derived similaritiesare the absence of prefrontal bones of the skull,the presence of long maxillaries, and a wide gapbetween the paravomerine tooth patches and theanterior vomerine teeth.

In contrast to the close similarity of the Eu-ropean and American Hydromantes, Karseniadiffers dramatically from both groups and moreclosely resembles other American genera, espe-cially Plethodon, because Karsenia retains thegeneralized morphology inferred for the fam-ily as a whole (Buckley et al., 2010). The skullof Hydromantes is weakly ossified and flat-tened, with incomplete articulations, relative tomost members of the subfamily Plethodonti-dae, whereas Karsenia, also a plethodontine,has a relatively well ossified, domed skull char-acterized by strong jaws. The genera differ dra-matically with respect to the tongue and hy-obranchial apparatus. Karsenia has a tonguesimilar to those of Plethodon and Aneides,whereas that of Hydromantes is the most spe-cialized of all salamanders (Lombard and Wake,1977; Deban et al., 1997). In short, nothing inthe osteology or general morphology of Karse-nia suggests that it is a close relative of Hydro-mantes.

The European and American species of Hy-dromantes, while overwhelmingly similar inmorphology, do differ in some respects, as notedabove (see also Wake, 1966; Lanza and Vanni,1981). In addition, the trunks of the Europeanspecies are slightly shorter than those of theAmerican species, the consequence of havingon average fewer vertebrae (mode 13 vs. mode14; Lanza et al., 1995). The vertebrae bear trans-verse processes that separate distally on the firstfew vertebrae of all species, but after the fourthvertebrae in the European species the trans-verse processes are fused and become reducedin length, whereas in the American species theyremain separated. The central and posterior ribsof the European species are unicipital, whereasthose of the American species retain the ances-tral bicipital anatomy (this is another way ofpresenting the information in the preceding sen-tence). The tails of American species are bluntlytipped whereas those of European species aremore sharply tipped and a little longer. Basal tailautotomy does not occur in Hydromantes, al-though tails are known to break near their tips inthe European species. American species of Hy-dromantes are well known for using their tailsin locomotion, in the manner of a fifth leg, es-pecially when walking on smooth or wet slopingsurfaces, and they have specialized tail tip cells(Serra et al., 1991); this behavior is not knownin the European species. Differences in tail mus-culature have been reported (Serra and Stefani,1974), but no detailed comparative analysis hasbeen conducted.

Hydromantes has 14 pairs of chromosomes(as in most plethodontids) but the Europeanspecies differ from the American in some de-tails (e.g., they have a more asymmetrical 14th

chromosome), and H. (A.) genei differs fromother European species in some respects (it andthe American species lack XY sex chromo-somes), but in most respects all species havesimilar karyotypes (in having all biarmed chro-mosomes) (Nardi, 1991; Sessions and Kezer,1991).

Plethodontid salamander history 329

Taxonomy

While there is little discussion of which speciestaxa of Hydromantes should be recognized,there is controversy over which generic namesshould be applied.

All agree that Hydromantes is a plethodontid,and all recent molecular phylogenetic analysesindicate that it is allied with taxa in the subfam-ily Plethodontidae. Recently Wake (2012) for-mally named a tribe Hydromantini to containHydromantes and Karsenia. Beyond this thereis some controversy. However, I will argue infavor of the following classification:

Family PlethodontidaeSubfamily Plethodontinae

Tribe HydromantiniGenus Hydromantes Gistel, 1848

Subgenus Hydromantes Gistel, 1838Species: platycephalus (Camp,

1916); brunus Gorman, 1954;shastae Gorman & Camp, 1953

Subgenus Atylodes Gistel, 1868Species: genei (Temminck & Schle-

gel, 1838)Subgenus Speleomantes Dubois, 1984

Species: italicus, Dunn, 1923; am-brosii, Lanza, 1955; flavus, Ste-fani, 1969; imperialis, Stefani,1969; sarrabusensis (Lanza,Leo, Forti, Cimmaruata, Capu-to, & Nascetti, 2001); strinatii,Aellen, 1958; supramontis, Lan-za, Nascetti, & Bullini, 1986.

