Neural basis of acoustic species recognition in a cryptic species complex

Abstract

Sexual traits that promote species recognition are important drivers of reproductive isolation, especially among closely related species. Identifying neural processes that shape species differences in recognition is crucial for understanding the causal mechanisms of reproductive isolation. Temporal patterns are salient features of sexual signals widely used in species recognition by several taxa, including anurans. Recent advances in our understanding of temporal processing by the anuran auditory system provide an opportunity to investigate the neural basis of species-specific recognition. The anuran inferior colliculus (IC) consists of neurons that are selective for temporal features of calls. Of potential relevance are auditory neurons known as interval-counting neurons (ICNs) that are often selective for the pulse rate of conspecific advertisement calls. Here, we tested the hypothesis that ICNs mediate acoustic species recognition by exploiting the known differences in temporal selectivity in two cryptic species of gray treefrog (Hyla chrysoscelis and Hyla versicolor). We examined the extent to which the threshold number of pulses required to elicit behavioral responses from females and neural responses from ICNs was similar within each species but potentially different between the two species. In support of our hypothesis, we found that a species difference in behavioral pulse number thresholds closely matched the species difference in neural pulse number thresholds. However, this relationship held only for ICNs that exhibited band-pass tuning for conspecific pulse rates. Together, these findings suggest that differences in temporal processing of a subset of ICNs provide a mechanistic explanation for reproductive isolation between two cryptic treefrog species.

Informational Masking Constrains Vocal Communication in Nonhuman Animals

“…Electrophysiological recordings of neurons in the IC of awake gray treefrogs show pulse-rate selectivity mirroring that observed in behavioral phonotaxis experiments with gravid females (Rose et al 1985;Gupta et al 2021). The vertebrate IC is a key auditory processing and audio-motor integration area thought to function in mediating acoustically guided behaviors with short latencies, such as responding to prey, predators, or conspecifics (Casseday & Covey, 1996), including phonotaxis in female frogs (Endepols et al, 2003;Hoke et al, 2007Hoke et al, , 2004.…”

“…These neurons only fire after they are presented with a threshold number of pulses occurring at an optimal pulse rate that typically coincides with the species-specific pulse rate of advertisement calls (Edwards et al, 2002;Rose, 2014). In addition, the pulse number thresholds of intervalcounting neurons closely match those measured behaviorally, indicating these neurons play a key functional role in processing biologically informative temporal features in pulsatile sounds (Gupta et al, 2021;Rose et al, 2015). Interval-counting neurons respond to the first pulse of a pulsatile sound with a brief excitatory postsynaptic potential (EPSP) followed by a large inhibitory postsynaptic potential (IPSP).…”

“…The male’s advertisement call consists of a pulse train of 12 to 43 pulses (mean = 30 pulses/call) produced at an average pulse rate of 50 pulses/s (Ward et al, 2013a). Females must hear a threshold number of pulses produced at a conspecific pulse rate before exhibiting a phonotaxis response indicating recognition of the call (Gupta et al, 2021; Vélez & Bee, 2011). In Experiment 1, we used an adaptive tracking procedure (Gupta et al, 2021) to test the prediction that pulsatile sounds at remote frequencies impair signal recognition, as evidenced by lower response rates, elevated pulse number thresholds, and longer response latencies compared with quiet and a control masking condition lacking pulsatile sounds.…”

“…We followed procedures described by Gupta et al (2021) to measure pulse number thresholds from 323 subjects. In the first of a sequence of single-speaker tests, we presented subjects with a sequence of target signals consisting of 8 pulses.…”

“…High levels of background noise and extensive call overlap -both by conspecific males and by males of other species that also produce pulsatile calls at different spectral frequencies -are commonplace in mixed species choruses (Kuczynski et al, 2010;Nityananda & Bee, 2011;Tanner & Bee, 2019). In these environments, females recognize and discriminate among potential males using information encoded by temporal features of advertisement calls (Bush et al, 2002;Gerhardt, 1994;Gupta & Bee, 2021;Nityananda & Bee, 2011;Ward et al, 2013a). However, chorus noise and overlapping calls can interfere with signal recognition and discrimination (Bee, 2008;Bee & Schwartz, 2009;Vélez et al, 2013a;.…”