How lizards turn into snakes: A phylogenetic analysis of body-form evolution in anguid lizards

One of the most striking morphological transformations in vertebrate evolution is the transition from a lizardlike body form to an elongate, limbless (snakelike) body form. Despite its dramatic nature, this transition has occurred repeatedly among closely related species (especially in squamate reptiles), making it an excellent system for studying macroevolutionary transformations in body plan. In this paper, we examine the evolution of body form in the lizard family Anguidae, a clade in which multiple independent losses of limbs have occurred. We combine a molecular phylogeny for 27 species, our morphometric data, and phylogenetic comparative methods to provide the first statistical phylogenetic tests of several long-standing hypotheses for the evolution of snakelike body form. Our results confirm the hypothesized relationships between body elongation and limb reduction and between limb reduction and digit reduction. However, we find no support for the hypothesized sequence going from body elongation to limb reduction to digit loss, and we show that a burrowing lifestyle is not a necessary correlate of limb loss. We also show that similar degrees of overall body elongation are achieved in two different ways in anguids, that these different modes of elongation are associated with different habitat preferences, and that this dichotomy in body plan and ecology is widespread in limb-reduced squamates. Finally, a recent developmental study has proposed that the transition from lizardlike to snakelike body form involves changes in the expression domains of midbody Hox genes, changes that would link elongation and limb loss and might cause sudden transformations in body form. Our results reject this developmental model and suggest that this transition involves gradual changes occurring over relatively long time scales.