Under Construction

This is an archived version of a Tree of Life page. For up-to-date information, please refer to the current version of this page.

Phylogenetic relationships among salamanders of the tribe Plethodontini (Highton and Larson, 1979; Maxson et al, 1979; Larson et al., 1981; Larson, 1984; Highton et al., 1989; Highton, 1991; Wynn et al., 1988).

Containing group: Plethodontidae

Introduction

The plethodontine tribe Plethodontini contains woodland salamanders of the genera Aneides and Plethodon, which occur both in eastern and western North America, and the western North American genus Ensatina. Members of all three genera can be found concealed under logs and rocks on the forest floor, where eggs are laid. These salamanders are completely terrestrial and have no free-living aquatic larval stage. Surface activity is highly seasonal for most species and usually occurs on wet nights.

Members of the genera Ensatina and Plethodon (except Plethodon petraeus) occur primarily on the forest floor and have only limited ability for climbing in low vegetation. Some members of the genus Aneides show greater climbing ability and associated arboreality (most highly developed in Aneides ferreus and Aneides lugubris, see Larson et al., 1981) or use of rock crevices (Aneides aeneus). Morphological changes associated with evolution of climbing in Aneides include lengthening of the limbs and digits, rearrangements of the cartilaginous carpal and tarsal elements, and expansion of terminal phalanges to enhance grasping (Wake, 1963; Larson et al., 1981). Plethodon petraeus (Wynn et al., 1988) demonstrates adaptations for climbing in rock crevices that parallel those of Aneides.

Aneides also demonstrates morphological evolutionary changes that strengthen the jaws, including fusion of premaxillary bones, enlarged unicuspid teeth, dorsoventral expansion of the posterior portion of the maxilla, and rearranged throat musculature (Wake, 1963; Larson et al., 1981: Wake and Larson, 1987). The prominent jaw muscles of Aneides give their head a more massive and triangular appearance relative to the other plethodonine salamanders. These features are often especially pronounced in males. The strengthened jaws and enlarged, sharp teeth of Aneides are used in aggressive encounters among conspecifics (Staub, 1993). When handled, Aneides lugubris occasionally delivers bites that can draw blood but are not seriously dangerous. The strengthened jaws of Aneides have been hypothesized to be adaptations for acquiring food while maintaining a perch in arboreal habitats (Larson et al., 1981).

The salamanders of the genus Ensatina have been used as an example of a ring species (Stebbins, 1949, 1954; Dobzhansky, 1958; Brown, 1974; Wake and Yanev, 1986; Wake et al., 1986, 1989; Moritz et al., 1992; Jackman and Wake, 1994). Populations of Ensatina eschscholtzii demonstrate extensive variation in coloration, forming seven recognized subspecies arranged geographically in a "ring" encircling the central valley of California. Hybridization and intergradation occur between adjacent subspecies in the ring except where coastal and inland populations make contact at the southern end of the geographic range of the species. This geographic pattern is interpreted to illustrate gradual evolution of reproductive barriers between populations, an important component of the formation of species. Because molecular evolutionary studies illustrate extensive genetic differentiation among populations of Ensatina, some systematists prefer to regard this genus as containing multiple species rather than just a single "ring species" (Frost and Hillis, 1990; Highton, 1990).

Geographic variation in reproductive interactions among species is observed also for species in the Plethodon glutinosus group (Highton et al., 1989) and Plethodon cinereus group (Highton, 1972). The amount of genetic differentiation observed among species within these two species groups is less than that observed within the genus Ensatina. A detailed behavioral analysis of the evolution of sexual isolation within the Plethodon glutinosus group is presented by Reagan (1992). Speciation in eastern North American salamanders of the genus Plethodon is reviewed by Highton (1995).

The tribe Plethodontini shows unusually high variation in the mass of DNA in the cell nucleus. The C-value (mass of DNA in a haploid, unreplicated set of chromosomes) has been reported to range from 18 pg to 69 pg in the tribe Plethodontini with the full range being evident within the genus Plethodon (reviewed by Larson, 1984; Sessions and Larson, 1987). Mass of the nuclear genome may be inversely proportional to developmental rates, especially rates of differentiation of regenerating limbs (Sessions and Larson, 1987).

Characteristics

Diagnosis

Plethodonine salamanders are terrestrial woodland salamanders that have no aquatic larval stage. They require moist environments but generally are not associated with standing water.

Detailed Characteristics of the Tribe Plethodontini

Characteristics are summarized from Lombard and Wake's (1986) phylogenetic analysis of major plethodontid lineages with special emphasis on evolution of feeding mechanisms. These characteristics are useful in combination for distinguishing plethodonine salamanders from other plethodontids, although most characteristics listed are not synapomorphies of the tribe Plethodontini.