This taxonomy (Wake, 2012) is followed bythe Amphibian Species of the World (Frost,2013) and the AmphibiaWeb (AmphibiaWeb,2013) websites. The taxonomic history of Hy-dromantes has been treated by Dubois (1984),Wake et al. (2005), and Lanza et al. (2006[2005]), and is abbreviated here. A confusingearly history ended when Dunn (1923) replacedthe invalid name Geotriton with Hydromantes,and named the mainland Italian species, whichcuriously had been without a legal name, as Hy-dromantes italicus. For many years there was

agreement that European and American specieswere congeneric until Lanza and Vanni (1981)proposed splitting the genus, placing the Amer-ican species in a new genus Hydromantoides;type species platycephalus. Dubois (1984) wasconcerned with procedures followed by Dunnand proposed a single genus with two subgen-era, the American species being assigned to Hy-dromantoides (Hydromantoides) and the Euro-pean species being assigned to Hydromantoides(Speleomantes); type species italicus. The In-ternational Commission on Zoological Nomen-clature (1997) ultimately resolved this mat-ter by changing the type species of Hydro-mantes to platycephalus, thereby rendering Hy-dromantoides a strict junior synonym. Wake etal. (2005) resurrected Atylodes as a subgenericname for genei and suggested that if Europeanspecies were to be considered a separate genusor subgenus, the appropriate name is Atylodes,but Crochet (2007) argued in favor of Speleo-mantes and his argument has been accepted bySpeybroeck et al. (2010), who recommendedagainst use of Atylodes at any level (see below).

Currently, there are five alternative, equallyvalid taxonomic options in my view:

1. Recognize no subgenera and place allof the species in Hydromantes. This is acommonly used option in general texts.

2. Recognize a genus Hydromantes, withtwo subgenera, Hydromantes for theAmerican species and Speleomantes forthe European species.

3. Recognize three subgenera of Hydro-mantes: Hydromantes, Speleomantes,Atylodes.

4. Recognize two genera, with two subgen-era of Speleomantes, Speleomantes andAtylodes.

5. Recognize three genera.In the following, I treat each of these options:

1. The monophyly of Hydromantes is nolonger questioned. I recommend thisoption for authors whose work dealswith fields such as physiology, develop-

330 D.B. Wake

ment, anatomy and functional morphol-ogy, and biomechanics.

2. While clearly forming a clade, Europeanand American species do differ in al-lozymes, DNA sequences, and in someanatomical and behavioral details. Torecognize this by using subgenera is ap-propriate, and this is a taxonomy thatI find acceptable.

3. A case can be made that H. genei dif-fers in substantive ways from other Eu-ropean species in some morphologicaland cytological details, as well as inallozymes, but some ambiguity existswith respect to support for two Europeanclades in the available DNA sequencedata (van der Meijden et al., 2009). Thisis the taxonomy I prefer and recom-mend.

4. My arguments for rejecting this optionare essentially the same as for option 5,below.

5. The fundamental reason for the ini-tial split of Hydromantes by Lanza andVanni (1981) was their suspicion thatEuropean and American clades had beenconvergently derived. Substantial evi-dence of monophyly has been obtainedfrom mitochondrial and nuclear genesequences, and by 2006, even Lanzaet al. (2006 [2005], p. 30) largely, butnot completely, conceded: “Almost cer-tainly Speleomantes and Hydromantesbelong to a monophyletic supergenus(Hydromantes), although a very remotepossibility exists that it may be poly-phyletic –”.

Although my support for option 3 and rejec-tion of options 4 and 5 may seem to devolveto a hollow argument over ranks, I think moreimportant issues are at stake. I would like tobe able to derive phylogenetic information fromtaxonomic ranks, without resorting to an alter-native, non-Linnean taxonomic system. One ef-fective way of attaining such a goal is throughthe use of subgenera. I think this is especially ef-

fective when there is strong evidence of mono-phyly from diverse sets of biologically signifi-cant traits. I will present three case studies fromPlethodontidae.

