Glucocorticoids, androgens, testis mass, and the energetics of vocalization in breeding male frogs.

Male advertisement vocalization in frogs is known to be one of the energetically most expensive activities of ectothermic vertebrates. Glucocorticoids have marked effects on energy metabolism, and, generally, plasma concentrations of glucocorticoids increase during the course of prolonged exercise bouts. Androgen concentrations are also known to vary considerably among breeding male frogs. Intraspecific and interspecific comparisons were used to test for a relationship among androgen concentration, corticosterone concentration, testis mass, and the energetics of vocalization in natural populations of calling male frogs. The results of this study indicate that: (1) intraspecific variation in androgen and corticosteroid concentrations in breeding male frogs is positively correlated as a result of both interindividual variation in the amount of performed vocalization and the relationship between calling effort of an individual male and the level of calling in other males, (2) interspecific variation in corticosteroid concentration of calling male frogs is correlated with the relative energy expended in the species-specific vocalization, and (3) when differences in testis mass are controlled for, vocalization effort is correlated with androgen concentration among species of breeding male frogs. These findings are in contrast to some recent work reported from laboratory experiments on calling frogs.

Molecular systematics and biogeography of the fanged frogs of Southeast Asia.

Our analysis of parts of the mitochondrial ribosomal 12S and 16S genes from 39 populations of Southeast Asian ranid frogs confirms that the fanged frogs are a monophyletic clade. This group, properly called Limnonectes, appears to have arisen in the early Tertiary at a time when free faunal exchange was possible among Southeast Asia, Borneo, Sumatra, Java, and, probably, Sulawesi. Four species groups are tentatively identified within the clade. Part of group 1 includes species related to L. kuhlii that occur in Borneo. Another part of group 1 includes species from Malay Peninsula and Thailand that are related to L. pileata. Species group 2, L. leporina, occurs only in Borneo. Species group 3 is restricted to species distributed in Sulawesi and the Philippines. Species group 4 includes L. blythii and relatives. There is a lack of compatibility between phylogenetic hypotheses generated from molecular and morphological data sets. These differences are related, in large part, to whether some species of Limnonectes have secondarily lost fangs or whether lack of fangs represents the primitive condition.

Mating vocalizations of female frogs: control and evolutionary mechanisms.

Vocalization behaviors of anuran amphibians are universally sexually dimorphic. Usually, only male frogs give an advertisement call, while female frog calls are limited to a soft and simple release call which is specifically suppressed at mating. In a very few species, however, female frogs also give mating vocalizations. We examined possible mechanisms for control of this rare heterotypical behavior. At the peripheral level, most differences in temporal and spectral characteristics between female mating calls and the calls of conspecific males related directly to sexual dimorphisms in laryngeal and oblique muscle morphology. At the neural and hormonal level, we first developed an integrated model for control of vocalizations, based primarily on male frog data. When this model is applied to females, female mating vocalizations were most similar to male advertisement calls, rather than being modified release calls. Females may have conscripted preexisting androgen-sensitive neural pathways typically used only by males but present in both sexes. Female mating calls have been heard only during courtship and amplexus. Androgen levels in females at this time are significantly higher than even those levels in males. Because this situation is common in frogs, female mating vocalizations likely evolved independently multiple times. Character optimization suggests that mate location is the most common biological role for female mate calling, but the particular aspects of reproductive biology vary widely across species.

Androgen receptors in two androgen-mediated, sexually dimorphic characters of frogs.

The presence/absence of androgen receptors is examined in two sexually dimorphic features of frogs: the nuptial pad and the external oblique muscle. Immunohistochemistry reveals that both males and females possess androgen receptors in these tissues. Males have a higher density of immunopositive nuclei in the oblique muscle than do females. The presence of androgen receptors in both male and female tissues is consistent with results from hormone experiments in which androgen supplements induce the expression of a nuptial pad and enlarge the external oblique muscles in castrated males and ovariectomized females.

Hormonal induction of thumb pads and the evolution of secondary sexual characteristics of the Southeast Asian fanged frog, Rana blythii.

The fanged frogs of Southeast Asia do not express most of the hormone-dependent secondary sexual characteristics such as thumb pads that are common to other ranid frogs. At the same point in the evolutionary history of the group that these androgen-mediated characteristics are lost, male parental care first evolves. This behavior is often correlated with low androgen levels. Prior work indicates that in one of the fanged frogs, Rana blythii, adult males have low androgen levels compared to North Temperate species of Rana. This leads to the question of whether these low androgen levels are related to the unusual male parental care and the lack of expression of the thumb pad and other hormone-dependent secondary sexual characteristics in this species. We tested that hypothesis by examining the effects of exogenous dihydrotestosterone supplements on the expression of thumb pads in Rana blythii. Dihydrotestosterone injections appear to stimulate the expression of the thumb pad in R. blythii. These results support the hypothesis that low androgen levels are involved in the loss of the thumb pad in R. blythii. This work provides an example of how mapping characters on phylogenies can be a powerful approach for gaining insights into proximate physiological mechanisms of selection at the evolutionary level.

The role of androgens in opportunistic breeding, tropical frogs.

In this paper we present the results of an interspecific study on the androgen levels of several species of Old World tropical frogs. These data are used to test three hypotheses: (1) in unpredictable, aseasonal environments with opportunistic breeding, gonadal hormones have a permissive rather than an activating role in the expression of mating behavior (Crews and Moore, 1986), (2) a behaviorally induced androgen response is present in opportunistic aseasonal species as well as in temperate seasonal breeders (Crews and Moore, 1986; Wingfield et al., 1990), and (3) because maintenance of high plasma testosterone levels has an associated energetic and/or fitness cost (Moore and Marler, 1987; Wingfield et al., 1990), continuously breeding frogs have lower testosterone levels than seasonal, discontinuous breeders. Androgen and corticosterone levels were found to vary significantly among species exhibiting the same mating behavior, providing support for the hypothesis that hormones have a permissive role. Differences in androgen level were correlated with (1) variation in level of male-male aggression, (2) relative density of male frogs, and (3) call rate and power output of male vocalization. These results indicate that a behaviorally induced androgen response is present in opportunistic, aseasonal breeders. Furthermore, tropical, aseasonal, opportunistic breeding frogs appeared to have lower androgen levels, generally, than confamilial temperate, seasonal breeders. This difference is consistent with the hypothesis that maintenance of high plasma testosterone levels is energetically expensive.

The effect of chemically produced shifts in developmental timing on postmetamorphic morphology in Bombina orientalis.

The effect of altering developmental timing on postmetamorphic morphology was examined in the frog Bombina orientalis. The length of the larval period was manipulated with the use of a thyroid inhibitor. Results show that differences in time to metamorphosis are correlated with shifts in postmetamorphic relative hindlimb length. Furthermore, these differences in relative hindlimb length are similar to those found among closely related species. Variation in the timing of development may be responsible for a significant portion of the postmetamorphic shape variation found among frogs.

Movement of the hyoid in frogs during feeding.

Feeding, breathing, and vocalization sequences of Bufo marinus were recorded by cineradiography. Results of film analysis indicate that the hyoid moves during all three behaviors. Movement of the hyoid is critical in tongue protrusion of frogs, and a biomechanical model of this action is presented. The hyoid appears to represent a compromise morphological system for three functions, rather than an optimal system for any one. This may explain, in part, the retention of a relatively inefficient breathing mechanism in frogs.