Tongue and Hyobranchial Apparatus

Tongues are attached to the jaw by a short muscle plus connective and mucosal tissue. Tongues are protrusible in Aneides and Plethodon and projectile in Ensatina. The hyobranchial skeleton includes a urohyal, cylindrical basibranchial, and radii that are broad and flat and independent of the basibranchial. The basibranchial, first ceratobranchial and epibranchial elements are of approximately equal length. The first ceratobranchial is larger than the second ceratobranchial and constitutes the main force-transmitting element in movement of the tongue. Embryos have three epibranchials. The rectus cervicis profundis muscle is linearly arranged and the rectus cervicis superficialis has a lateral slip. Omohydoideus, genioglossus, circumglossus, intraglossus and basiradialis muscles are present. The hyoglossus muscle has a complete anterior section and posteriorly oriented fibers in the posterior section. The suprapeduncularis muscle is weakly developed.

Cranial Osteology and Structure of the Inner Ear

The vomer differs from those of desmognathines and hemidactyliines in lacking the bony shelf anterior to the preorbital process. Parietal bones are relatively simple, scalelike structures. The facial process of the maxilla is located in a relatively posterior position, near the center of the pars dentalis. The premaxillae surround an intermaxillary gland that lies directly behind the pars dentalis. In the inner ear, the amphibian periotic canal forms a ventral loop immediately after leaving the periotic cistern. The bore radius of the otic semiarticular ducts has a negative allometry with respect to body weight, although only slightly so in Ensatina.

The diploid number of chromosomes is 28.

Classification

The tribe Plethodontini as formulated by Wake (1966) comprises the genera Aneides, Ensatina and Plethodon. Plethodon is the largest plethodonine genus in number of species (42, compiled by Frost [1985] and Duellman [1993]), many of which are cryptic species discovered using electrophoretic studies of protein variation. Aneides contains 5 species noteworthy because of evolutionarily derived structures in the limbs and jaws (see introduction section above), although recognition of Aneides appears to make Plethodon paraphyletic (see discussion of phylogenetic relationships below). Ensatina is currently recognized as a single species, although some concepts of species would require that it be recognized as several to many different species (Frost and Hillis, 1990; Highton, 1990).

Because of its large size, the genus Plethodon has been divided into 8 species groups (Highton and Larson, 1979) as follows (including species recognized after 1979):

1. Plethodon cinereus group: P. cinereus, P. hoffmani, P. hubrichti, P. nettingi, P. richmondi, P. serratus, P. shenandoah
2. Plethodon glutinosus group: P. albagula, P. aureolus, P. caddoensis, P. chattahoochee, P. chlorobryonis, P. cylindraceus, P. fourchensis, P. glutinosus, P. grobmani, P. jordani, P. kentucki, P. kiamichi, P.kisatchie, P. mississippi, P. ocmulgee, P. ouachitae, P. petraeus, P. savannah, P. sequoyah, P. teyahalee, P. variolatus, P. yonahlossee)
3. Plethodon wehrlei group: P. punctatus, P. wehrlei
4. Plethodon welleri group: P. dorsalis, P. websteri, P. welleri
5. Plethodon elongatus group: P. elongatus, P. stormi
6. Plethodon neomexicanus group: P. larselli, P. neomexicanus
7. Plethodon vandykei group: P. idahoensis, P. vandykei
8. Plethodon vehiculum group: P. dunni, P. vehiculum.

Members of the P. cinereus, P. glutinosus, P. wehrlei and P. welleri groups are collectively called "eastern plethodons" because they are found in eastern North America, whereas members of the P. elongatus, P. neomexicanus, P. vandykei and P. vehiculum groups are termed "western plethodons" because they live in western North America.

The adjective "plethodonine" is used to refer specifically to members of the tribe Plethodontini; "plethodontine" refers to members of the plethodontid subfamily Plethodontinae which includes the tribe Plethodontini (plus the tribes Bolitoglossini and Hemidactyliini).

Discussion of Phylogenetic Relationships

Phylogenetic relationships within the tribe Plethodontini are inferred primarily from allozymic and immunological data, plus morphological characters for the genus Aneides (Highton and Larson, 1979; Maxson et al, 1979; Larson et al., 1981; Larson, 1984; Highton et al., 1989; Highton, 1991; Wynn et al., 1988). Statistical analyses (Highton, 1991) strongly support monophyly of Aneides and of each of the eight species groups of Plethodon.

Relationships among species within the P. cinereus and P. glutinosus groups are more tentative. Within the P. glutinosus group, exact placement of the deepest branches (P. petraeus, P. yonahlossee and the P. ouachitae complex [P. caddoensis, P. fourchensis and P. ouachitae]) is particularly uncertain.

Within Aneides, exact relationships among the species from the west coast of North America (A. ferreus, A. flavipunctatus and A. lugubris) are uncertain although these three species form a monophyletic group with respect to the other Aneides species. The single eastern North American Aneides (A. aeneus) appears to be the sister taxon to the other four species combined.

Molecular data indicate that Plethodon is paraphyletic with respect to Aneides, although taxonomic changes are not recommended until the exact phylogenetic placement of Aneides relative to the plethodons can be determined more confidently. Available data sets agree that Ensatina forms the sister group to Aneides and Plethodon combined.

References

Brown, C. W. 1974. Hybridization among the subspecies of the plethodontid salamander Ensatina eschscholtzii. University of California Publications in Zoology 98:1-57.

