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Dissimilarities in Auditory Tuning in Midwife Toads of the Genus Alytes (Amphibia: Anura)

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Dissimilarities in Auditory Tuning in Midwife Toads of the Genus Alytes (Amphibia: Anura) Biological Journal of the Linnean Society, 2015, 116, 41–51. With 3 figures. Dissimilarities in auditory tuning in midwife toads of the genus Alytes (Amphibia: Anura) 1 1,2 3 MARIO PENNA *, NELSON A. VELASQUEZ and JAIME BOSCH 1Programa de Fisiologıa y Biofısica, Facultad de Medicina, Instituto de Ciencias Biomedicas, Universidad de Chile, Casilla 70005, Correo 7, Santiago, Chile 2Facultad de Ciencias Basicas, Universidad Catolica del Maule, San Miguel 3605, 3480112, Talca, Chile 3Museo Nacional de Ciencias Naturales, CSIC, Jose Gutierrez Abascal 2, 28006, Madrid, Spain Received 23 January 2015; revised 15 March 2015; accepted for publication 15 March 2015 The auditory sensitivity in three species of the anuran genus Alytes (Alytidae) was examined to determine patterns of intra- and interspecific variation, relating these measurements to behavioural preferences measured in previous studies and to the adaptive and evolutionary significance of this sensory function. The audiograms obtained with multi-unit recordings in the torus semicircularis of 13 Alytes cisternasii,10Alytes obstetricans, and eight Alytes dickhilleni show two regions of enhanced sensitivity, between approximately 100–500 and 1200– 2400 Hz, with minimum thresholds at approximately 40 and 45 dB SPL, respectively. The mean and range of the high-frequency region differed among species, although the sensitivity, measured as minimum thresholds, was similar. The region of high-frequency sensitivity was centred at approximately the frequency of the advertisement call in A. cisternasii but, in A. obstetricans and A. dickhilleni, was centred at frequencies higher than the conspecific calls. These results contrast with preferences for lower frequencies exhibited by Alytes in female phonotactic and in male evoked vocal responses. Such loose relationships between signals and receivers suggest that the divergence of the sound communication system in Alytes has implied environmental and phylogenetic factors in addition to sexual selection processes. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 116,41–51. ADDITIONAL KEYWORDS: acoustic communication – auditory sensitivity – torus semicircularis. INTRODUCTION the basilar papilla of this species (Frishkopf, Capranica & Goldstein, 1968). Animal communication involves the exchange of In general, such a trend has been confirmed in information between emitters and receivers, a pro- more recent studies (Gerhardt & Schwartz, 2001); cess favoured by a broad correspondence between however, various instances with a lack of correspon- signal structure and receptor’s sensitivity. dence between vocalizations and auditory tuning The notion of a strict matching between signals have been reported. Gross mismatches occur in anu- and receptors oriented pioneering research in sound rans that communicate with calls having their main communication of anurans (Capranica, 1965; Capra- spectral components restricted to the high-frequency nica & Moffat, 1983). Males of the original experi- region, with their low frequency sensitivity having mental subject of this research, Rana catesbeiana, no apparent communicative role (Ryan & Rand, now Lythobates catesbeianus, give evoked vocal 1993; Bosch & Boyero, 2003a). At a finer scale, in a responses only to stimuli containing spectral energy number of anuran species communicating with calls both in low and high-frequency regions, matching in the high-frequency region, females prefer frequen- the spectral design of the conspecific advertisement cies lower than the mean of the dominant frequency call. These two components in turn match the sensi- of the conspecific call, originating processes of direc- tivities of the auditory receptors, the amphibian, and tional selection by which conspecific calls of relative low frequencies within the high-frequency range are *Corresponding author. E-mail: [email protected] favoured (Ryan, Perrill & Wilczynski, 1992; Wollerman, © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 116, 41–51 41 42 M. PENNA ET AL. 1998; Castellano et al., 2000). By contrast, in other frequency of the call of this species (approximately anurans, preferences for mean frequencies within 1100 Hz). By contrast, audiograms of A. cisternasii the conspecific call range, leading to stabilizing selec- reported by Bosch & Wilczynski (2003) show a region tion processes have been reported (Grafe, 1997; of high-frequency sensitivity tuned at approximately Gerhardt & Schwartz, 2001). Hence, carrier fre- 1400 Hz, which closely matches the dominant fre- quency appears to be subject to directional selection quency of the call of