The evolution of motor control in lizards



The study of motor control in vertebrates is one of the active areas of research in feeding functional morphology. The complex integrated feeding system of vertebrates (musculo-skeletal and neuronal components of the tongue, hyobranchium, jaws and neurocranium) is an ideal system to investigate the evolution of motor control. Motor control of feeding in vertebrates is complex and involves integration of sensory input (such as visual, tactile, olfactory, vomeronasal stimuli) into the control of feeding behaviours. It has been suggested that for cyclical, repeated behaviours in general, a simple neuromotor steering based on a centralised pattern generator exists. Although this hypothesis is largely based on studies on the locomotor apparatus, a similar control system is usually put forward for mammalian chewing cycles.

Based on large similarities between lower tetrapod and mammalian feeding cycles it was hypothesized that the evolution of feeding motor patterns across major taxonomic groups might have occurred without large modifications of the central pattern generator(s) controlling the jaw and hyolingual muscles but relatively large alterations in the peripheral feeding structures (bones, muscles, dentition). However, similarities in the feeding cycle between lizards and mammals need not always be the expression of a conserved intrinsic pattern but they can also be caused by simple functional or physical constraints. Nonetheless, there is some evidence for the existence of an underlying basic pattern in lower tetrapods as well (e.g. herbivorous lizards). However, as most vertebrates modulate the control of their feeding system in response to for example differences in prey properties, it is often difficult to determine the components of the underlying CPG. Elimination of sensory feedback using nerve transections can help to solve this problem and may provide insights into the existence of a central pattern generator. Squamates are an ideal system to test hypothese of conservation of motor control because of the variation in morphology and function of the jaw and hyolingual systems.

The specific goals of this project are 1) to investigate the presence of a central pattern generator (CPG) controlling feeding behaviour in Squamates and 2) to test hypotheses of constraint on the evolution of motor control. The data will be used to create a model for the control of food transport in an ‘ancestral lizard’ which will be compared to data available for mammals and other vertebrates.


The project can roughly be divided in five distinct research components:

  • Provide a detailed description of the structure and innervation of the jaw and hyobranchial musculature in representatives of major lizard groups (Pogona vitticeps, Chameleo calyptratus, Varanus ornatus, Tupinambis merianae, Tiliqua scincoides and Gherrosaurus major). The picture on the right shows a cleared and stained lower jaw and hyobranchium of an agamid lizard (modified after Meyers et al., 2002). The nerves have been stained using Sudan Black B.
  • Quantitative description of the movements of the jaws and hyolingual apparatus during prey transport in the same species while feeding on an array of food types. High-speed cineradiography will be used to describe the movements of the jaws and the hyobranchium during prey transport.
  • Quantitative description of the electrical activity of the jaw and hyolingual muscles in response to different prey types for the same set of species. The focus of this research component will be on the activities of the jaw opener (MDM), the external jaw adductor (MAME), the tongue protractor (MGG) and the tongue retractor (MHG). Activity patterns of these muscles will be recorded simultaneously for both sides.
  • Elimination of the sensory feedback by using nerve transection experiments to evaluate the presence of a CPG. This will be combined with cineradiographic and electromyographic records to quantify changes in control and movements after nerve transection. Here we will focus on eliminating sensory afferents from the tongue (N. glossopharyngeus and sensory components of the N. trigeminus).
  • Reconstructing the evolution of motor control and the role of sensory feedback in lizards and comparing these results with published data for mammals and other vertebrates.

    Publications

  • Herrel, A., V. Schaerlaeken, J.J. Meyers, K.A. Metzger and C.F. Ross (2007) The evolution of cranial design and performance in squamates: consequences of skull-bone reduction on feeding behavior. Integr. Comp. Biol. 47: 107-117. full text (PDF).

  • Ross, C.F., A. Eckhardt, A. Herrel, W.L. Hylander, K.A. Metzger, V. Schaerlaeken, R.L. Washington and S.H. Williams (2007) Modulation of intra-oral processing in mammals and lepidosaurs. Integr. Comp. Biol. 47: 118-136. full text (PDF).

  • Schaerlaeken, V., J.J. Meyers and A. Herrel (2007) Modulation of prey capture kinematics and the role of lingual sensory feedback in the lizard Pogona vitticeps. Zoology 110: 127-138. full text (PDF).

  • Herrel, A., V. Schaerlaeken, C.F. Ross, J.J. Meyers, K.C. Nishikawa, V. Abdala, A. Manzano and P. Aerts (2008) Electromyography and the evolution of motor control: limitations and insights. Integr. Comp. Biol. 48: 261-271. full text (PDF).

  • Schaerlaeken, V., A. Herrel and J.J. Meyers (2008) Modulation, individual variation, and the role of lingual sensory afferents in the control of prey transport in the lizard Pogona vitticeps. J. Exp. Biol 211: 2071-2078. full text (PDF).

  • Schaerlaeken, V., A. Herrel, P. Aerts and C.F. Ross (2008) The functional significance of the lower temporal bar in Sphenodon. J. Exp. Biol. 211: 3908-3914. full text (PDF).

  • Herrel, A., S.M. Deban, V. Schaerlaeken, J-P. Timmermans and D. Adriaens (2009) Are morphological specializations of the hyolingual system in chameleons and salamanders tuned to demands on performance? Physiol. Biochem. Zool. 82: 29-39. full text (PDF).

  • Herrel, A., V. Schaerlaeken, J. Moravec and C.F. Ross (2009) Sexual shape dimorphism in tuatara, ecological niche divergence or sexual selection ? Copeia 2009: 727-731.

  • Montuelle, S., A. Herrel, V. Schaerlaeken, K. A. Metzger, A. Mutuyeyezu and V. L. Bels (2009) Inertial feeding in the teiid lizard Tupinambis merianae: the effect of prey size on the movements of hyolingual apparatus and the cranio-cervical system. J. Exp. Biol. 212: 2501-2510.

  • Ross, C.F., A.L. Baden, J. Georgi, A. Herrel, K.A. Metzger, D.A. Reed, V. Schaerlaeken and M. S. Wolff (2010) Chewing variation in lepidosaurs and primates. J. Exp. Biol. 213: 572-584.

  • Schaerlaeken, V., S. J. Montuelle, P. Aerts and A. Herrel (2010) Jaw and hyolingual movements during prey transport in varanid lizards: effects of prey type. Zoology (accepted)