Female sexual arousal in amphibians

Abstract

Rather than being a static, species specific trait, reproductive behavior in female amphibians is variable within an individual during the breeding season when females are capable of reproductive activity. Changes in receptivity coincide with changes in circulating estrogen. Estrogen is highest at the point when females are ready to choose a male and lay eggs. At this time female receptivity (her probability of responding to a male vocal signal) is highest and her selectivity among conspecific calls (measured by her probability of responding to a degraded or otherwise usually unattractive male signal) is lowest. These changes occur even though females retain the ability to discriminate different acoustic characteristics of various conspecific calls. After releasing her eggs, female amphibians quickly become less receptive and more choosy in terms of their responses to male sexual advertisement signals. Male vocal signals stimulate both behavior and estrogen changes in amphibian females making mating more probable. The changes in female reproductive behavior are the same as those generally accepted as indicative of a change in female sexual arousal leading to copulation. They are situationally triggered, gated by interactions with males, and decline with the consummation of sexual reproduction with a chosen male. The changes can be triggered by either internal physiological state or by the presence of stimuli presented by males, and the same stimuli change both behavior and physiological (endocrine) state in such a way as to make acceptance of a male more likely. Thus amphibian females demonstrate many of the same general characteristics of changing female sexual state that in mammals indicate sexual arousal.

Figure 1

Examples of phonotaxis tests in female túngara frogs at different reproductive stages indicating differences in sexual arousal. A: Diagram of receptivity test; conspecific call of some type is played from each speaker on either side of the test chamber. Female is considered receptive if she approaches either speaker. B: Percent of females expressing behavior when in the unamplexed state (prior to choosing a male), when in the amplexed stage (after choosing a male and initiating mating, when eggs are close to release), and after mating. C: Diagram of permissiveness test; a synthetic call melding conspecific and heterospecific acoustic elements usually yielding low responses is played from one speaker and noise from the other. Female permissiveness is measured by how likely she is to approach the synthetic —hybrid call. D: Percent of females expressing behavior when in the unamplexed state (prior to choosing a male), when in the amplexed stage (after choosing a male and initiating mating, when eggs are close to release), and after mating. Permissiveness increases when receptivity is high. E: Diagram of discrimination test; attractive 2-syllable conspecific call is played from one speaker and a less attractive 1-syllable call is played from the other to test female’s ability to discern differences in conspecific calls. F: Percent of females choosing the 2 syllable call is high in both the unamplexed and amplexed stages indicating that the receptivity and permissiveness results are not due to a difference in an ability to detect call differences. Discrimination decreases after mating when receptivity is low and female choices become inconsistent. Data are taken from Lynch et al., 2005. See that paper for further description of experimental design and controls procedures.

Figure 2

Level of plasma estrogen in female túngara frogs prior to interacting with a male (unamplexed), in the amplexed stage when eggs are close to release and females have chosen a male for mating, and after mating and egg release. Compare the hormone pattern to the behavioral patterns shown in Figure 1. From Lynch and Wilczynski, 2005.

Figure 3

Change in plasma estrogen in female túngara frogs hearing conspecific male vocal signals vs. random tones (matched for duration and amplitude) for ten consecutive nights. Hearing male signals significantly increases estrogen. From Lynch and Wilczynski, 2006.

Figure 4

Top A–D: Expression of the immediate early gene egr-1 in the midbrain (laminar nucleus of the torus semicircularis) in a female túngara frog under conditions of low estrogen + no call stimulation, low estrogen + conspecific call stimulation, high estrogen + no call stimulation, and high estrogen + conspecific cal stimulation respectively. Bottom: Suggested model of how elevated estrogen and stimulation by various calls interact in stimulating the midbrain. White bars indicate baseline midbrain activity due to hormone action, gray bars indicate midbrain activity due to call stimulation. When hormone levels are low, attractive calls may reach threshold for triggering a phonotaxis response, but unattractive calls fail to reach threshold. When hormone levels are high, both call types could reach threshold for triggering a phonotaxis response. Behavioral, this would appear to be an increase in both receptivity and permissiveness in the female, with preservation of her ability to discriminate calls based on the level of activation. Based on figures in Lynch and Wilczynski, 2008.