Dobzhansky, T. 1958. Species after Darwin. Pp. 19-55 in S. A. Barnett (ed.) A Century of Darwin. Harvard Univ. Press. Cambridge, Massachusetts.

Duellman, W. E. 1993. Amphibian Species of the World: Additions and Corrections. Univ. of Kansas Printing Service. Lawrence, KS.

Estes, R. 1981. Gymnophiona, Caudata. Handbuch der Paläoherpetologie 2:1-115.

Frost, D. R. 1985. Amphibian Species of the World. Allen Press and the Association of Systematics Collections. Lawrence, Kansas.

Frost, D. R. and D. M. Hillis. 1990. Species in concept and practice: Herpetological applications. Herpetologica 46:87-104.

Highton, R. 1972. Distributional interactions among eastern North American salamanders of the genus Plethodon. Virginia Polytechnic Institute Research Division Monograph 4:139-188.

Highton, R. 1990. Taxonomic treatment of genetically differentiated populations. Herpetologica 46:114-121.

Highton, R. 1991. Molecular phylogeny of plethodonine salamanders and hylid frogs: Statistical analysis of protein comparisons. Molecular Biology and Evolution 8:796-818.

Highton, R. 1995. Speciation in eastern North American salamanders of the genus Plethodon. Annual Review of Ecology and Systematics 26:579-600.

Highton, R. and A. Larson. 1979. The genetic relationships of the salamanders of the genus Plethodon. Systematic Zoology 28: 579-599.

Highton, R., G. C. Maha and L. R. Maxson. 1989. Biochemical evolution in the slimy salamanders of the Plethodon glutinosus complex in the eastern United States. Illinois Biological Monographs 57:1-154.

Jackman, T. R. and D. B. Wake. 1994. Evolutionary and historical analysis of protein variation in the blotched forms of salamanders of the Ensatina eschscholtzii complex (Amphibia: Plethodontidae). Evolution 48:876-897.

Larson, A. 1984. Neontological inferences of evolutionary pattern and process in the salamander family Plethodontidae. Evolutionary Biology 17:119-217.

Larson, A., D. B. Wake, L. R. Maxson and R. Highton. 1981. A molecular phylogenetic perspective on the origins of morphological novelties in the salamanders of the tribe Plethodotini (Amphibia, Plethodontidae). Evolution 35:405-422.

Lombard, R. E. and D. B. Wake. 1986. Tongue evolution in the lungless salamanders, family Plethodontidae. IV. Phylogeny of plethodontid salamanders and the evolution of feeding dynamics. Systematic Zoology 35:532-551.

Maxson, L. R., R. Highton and D. B. Wake. 1979. Albumin evolution and its phylogenetic implications in the plethodontid salamander genera Plethodon and Ensatina. Copeia 1979:502-508.

Moritz, C., C. J. Schneider, and D. B. Wake. 1992. Evolutionary relationships within the Ensatina eschscholtzii complex confirm the ring species interpretation. Systematic Zoology 41:273-291.

Reagan, N. L. 1992. Evolution of Sexual Isolation in Salamanders of the Genus Plethodon. Ph.D. dissertation. University of Chicago.

Sessions, S. K. and A. Larson. 1987. Developmental correlates of genome size in plethodontid salamanders and their implications for genome evolution. Evolution 41:1239-1251.

Staub, N. L. 1993. Intraspecific agonistic behavior of the salamander Aneides flavipunctatus (Amphibia: Plethodontidae) with comparisons to other plethodontid species. Herpetologica 49:271-282.

Stebbins, R. C.. 1949. Speciation in salamanders in the plethodontid genus Ensatina. University of California Publications in Zoology 48:377-526.

Stebbins, R. C. 1954. Natural history of the salamanders of the plethodontid genus Ensatina. University of California Publications in Zoology 54:47-124.

Wake, D. B. 1963. Comparative osteology of the plethodontid salamander genus Aneides. Journal of Morphology 113:77-118.

Wake, D. B. 1966. Comparative osteology and evolution of the lungless salamanders, family Plethodontidae. Memoirs of the Southern California Academy of Sciences 4:1-111.

Wake, D. B. and A. Larson. 1987. Multidimensional analysis of an evolving lineage. Science 238:42-48.

Wake, D. B. and K. P. Yanev. 1986. Geographic variation in allozymes in a "ring species," the plethodontid salamander Ensatina eschscholtzii of western North America. Evolution 40:702-715.

Wake, D. B., K. P. Yanev and C. W. Brown. 1986. Intraspecific sympatry in a "ring species," the plethodontid salamander Ensatina eschscholtzii of southern California. Evolution 40:866-868.

Wake, D. B., K. P. Yanev and M. M. Frelow. 1986. Sympatry and hybridization in a "ring species": The plethodontid salamander Ensatina eschscholtzii. Pp. 134-157 in D. Otte and J. A. Endler (eds.) Speciation and its Consequences. Sinauer Associates. Sunderland, Massachusetts.

Wynn, A. H., R. Highton and J. F. Jacobs. 1988. A new species of rock-crevice dwelling Plethodon from Pigeon Mountain, Georgia. Herpetologica 44:135-143.