Historical Processes and Genetic Implications of Limb Reduction and Loss in an Island Skink Lineage

Abstract

Evolutionary simplification, or loss of complex characters, is a major theme in studies of body form evolution. The apparently infrequent evolutionary reacquisition of complex characters has led to the assertion (Dollo's Law) that once lost, complex characters may be impossible to re-evolve, at least via the exact same evolutionary process. The spectacular, virtually endemic radiation of Philippine semi-fossorial skinks of the genus Brachymeles represent one of the few radiations of scincid lizards to possess both fully limbed and limbless species. And yet, nothing is known of the phylogenetic relationships of this exceptional group. Morphologically similar body plans have made it difficult to assess species-level diversity, and the genus has long been recognized as one of the more modest radiations of southeast Asian lizards. However, taxonomic studies indicate that the diversity within the genus Brachymeles is grossly underestimated. Here I provide one of the most comprehensive, fine-scale analyses of squamate body-form evolution to date, introducing a new model system of closely related, morphologically variable, lizards. In this study I provide the first robust estimate of phylogenetic relationships within the genus Brachymeles using a multi-locus dataset and nearly complete taxonomic sampling. Systematic revisions guided by robust estimates of phylogeny subsequently result in a 125% increase in species diversity. I provide statistical tests of monophyly for all polytypic species and two widespread limb-reduced species and our results indicate wholesale deviations from past summaries and taxonomic evaluations of the genus. A Bayesian reconstruction of ancestral areas indicates strong statistical support for a minimum of five major dispersal events that have given rise to a major component of the observed species diversity across the archipelago. Our phylogenetic results support independent instances of complete limb loss as well as multiple instances of digit and external ear opening loss and re-acquisition. Even more striking, I find strong statistical support for the re-acquisition of a pentadactyl body form from a digit-reduced ancestor. Our findings have broad, general implications for body form evolution in burrowing vertebrates: whatever constraints have shaped trends in morphological evolution among other squamate groups (excluding Bipes) have been lost in this one exemplary clade.