the population analyzed. How- in some cases and stabilizing selection in others ever, it is not clear how comparable these (Gerhardt & Huber, 2002). measurements are because each species was studied Instances of precise matching between preferences in different settings, different laboratories and with and traits are known to occur in animal groups other an interval of decades in between. In addition to than anurans (Schmidt, Riede & Romer,€ 2011; Henry these explorations, two studies on auditory midbrain & Lucas, 2010), although female preferences for single and few-unit recordings have been carried out traits deviating from the species mean and even for in A. obstetricans (Mohneke, 1982, 1983). traits other than those exhibited by conspecific males In the present study, we conducted measurements have been extensively documented (Ryan & Keddy- of the auditory sensitivity of Alytes cisternasii, Hector, 1992; Andersson, 1994; Endler & Basolo, A. obstetricans and Alytes dickhillenii, aiming to 1998). These variants from a strict correspondence examine patterns of variation within and among spe- between emitters and receivers have been explained cies, relating these sensitivities to the spectral struc- in terms of constraints imposed by environmental ture of their calls and to behavioural preferences for factors (Endler, 1992) or by sensory systems (Ryan, these signals reported in previous studies on this 1990; Arak & Enquist, 1995). In particular, the sen- genus. We aimed to determine whether the tuning of sory bias hypothesis proposes that natural selection the auditory sensitivity of these anurans has a corre- models female preferences and males take advantage spondence with the preferences of males and females on these sensory designs for mate attraction (Fuller, for calls of low dominant frequencies within the con- Houle & Travis, 2005). specific ranges reported in the literature. In addition, Explorations of correspondences between signal the current knowledge of the phylogenetic relation- structure and receptor sensitivity have been con- ships among these taxa (Martınez-Solano et al., ducted mostly in derived anurans, which, in some 2004; Maia-Carvalho et al., 2014) allows interpreta- cases, communicate by means of signals having com- tions on evolutionary trends of correspondences plex structure (Ryan & Rand, 1999; Meenderink, between auditory sensitivity and vocal traits. These Kits & Narins, 2010). Anurans of the family Alyti- explorations were carried out using a common set-up dae, having a sister status relative to Neobatrachia, between the three taxa, aiming to provide interpreta- have proved to be advantageous subjects for research tions on potential interspecific differences in auditory on sound communication (Marquez & Bosch, 2001). sensitivity devoid of difficulties of comparisons based The advertisement calls of toads of the genus Alytes on two previous independent studies (Mohneke & are low-amplitude, short-duration pure tones lacking Schneider, 1979; Bosch & Wilczynski, 2003). frequency and amplitude modulation. The signals of four species found in the Iberian Peninsula differ in their dominant frequency and duration (Heinzmann, MATERIAL AND METHODS 1970; Marquez & Bosch, 1995; Bush, 1996). Phono- taxis studies on Alytes cisternasii and Alytes obstericans EXPERIMENTAL SUBJECTS AND SURGICAL have reported that females orient preferentially to PROCEDURES low-frequency calls within the conspecific range, a The adult individuals used for the present study preference pattern congruent with mating advanta- were captured in different localities in Spain ges of larger males found in nature (Marquez, 1995a, between 2003 and 2006: 13 A. cisternasii (nine b; Marquez & Bosch, 1997; Bosch & Marquez, 2005; females and four males from Merida, 38.917°N, Marquez, Bosch & Eekhout, 2008). Males also call 6.333°W), 10 A. obstetricans (three females and more actively in response to synthetic call dummies seven males from Toro and Picos de Europa National having lower dominant frequencies (Bosch & Park, 41.525°N, 5.392°W and 43.187°N, 4.871°W, Marquez, 1996), indicating the relevance of this trait respectively), and eight A. dickhillenii (three females for intrasexual competition. and five males from Cazorla Natural Park, 38.158°N, Measurements of auditory sensitivity have been 2.738°W). The frogs were carried to the Laboratory conducted for two species of Alytes. Audiograms of of Neuroethology at the University of Chile in Santi- A. obstetricans reported by Mohneke & Schneider ago, Chile where they were housed in terraria under (1979) show a high-frequency sensitivity centred at an inverted 12 : 12 h light/dark cycle at 15 Æ 1 °C approximately 1800 Hz, well above the dominant and fed with tenebrionid larvae once per week. The © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 116, 41–51
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