Bolitoglossa contains more species than allthe members in any other family of salamanders(at present, 128). The taxon has distinctive oste-ology and external morphology (e.g., all specieshave partially to fully webbed digits) and isimmediately identifiable in the field. It has aunique tongue that is one of the most specializedin the Bolitoglossini. Bolitoglossa is always dif-ferentiated in DNA sequences, and Parra-Oleaet al. (2004) recognized seven subgenera. Whilethese are based primarily on molecular data,there is some supporting morphological data,and most of subgenera have unique distribu-tions. However, there are some questions aboutthe monophyly of at least two of the subgenera(Mayamandra, Pachymandra). In short, there isno reason break up this genus at this time, andgood reasons not to do so.

Batrachoseps is a relatively speciose (21-22 species) group of plethodontid species fromthe west coastal region of North America. Thespecies are immediately identifiable in the fieldby having only four digits on the hind limb andby being slender, with long tails. They have aunique tongue, and they differ from all excepttropical plethodontids in having only 13 pairs ofchromosomes. Based on some osteological de-tails, allozymes and DNA sequences, two cladesare recognized; these were treated as subgeneraby Jackman et al. (1997) and subsequent au-thors. The DNA sequence differences are thesame magnitude as those separating Europeanand American species of Hydromantes (Vieiteset al., 2007, 2011).

Oedipina is a deeply tropical clade of 36species. Species are immediately identifiablebecause they are slender with elongate bodies(four or more trunk vertebrae than any othertropical salamander) and long, slender tails,with short to diminutive limbs. Three cladeshave been identified using DNA sequences, butonly one of them has morphological characters

Plethodontid salamander history 331

and even those are somewhat equivocal. Ac-cordingly, the three clades have been assignedto three subgenera.

In each of these cases the depth of diver-gence, measured by DNA sequences, is roughlyequivalent to that between European and Ameri-can species of Hydromantes, and there are somemorphological characters. Yet, the clades shareso much in common that all interests are servedby using a subgeneric classification. Hydro-mantes is a fourth instance. However, in the caseof Hydromantes the degree of shared special-ization and high level of synapomorphic mor-phology and behavior is even greater than inthe other three cases. Furthermore, the very factthat the clade is present in Europe and westernNorth America and presents a unique zoogeo-graphic enigma for salamanders argues in favorof retaining a single genus for these species. Thetaxonomy draws attention to the puzzle and el-evates its significance, spurring action in searchof a solution to the question as to how this dis-tribution can be explained.

Biogeography

Hydromantes is a biogeographic enigma amongsalamanders, but there are some informativecomparisons to be made with other amphib-ians. Holarctic distributions are not unusual;Rana and bufonids are two notable examples.The western North American Rana are mem-bers of a clade widespread in Eurasia, and NorthAmerican bufonids are closely related (althoughno longer considered congeneric) with Eurasiantoads. Salamandrids are represented in bothNorth America and Eurasia, and proteids arefound in Europe and North America (but theproteid split is much older than the others –Early Cretaceous [Zhang and Wake, 2009]).What is unique about the plethodontids is repre-sentation in Korea and the Sardinian and Italianmainland-SE France, and nowhere else in Eura-sia.

Even before discovery of Karsenia there wascontroversy over the biogeographic history of

Hydromantes. Acceptance that Hydromantes isa clade and the availability of time trees ad-vances us beyond the analysis of Lanza etal. (2006 [2005]), which concluded that whileKarsenia may well have dispersed from west-ern North America via a Beringian connec-tion, Hydromantes was likely to have arrivedat its present distribution as a result of a vi-cariant event following break-up of the NorthAmerican-European connection via Greenland.Delfino et al. (2006 [2005]) also discussed whatthey term the “Hydromantes problem”, conclud-ing that direct spread from North America ontoEurope via a North Atlantic connection anda subsequent break-up of the land connection“was less unlikely than a dispersal requiringthe crossing of the Beringian Bridge and thewhole of Asia” (p. 57) (note that this was writ-ten before the discovery of the Asian Karsenia).Lanza et al. (2006 [2005]) do discuss Karsenia,but are not convinced that it has much to offerwith respect to understanding the biogeographichistory of Hydromantes. What most concernsboth sets of authors is the absence of plethod-ontids across vast stretches of Eurasia and nofossil record (although Delfino et al. note thatplethodontid fossils are, in general, rare and rel-atively recent).

