Abstract

Foraging mode plays a pivotal role in traditional reconstructions of squamate evolution. Transitions between modes are said to spark concerted changes in the morphology, physiology, behaviour, and life history of lizards. With respect to their sensory systems, species that adopt a sit-and-wait strategy are thought to rely on visual cues primarily, while actively hunting species would predominantly use chemical information. The morphology of the tongue and the vomeronasal-organs is believed to mirror this dichotomy. Still, support for this idea of concerted evolution of the morphology of the lizard sensory system merely originates from studies comparing only a few, distantly related taxa that differ in many aspects of their biology besides foraging mode. Hence, we compared vomeronasal-lingual morphology among closely related lizard species (Lacertidae). Our findings show considerable interspecific variation indicating that the chemosensory system of lacertids has undergone substantial change over a short evolutionary time. Although our results imply independent evolution of tongue and vomeronasal-organ form, we find evidence for co-variation between sampler and sensor, hinting towards an ‘optimization’ for efficient chemoreception. Furthermore, our findings suggest species’ degree of investment in chemical signalling, and not foraging behaviour, as a leading factor driving the diversity in vomeronasal-lingual morphology among lacertid species.

Highlights

  • Squamate reptiles strongly rely on chemical cues to find food and to avoid predators, and many use chemical signals to communicate with hetero- or conspecifics

  • Squamate ‘vomerolfaction’ is mediated by ‘tongue-flicking’ behaviour in which the tongue samples substrate-bound or air-born chemicals in the environment and delivers them to the paired vomeronasal organs (VNOs) above the roof of the mouth[6]. Unlike those of other vertebrates, the paired VNOs of squamates have lost their anatomical connection to the main olfactory system completely, and they operate as autonomous chemosensory organs[7,8,9]

  • Of all measures taken on the lizard tongues and VNOs, only tonguefork score (TFS), tongue elongation (Telong) and VNOthick did not show a significant relationship with head length

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Summary

Introduction

Squamate reptiles (lizards and snakes) strongly rely on chemical cues to find food and to avoid predators, and many use chemical signals to communicate with hetero- or conspecifics. Squamate ‘vomerolfaction’ is mediated by ‘tongue-flicking’ behaviour in which the tongue samples substrate-bound or air-born chemicals in the environment and delivers them to the paired vomeronasal organs (VNOs) above the roof of the mouth[6]. A deeply forked tongue is hypothesized to permit efficient prey-searching by tropotaxis; that is the ability to sample and sense relative signal strength from each side of the body separately and simultaneously[19] These strongly bifid tongues are often highly elongated, which is believed to increase the protrusibility and flexibility of the tongue[3]. Strongly bifid tongues (specialized for vomerolfaction) have large VNOs, with large mushroom bodies and sensory-rich vomeronasal epithelia They tongue-flick at higher rates and sample larger volumes of air while doing so[5,17,29]

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