Phylogeny of Mental Glands, Revisited

Abstract

Mental glands and their associated delivery behaviors during courtship are unique to the plethodontid salamanders. Because previous interpretations of the evolution of these features were conducted using older phylogenetic hypotheses, we reanalyzed these traits with newer courtship descriptions and contemporary phylogenetic methods. Using Bayesian ancestral state reconstruction methods that have been developed since the first phylogenetic analyses were conducted in the mid-1990s, we reconstructed mental gland and courtship behavior evolution on a Bayesian phylogeny of the nuclear gene Rag1. The most probable ancestral condition for plethodontids was resolved as presence of a mental gland. Loss of a mental gland occurred in each subfamily and was recovered as the most probable ancestral condition for the Spelerpinae. In contrast, parsimony reconstruction recovered the presence of a mental gland in the ancestor to Spelerpinae with multiple secondary losses. We hypothesize that that absence of a mental gland is possibly ancestral in some clades (i.e., Spelerpinae) and secondary in others (e.g., paedomorphic Eurycea). The most probable ancestral form of the mental gland is likely to be the large pad-type distributed extensively in Plethodontinae and Bolitoglossinae. Desmognathans have the most unique mental glands, occurring in an anterior protrusion or bifurcated form (in Desmognathus wrighti). Fan-shaped mental glands evolved independently in Eurycea and Oedipina. Small pads arose independently in Bolitoglossinae, Plethodontinae, and Spelerpinae. Head-rubbing behavior for mental gland delivery mode was recovered as the most probable and parsimonious ancestral state for the Plethodontidae, with independent losses of this behavior in Plethodontinae and Spelerpinae. Because head-rubbing was observed in outgroups, we hypothesize that head-rubbing behavior predated mental gland evolution. Pulling, snapping, slapping, and biting behaviors evolved independently in the Plethodontinae and Spelerpinae and are not homologous with head-rubbing. All hypotheses of mental gland and courtship evolution invoke homoplasy.

Fig. 1

Mental gland types. (A) Character state 1, in Eurycea spelaea, from Sever (1976). (B) Character state 2, in Bolitoglossa. (1) External appearance in B. aspera, from Noble (1927); (2) Horizontal section through the pad of B. mexicana, from Truffeli (1954). (C) Character state 3, in Desmognathus fuscus. (1) Site of the mental gland ventral and anterior to the mandibular symphysis, from Noble (1927); (2) Mental gland tubules terminating in secretory pores (circles), from Sever (1976). (D) Character state 4, in Desmognathus wrighti, from Sever (1976). Glands secrete at the base of anterior mandibular teeth.

Fig. 2

Mental gland shapes continued, character state 5. (A) Eurycea wilderae (1) secretory area at apex of mandibles and extent of pad indicated by dotted lines, from Arnold (1976); (2) Pores (circles) and gland tubules, from Sever (1979); (3) Snapping and pulling behavior by which the male delivers pheromones to the female with the aid of sexually dimorphic teeth, from Arnold (1976). (B) Oedipina, from Trufelli (1954). (1) O. uniformis, ventral view; (2) O. uniformis, lateral view; (3) O. cyclocauda, sagittal section.

Fig. 3

Bayesian reconstruction of mental glands within Plethodontidae. Two states were considered: absent (white) and present (black). Pie charts at each node provide the proportional probability of each state. Numerical values indicate the highest probability at each node. The phylogeny was reconstructed using a Bayesian analysis of Rag1 sequences (see Materials and Methods).

Fig. 4

Bayesian reconstruction of mental gland morphology within Plethodontidae. Six unordered states were considered: absent (white), small pad (black), large pad (red), anterior protrusion (yellow), bifurcated (green), and fan-shaped (blue). Pie charts at each node provide the proportional probability of each state. Numerical values indicate the highest probability at each node. The phylogeny was reconstructed using a Bayesian analysis of Rag1 sequences (see Materials and Methods).

Fig. 5

Bayesian reconstruction of head-rubbing behavior within Plethodontidae. Two states were considered: absent (white) and present (black). Pie charts at each node provide the proportional probability of each state. Numerical values indicate the highest probability at each node. The phylogeny was reconstructed using a Bayesian analysis of Rag1 sequences (see Materials and Methods).

Fig. 6

Bayesian reconstruction of pulling behavior within Plethodontidae. Two states were considered: absent (white) and present (black). Pie charts at each node provide the proportional probability of each state. Numerical values indicate the highest probability at each node. The phylogeny was reconstructed using a Bayesian analysis of Rag1 sequences (see Materials and Methods).

Fig. 7

Bayesian reconstruction of snapping behavior within Plethodontidae. Two states were considered: absent (white) and present (black). Pie charts at each node provide the proportional probability of each state. Numerical values indicate the highest probability at each node. The phylogeny was reconstructed using a Bayesian analysis of Rag1 sequences (see Materials and Methods).

Fig. 8

Bayesian reconstruction of slapping behavior within Plethodontidae. Two states were considered: absent (white) and present (black). Pie charts at each node provide the proportional probability of each state. Numerical values indicate the highest probability at each node. The phylogeny was reconstructed using a Bayesian analysis of Rag1 sequences (see Materials and Methods).

Fig. 9

Bayesian reconstruction of biting/restraint behavior within Plethodontidae. Two states were considered: absent (white) and present (black). Pie charts at each node provide the proportional probability of each state. Numerical values indicate the highest probability at each node. The phylogeny was reconstructed using a Bayesian analysis of Rag1 sequences (see Materials and Methods).