Time trees are now available for the NorthAmerican-European divergence of salaman-drids and plethodontids. Available evidencesuggests a divergence of about 60-70 MYA(Zhang et al., 2008; Vieites et al., unpublisheddata). However, this is not a “clean” separa-tion of Europe and America, but of Eurasia andAmerica, because the eastern Asian salaman-drids (Cynops, Laotriton, Pachytriton, Parame-sotriton) are nested internally within the cladeof modern European newts, which in turn isthe sister clade to the North American ge-nera (Notopthalmus, Taricha). In contrast to thelong separation of Karsenia + Hydromantesfrom other plethodontids (see below), the di-vergence of European and American Hydro-mantes is dated at about 41 MYA (Vieites et al.,2007). Available molecular evidence suggests

332 D.B. Wake

that Karsenia and Hydromantes are sister taxa(Vieites et al., 2007, 2011), but some analyticaltreatments of the data, especially those that useno mitochondrial sequences (some treatments inVieites et al., 2011) or only a fraction of theavailable mitochondrial sequences (Pyron andWiens, 2011) do not find support for such aclade. Assume, for the moment, that the rela-tionship is real. The estimated time of diver-gence of Karsenia + Hydromantes in relation tothe other plethodontines is 74-77 MYA, a littleearlier than the estimated age of the salaman-drid split (the error estimates overlap). The es-timate of the divergence of Karsenia from Hy-dromantes is 67-69 MYA (Vieites et al., 2007).

These time estimates led Vieites et al. (2007)to propose a biogeographic scenario in whicha common ancestor of Karsenia + Hydro-mantes dispersed from western North Amer-ica to Eurasia. The Western Interior Seawayseparated eastern from western North Americafrom the mid-Cretaceous well into Paleoceneand was likely responsible for the origin of thetwo main plethodontid clades (plethodontinesin the west and hemidactyliines in the east).When the dispersal to Asia began (Late Creta-ceous), the earth was warm and the salamanderswould have lived far north, where distances be-tween continents are relatively short. The Tur-gai Sea separated Asia from Europe at the time,and it was continuous with the Western InteriorSeaway in North America. The split betweenKarsenia and Hydromantes took place near theend of Cretaceous. A long period of evolutionof Hydromantes ensued, during which time itevolved its many morphological and behavioralspecializations, followed by a split between theH. (Atylodes + Speleomantes) clade and the H.(Hydromantes) clade, the former (which retainsmore ancestral traits) dispersing west to Europefollowing closure of the Turgai Sea, and the lat-ter dispersing back into North America, leavingno trace in eastern Asia. The split between thetwo European clades is dated at 16-17 MYA,whereas the first split in North America wasmore recent (ca. 8 MYR). The only relevant fos-

sil, a trunk vertebra (diagnosable as H. (Speleo-mantes) sp. from Slovakia) is dated at 13.75 Ma(±1.25 Ma) (Venczel and Sanchíz, 2005), a datecompatible with the dates obtained from analy-ses of molecular data (for detailed analysis seeVieites et al., 2007).

