Lynne D. Houck

The Biology of Plethodontid Salamanders

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Male courtship pheromones increase female receptivity in a plethodontid salamander

Abstract The effect of courtship pheromones on female receptivity was tested in the terrestrial plethodontid salamander Desmognathus ochrophaeus by staging encounters between 50 male-female pairs. Male mental glands were ablated to prevent uncontrolled delivery of the pheromones. Glands were used to create a pheromone extract for experimental application. A female was treated with the extract 30 min prior to a courtship encounter and, in other encounters, the same female was treated with a saline control. Observations of courtship behaviour were taken by scan samples every 15 min for 6 h. A female receiving the pheromone treatment mated an average of 28% (59 min) sooner than she did after receiving the control treatment. These results are the first quantitative documentation that courtship pheromones function in salamanders directly to increase female receptivity.

A STATISTICAL STUDY OF MATE CHOICE: SEXUAL SELECTION IN A PLETHODONTID SALAMANDER (DESMOGNATHUS OCHROPHAEUS)

Our experiment revealed the existence of significant variation in mating success in a salamander species in which males do not provide courtship feeding, nest sites, or parental care. Differences in mating success were based on natural variation among adult males and females, rather than on traits of an artificially selected set of potential mates. Courtship encounters deliberately involved only one male and one female, thus eliminating the potentially confounding effects of male‐male competition and variations in mate encounter rate. Even after eliminating these effects and random error, some females were more likely than others to elicit spermatophore deposition by a male, and some males were more likely than others to inseminate a female. Such variation among individuals represents an opportunity for sexual selection to act on phenotypic characters that affect mating success.

Pheromone Communication in Amphibians and Reptiles

This selective review considers herpetological papers that feature the use of chemical cues, particularly pheromones involved in reproductive interactions between potential mates. Primary examples include garter snake females that attract males, lacertid lizards and the effects of their femoral gland secretions, aquatic male newts that chemically attract females, and terrestrial salamander males that chemically persuade a female to mate. Each case study spans a number of research approaches (molecular, biochemical, behavioral) and is related to sensory processing and the physiological effects of pheromone delivery. These and related studies show that natural pheromones can be identified, validated with behavioral tests, and incorporated in research on vomeronasal functional response.

Pheromonal activation of vomeronasal neurons in plethodontid salamanders

Pheromones from the mental glands of male plethodontid salamanders increase sexual receptivity in conspecific females. The pheromone enters the vomeronasal organ during courtship to produce this effect. Vomeronasal neurons from female Plethodon shermani were examined following exposure to male pheromone or saline placed on the nares. Agmatine was used in conjunction with the pheromone to enable immunocytochemical visualization of chemosensory neurons that were activated by the pheromone. Olfactory neurons exposed to pheromone or saline, and vomeronasal neurons exposed to saline did not demonstrate significant labeling. A population of vomeronasal neurons was intensely labeled following exposure to the pheromone. This study suggests that a specific population of vomeronasal neurons in a female plethodontid salamander is responsible for transmitting pheromonal information to the brain to produce modifications in behavior.

The Evolution of Salamander Courtship Pheromones

Among vertebrates, the importance of chemical signals and chemosensory perception is unquestioned, especially for mammals (Birch, 1974b; Doty, 1976; Muller-Schwarze and Mozell, 1977). Chemosensory perception also is well documented for many reptiles (Burghardt, 1970), fish (Bardach and Todd, 1970; Liley, 1982; Pfeiffer, 1974; Stacey, 1983), and even some birds (Grubb, 1974; Stager, 1967; Walcott and Lednor, 1983). It is less widely appreciated that the perception and production of chemical information represents a critical mode of communication for amphibians (Madison, 1977), salamanders in particular. Salamanders produce chemical secretions from a glandular skin, from specialized glands located on the head, or from discrete glands within the cloaca (Brodie, 1968; Noble, 1931; Sever, 1976). For many salamanders, skin secretions include noxious poisons that are effective at repelling potential predators (Labanick and Brandon, 1981; Madison, 1977). Within species, salamanders use chemical perception as one of several significant cues when migrating long distances to breeding sites (Dolmen, 1982; Grant et al., 1968; Kleeberger and Werner, 1982; Twitty, 1959, 1961) or when returning to “home” areas from which they have been displaced (Holomuzki, 1982; Madison 1969, 1972; Madison and Shoop, 1970). Forester (1977, 1979) has shown that females of at least one plethodontid species (Desmognathus ochrophaeus) returned from months of foraging in the forest litter to the precise streamside site where they had oviposited in a previous year.

