Chemical communication plays a central role in social, sexual and ecological interactions among animals. However, the macroevolutionary diversification of traits responsible for chemical signaling remains fundamentally unknown. Most research investigating evolutionary diversification of glands responsible for the production of chemical signals has focused on arthropods, while its study among vertebrates remains neglected. Using a global-scale dataset covering > 80% (7,904 species) of the living diversity of lizards and snakes (squamates), we investigate rates, trajectories and phylogenetic patterns of diversification of their follicular glands for chemical communication. We observed these glands in 13.66% of species, that their expression has varying phylogenetic signal among lineages, and that the crown squamate ancestor lacked follicular glands, which therefore originated and diversified subsequently during their evolutionary history. Additionally, our findings challenge the longstanding view that within squamates the Iguania are visually oriented while Scleroglossa are chemically-oriented, given that Iguania doubles Scleroglossa in the frequency of glands. Our phylogenetic analyses identified stabilizing selection as the best model describing follicular gland diversification, and revealed high rates of disparity. We provide the first global-scale analysis investigating the diversification of one of the main forms of communication among reptiles, presenting a macroevolutionary angle to questions traditionally explored at microevolutionary scale.

/pdf/macroevolutionary-diversification-of-glands-for-chemical-64da932ux7.pdf

Macroevolutionary diversification of glands for chemical communication in squamate reptiles

Sophisticated vocal communication systems of birds and mammals, including human speech, are characterized by a high degree of plasticity in which signals are individually adjusted in response to changes in the environment. Here, we present, to our knowledge, the first evidence for vocal plasticity in a reptile. Like birds and mammals, tokay geckos (Gekko gecko) increased the duration of brief call notes in the presence of broadcast noise compared to quiet conditions, a behaviour that facilitates signal detection by receivers. By contrast, they did not adjust the amplitudes of their call syllables in noise (the Lombard effect), which is in line with the hypothesis that the Lombard effect has evolved independently in birds and mammals. However, the geckos used a different strategy to increase signal-to-noise ratios: instead of increasing the amplitude of a given call type when exposed to noise, the subjects produced more high-amplitude syllable types from their repertoire. Our findings demonstrate that reptile vocalizations are much more flexible than previously thought, including elaborate vocal plasticity that is also important for the complex signalling systems of birds and mammals. We suggest that signal detection constraints are one of the major forces driving the evolution of animal communication systems across different taxa.

https://royalsocietypublishing.org/doi/pdf/10.1098/rspb.2017.0451

Vocal plasticity in a reptile

We provide a detailed description of the rutting vocalisations of free-ranging male Iberian deer (Cervus elaphus hispanicus, Hilzheimer 1909), a geographically isolated and morphologically differentiated subspecies of red deer Cervus elaphus. We combine spectrographic examinations, spectral analyses and automated classifications to identify different call types, and compare the composition of the vocal repertoire with that of other red deer subspecies. Iberian stags give bouts of roars (and more rarely, short series of barks) that are typically composed of two different types of calls. Long Common Roars are mostly given at the beginning or at the end of the bout, and are characterised by a high fundamental frequency (F0) resulting in poorly defined formant frequencies but a relatively high amplitude. In contrast, Short Common Roars are typically given in the middle or at the end of the bout, and are characterised by a lower F0 resulting in relatively well defined vocal tract resonances, but low amplitude. While we did not identify entirely Harsh Roars (as described in the Scottish red deer subspecies (Cervus elaphus scoticus)), a small percentage of Long Common Roars contained segments of deterministic chaos. We suggest that the evolution of two clearly distinct types of Common Roars may reflect divergent selection pressures favouring either vocal efficiency in high pitched roars or the communication of body size in low-pitched, high spectral density roars highlighting vocal tract resonances. The clear divergence of the Iberian red deer vocal repertoire from those of other documented European red deer populations reinforces the status of this geographical variant as a distinct subspecies.

/pdf/roaring-high-and-low-composition-and-possible-functions-of-16j5sn61cv.pdf

Roaring high and low: composition and possible functions of the Iberian stag's vocal repertoire.

Most amphibians and reptiles produce sounds with a larynx containing a pair of vocal cords. Clicking and hissing are common in both groups whereas tonal sounds are found most frequently in anurans and geckos. Calls can exceed 90 dB SPL at a distance of 1 m and they can have fundamental frequencies above 20 kHz. Calling is used mostly by males for courtship and territorial displays. Offspring and females call to synchronize hatching and to mediate maternal care. Adults and juveniles in many groups produce hissing when threatened. Amphibians and reptiles include more than 17,000 species. As a result of this diversity, major advances in the field of vocalization are made through exploratory research but also through careful experimentation and the use of novel technologies. Combining the study of vocal and auditory systems is important to explain issues such as the diversity of frequency tuning in the group. Many questions can also be answered through comparative studies in amphibians and reptiles because these groups have evolved independent solutions to common communication problems.

Vocal Sound Production and Acoustic Communication in Amphibians and Reptiles

Reptiles from all major phylogenetic radiations—turtles, lizards, snakes, and crocodilians—respond, both physiologically and behaviorally, to auditory stimuli. There is considerable variation in the auditory frequency response range among different reptilian groups, though the underlying biophysical and neurological bases for these differences are poorly known. In some reptiles the auditory neural processing appears to have reasonably discrete low- and high-frequency components. In these reptiles, which include some lizards and crocodilians, vocal communication has evolved multiple times; associated with this vocal communication is a diversity of intraspecific behaviors including territoriality, parental care, and courtship. In other reptiles, most notably, but not exclusively, the snakes, the response to high-frequency stimuli has been lost. Vocal communication is rare in these taxa and plays little to no part in intraspecific behaviors. The commonality of low-frequency auditory responses across reptiles is associated with a common, and very generalized, avoidance response.

Reptile Auditory Neuroethology: What Do Reptiles Do with Their Hearing?

Geographic variations in vocalizations and morphological characteristics of the tokay gecko (Gekko gecko L.) complex were identified using subjects recorded and/or collected in China and Southeast Asia. Populations in south China and northeast Vietnam (the black tokay) were compared with those in Thailand, Laos and south Vietnam (the red tokay). Red tokays possess gray- or dark green-colored skin with brick red spots interspersed on the dorsum, while black tokays possess dark-green skin with black spots or spots of other colors except brick red. Each group produces advertisement calls which consist of distinct acoustic phases. In both groups the first call phase consists of a series of pulses and the second phase consists of a series of two-note syllables. Only red tokays produce a third phase consisting of single notes. Frequency modulation patterns were profoundly different for call elements produced between the two groups. Calls of the black but not red tokay exhibit intricate frequency modulated eleme...

Geographic variation in the advertisement calls of Gekko gecko in relation to variations in morphological features: implications for regional population differentiation

X. Yu

Papers

Geographic variation in the advertisement calls of Gekko gecko in relation to variations in morphological features: implications for regional population differentiation