The paleogeography of the northern regionsof Earth is undergoing nearly constant revi-sion (e.g., Jones, 2011). Three possible landbridges are relevant to the discussion of his-torical biogeography of Hydromantes: BeringLand Bridge, Thulean Land Bridge and DeGeer Land Bridge. One must keep in mind thatthere is much circularity in interpreting the ev-idence for and against land bridges at particu-lar times. Distributions of organisms, usuallyland mammals, “demand” that a dispersal routehave been present, and the geological evidenceis sought. Thus the paleogeographic reconstruc-tions are based on some amalgam of distri-butional and geological evidence. The BeringLand Bridge is widely accepted as having beenin existence at least (although perhaps intermit-tently at first) from the Late Cretaceous (ca.100-65 Ma) well into the Oligocene. VariousAmerican mammals are thought to have dis-persed into Eurasia via this bridge from theEarly Eocene into the Early Oligocene (ca. 34-28 Ma); additional dispersals are postulated forLate Oligocene to earliest Miocene (28-20 Ma),and Late Early to early Middle Miocene (20-14 Ma) (Briggs, 1995; Eberle and Greenwood,2012). The bridge was again in place whenthree-toed horses dispersed from America intoEurasia and Africa in the Vallesian EuropeanLand Mammal Age (Miocene; 11-9 Ma).

In contrast to the dating of the Bering route,the Thulian Land Bridge is thought to have beenan intermittent connection across the North At-lantic (North America to Greenland, Iceland,the Faeroes to Scotland) only in the EarlyEocene (Eberle and Greenwood, 2012). A DeGeer Land Bridge, further to the north, thoughtto have connected North America throughGreenland and Svalbard to present-day north-ern Norway, is more problematic. There are

Plethodontid salamander history 333

significant problems with both possible bridges(summarized by Jones, 2011), not the least ofwhich is the high probability of some deep sea-ways (hundreds of meters in depth!) at pointsin both the Thulian and De Geer bridges. How-ever, there is some new evidence that a short-lived Thulian Bridge was in place 55-53.5 Ma(earliest Eocene; Jones, 2011), although Storeyet al. (2007) argue on the basis of radiometricdates, that the opening of the northeast Atlantictook place 55.5 (± 0.5 Ma). There is, in gen-eral, far less evidence of the Thulian and DeGeer bridges than of the Bering Bridge, and theyappear to have been intermittent and relativelyshort-lived, which would hardly have been fa-vorable for the dispersal of salamanders.

From the above data, I conclude that thelikeliest scenario for the current disjunct dis-tribution of Hydromantes is that salamandersdispersed by way of the Bering Land Bridgeand reached Europe sometime following theclosure of the Turgai Strait (also known asthe Obik Sea). That seaway connected thePeri-Tethyan basins, the West Siberian Bo-real basins and the Western Interior Seawayin North America, producing a landmass inwestern North America/eastern Eurasia, wherethe ancestors of Hydromantes (or of Hydro-mantes and Karsenia) originated (for discus-sion of the once-favored Appalachian origin ofplethodontids, see Mueller et al., 2004; Vieiteset al., 2007). The Turgai Strait closed start-ing in the Late Eocene or Oligocene, when thetwo major clades of Hydromantes had alreadydiverged; the clade retaining the greater num-ber of ancestral morphological and behavioraltraits was then able to move westward into cen-tral/southern Europe, where they certainly werepresent as early as 13.75 Ma (Miocene). Thereare problems with any postulated history, butI think there are fewer with this one than withothers. For example, the estimated 41 Ma sep-aration of European and American clades ofHydromantes fits well with the likely existenceof a broad and long-lasting Bering Bridge, that

seems to have persisted from at least the LateCretaceous well into the Miocene.

The alternative route, favored by Delfino etal. (2006 [2005]), Lanza et al. (2006 [2005]),and Lanza et al. (2009), is based on use of eitherthe Thulian or De Geer bridges, which were lesslong lasting than the Bering Bridge, and far lesswell-documented. Furthermore they were sepa-rated from the western North American place oflikely origin of a Karsenia + Hydromantes an-cestral clade, or a Hydromantes ancestral clade,by the Western Interior Seaway. These authorswere writing when it was still thought that theEuropean and American clades of Hydromanteshad separated 28 Ma (Wake et al., 1978) or50 Ma (Lanza and Vanni, 1981), rather than thenew estimate of 41 Ma and the much older esti-mate of 74-77 Ma for Karsenia + Hydromantes.Furthermore, the 41 Ma timing estimate for thedivergence within Hydromantes is considerablymore recent than the radiometrically determinedopening of the North Atlantic (55.5 Ma; Storeyet al., 2007).