A new vertebrate courtship pheromone, PMF, affects female receptivity in a terrestrial salamander

Vertebrate pheromones that affect female receptivity have been documented only in salamanders. These courtship pheromones have been investigated most intensively in plethodontid salamanders. The source of the plethodontid courtship pheromone is the male’s submandibular (mental) gland, which produces a multiprotein secretion. In earlier work with our main study species, Plethodon shermani (the red-legged salamander), an extract of protein secretions obtained from male mental glands acted to increase sexual receptivity in females. In addition, one particular protein in the gland secretion, plethodontid receptivity factor (PRF), could act alone to increase female receptivity. We now report that a second protein, termed ‘plethodontid modulating factor’ (PMF), acts oppositely to reduce female receptivity. The natural courtship pheromone blend thus includes two proteins that separately produce opposing messages, even though the combined effect of both proteins is to increase female receptivity.

Population Variation in Salamander Courtship Pheromones

We examined intraand interspecific chemical variation in salamander courtship pheromones. The extent to which plethodontid receptivity factor (PRF) and other glandular components vary among populations of Plethodon jordani was analyzed by reverse-phase HPLC. Gland extracts from individuals revealed that males within a population differ in the relative amounts of the glandular components as well as in the presence and absence of components, including PRF. Comparisons between populations showed that each population had a unique elution profile and differed significantly in the relative amounts of PRF and the other extract components. Knowledge about the nature of geographic variation in the courtship pheromone, combined with behavioral tests of female response, will contribute towards understanding how the pheromone evolved.

The effect of body size on male courtship success in a plethodontid salamander

Abstract Two different sets of courtship encounters between female Desmognathus ochrophaeus and males of large ( X¯ =58) and small ( X¯ =38 mm) body size were staged in the laboratory. In the first set, encounters were arranged between male-female pairs so that each of five females individually encountered each of 10 males. In these encouters, small and large males were equally likely to court with and inseminate females. In the second set, each encounter was staged for a trio fo one female and two males (one large and one small); each female had a courtship opportunity with five large-small pairs of males, and each pair of males encountered five different females. In the 25 trio encounters, the large male always chased away the small male before proceeding to court the female. Small males never deposited spermatophores if a large male was present. Male body size should have a significant effect on courtship success in natural populations of D. ochrophaeus if male-male competition affects access to females.

EVOLUTIONARY REPLACEMENT OF COMPONENTS IN A SALAMANDER PHEROMONE SIGNALING COMPLEX: MORE EVIDENCE FOR PHENOTYPIC-MOLECULAR DECOUPLING

Abstract In this article we explore the evolutionary history of a functional complex at the molecular level in plethodontid salamanders. The complex consists of a proteinaceous courtship pheromone, a pheromone-producing gland on the males chin, and a set of behaviors for delivering the pheromone to the female. Long-term evolutionary stasis is the defining feature of this complex at both the morphological and behavioral levels. However, our previous assessment of the pheromone gene, plethodontid receptivity factor (PRF), revealed rapid evolution at the molecular level despite stasis at higher levels of organization. Analysis of a second pheromone gene, sodefrin precursor-like factor (SPF), now indicates that evolutionary decoupling in this complex is pervasive. The evolutionary profiles of SPF and PRF are remarkably similar in that: (a) both genes exhibit high levels of sequence diversity both within and across taxa, (b) genetic diversity has been driven by strong positive selection, and (c) the genes have evolved heterogeneously in different salamander lineages. The composition of the pheromone signal as a whole, however, has experienced an extraordinary evolutionary transition. Whereas SPF has been retained throughout the 100 MY radiation of salamanders, PRF has only recently been recruited to a pheromone function (27 million years ago). When SPF and PRF coexist in the same clade, they show contrasting patterns of evolution. When one shows rapid evolution driven by positive selection, the other shows neutral divergence restrained by purifying selection. In one clade, the origin and subsequent rapid evolution of PRF appear to have interfered with the evolution and persistence of SPF, leading to a pattern of evolutionary replacement. Overall, these two pheromone genes provide a revealing window on the dynamics that drive the evolution of multiple traits in a signaling complex.