Sexual selection for sensory exploitation in the frog Physalaemus pustulosus

Abstract

The sensory bases of species and population mate preferences are well known; in frogs properties of the female auditory system influence such preferences. By contrast, there is little understanding of how sensory characteristics could result in sexual selection within a population. One possible mechanism is that females are more sensitive to male courtship signals that deviate from the population mean. We document this mechanism in the frog Physalaemus pustulosus. Female basilar papilla tuning is biased toward lower-than-average frequencies in the 'chuck' portion of the male's call, explaining female preference for the lower-frequency chucks produced by larger males. The tuning does not differ between P. pustulosus and its close relative P. coloradorum, a species in which males never evolved the ability to produce chucks; thus the female tuning evolved before the chuck and therefore the chuck played no role in the evolution of the preference. This allows us to reject two popular hypotheses for the evolution of this female preference (runaway sexual selection and natural selection) in favour of a third: sexual selection for sensory exploitation.

The ability to perform physically challenging songs predicts age and size in male swamp sparrows, Melospiza georgiana

“…In a laboratory experiment, female swamp sparrows gave more copulation solicitation postures to natural songs that were closer to the performance limit (Ballentine et al 2004). This empirical evidence of female preferences for physically challenging songs supports the general hypothesis that vocal performance is a reliable signal of male quality, but it does not rule out alternative hypotheses such as sensory biases (Ryan et al 1990) or runaway selection (Fisher 1930). If female preferences for vocal performance represent adaptive female choice for high-quality males, because vocal performance is a reliable signal of male quality, then it is necessary to determine whether vocal performance correlates with male quality.…”

Social regulation of plasma estradiol concentration in a female anuran

“…Classic studies demonstrate that the whine is sufficient to elicit phonotaxis (i.e., species recognition), the chuck alone does not, but when placed at the end of the whine, it increases the whine's attractiveness (Rand and Ryan, 1981;Ryan, 1985;Wilczynski et al, 1995Wilczynski et al, , 1999. In addition, females prefer chucks with a lower fundamental frequency (Ryan, 1980;Ryan et al, 1990). Future studies may reveal whether the female's hormonal response would reflect the known behavioral responses to these types of signals.…”

The mixed-species chorus as public information: túngara frogs eavesdrop on a heterospecific

“…Although this is generally true, many species use only one of these organs for conspecific communication, though both are tuned (Lewis and Lombard 1988;Zakon and Wilczynski 1988;Lewis and Narins 1999;Gerhardt and Schwartz 2001). For example, all species of the Physalaemus pustulosus species group are thought to possess a tuned BP, yet the tungara frog is one of the few species known to use these frequencies in conspecific communication (Ryan et al 1990;Wilczynski et al 2001). Because the maintenance of a tuned auditory organ presumably incurs costs, the persistence of the BP in this species group has fueled speculation that it may take part in unidentified functions (Bradbury and Vehrencamp 2000).…”

“…The spectral content of the L. labialis call falls in a range frequency responses attributed to the BP of the tungara frog, an auditory organ that is not tonotopically organized and tends to be permissive for broad classes of stimuli. (The actual neurophysiological responses are derived from midbrain recordings, not from direct recordings of the BP [Ryan et al 1990].) This further argues that tungara frogs are unlikely to make meaningful distinctions within this class of stimuli.…”

“…In Panama, male tungara frogs calling in open areas can be found near calling male L. labialis. The call of L. labialis is an ascending frequency sweep covering much higher frequencies, with a substantial amount of spectral energy corresponding to the presumed tuning of the tungara frog's basilar papilla (BP), a different auditory organ than is thought to receive the species-specific whine of the tungara frog (tuning based on auditory midbrain recordings, Ryan et al 1990). We predicted that male tungara frogs would use the calls of L. labialis to assess predation risk, despite the fact the 2 species' calls are extremely dissimilar.…”