The two amphibian taxa most relevant forcontributing some understanding of plethodon-tid history are the newts, Salamandridae (Pleu-rodelinae), and the ranid frogs of the genusRana (which I recognize as containing twosubgenera, Rana in western North Americaand across northern Eurasia, and Lithobates,mainly central and eastern North America intothe tropics as far as Bolivia). I earlier notedthat the age of separation of the North Amer-ican from the Eurasian salamandrids is 60-70 Ma, which times span the uppermost Creta-ceous to the mid-Paleocene. The salamandridsmost likely moved eastward into North Amer-ica across the Bering Bridge, while plethodon-tids initially moved from westward into Asiaacross the same bridge, although perhaps a lit-tler earlier. Bossuyt et al. (2006), using molec-ular phylogenetic inferences, estimate that an-cestral Rana began differentiating on the orderof 31-32 Ma, in Early Oligocene, while the sep-aration of Rana (Rana) and Rana (Lithobates)dates to about 21-22 Ma, Early Miocene. The

334 D.B. Wake

ranids underwent a major divergence in NorthAmerica, and the ancestors of Rana (Rana) dis-persed westward back into Eurasia, leaving asmall part of that clade and all of R. (Litho-bates) behind. The first Rana appear in theEuropean fossil record in Late Eocene (lowerHeadonian stage, standard level MP 16; Rageand Rocek, 2003, Rage, 2012). According tothe latest estimates (International Commissionon Stratigraphy, 2013), the age of this recordis between 38-41 Ma, which is difficult to rec-oncile with the molecular timing estimate andthe Bossyut et al. (2006) scenario. Perhaps an-cestral Rana were present earlier than estimatedin Europe, and they may have made their wayinto North America at about the same time(sometime a little more recent than 41 Ma)that H. (Hydromantes) was moving east. How-ever, the Bering Land Bridge was present atvarious times from the Cretaceous well intothe Tertiary, and was most likely available forplethodontid and salamandrid salamanders be-tween 60-74 Ma and again for ranids and Hy-dromantes in late Eocene to early Oligocene.If the Thulian and De Geer bridges existedat all, they occurred in the Early Eocene, toolate for the salamandrid and plethodontid ini-tial dispersal, and too early for Hydromantesand Rana. Thus, an eastern route from NorthAmerica to Europe for amphibians appears to behighly unlikely because it was short-lived anddid not exist during the times of inferred disper-sals.

Not only are fossil plethodontids rare, butplethodontids themselves are rare in Eurasia.Yet, the existence of a single fossil in theMiocene of Slovakia bears witness to the pre-viously more widespread distribution of Hy-dromantes. The surprisingly recent discoveryof Karsenia in Korea gives hope that otherplethodontids remain to be discovered in thevast reaches across the Eurasian land mass.Each year numerous species of plethodontidsalamanders are discovered and described (seeAmphibiaWeb, 2013), and it will not surpriseme if there are more to be discovered in Asia

that could shed light on the enigma of plethod-ontids in the Old World.

Acknowledgements. Benedetto Lanza has been an inspi-ration to me since I began my work on plethodontid sala-manders and I am pleased to dedicate this paper to him.He showed me how to find Hydromantes near Firenze andwelcomed me into his home, always in a spirit of cordial-ity and generosity, and I am grateful to him. I thank WilliamClemens and Jaelyn Eberle for discussion of Arctic and sub-Arctic paleobiogeography, and Sebastiano Salvidio and An-tonio Romano for answering questions. I thank MarvaleeWake for discussion and comments on the manuscript. Myresearch has long been supported by the National ScienceFoundation.

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Submitted: February 28, 2013. Final revision received:April 16, 2013. Accepted: May 11, 2013.Associated Editor: Sebastian Steinfartz.