Rapid and repeated limb loss in a clade of scincid lizards

Abstract

Background: The Australian scincid clade Lerista provides perhaps the best available model for studying limb reduction in squamates (lizards and snakes), comprising more than 75 species displaying a remarkable variety of digit configurations, from pentadactyl to entirely limbless conditions. We investigated the pattern and rate of limb reduction and loss in Lerista, employing a comprehensive phylogeny inferred from nucleotide sequences for a nuclear intron and six mitochondrial genes.

Results: The inferred phylogeny reveals extraordinary evolutionary mutability of limb morphology in Lerista. Ancestral state reconstructions indicate at least ten independent reductions in the number of digits from a pentadactyl condition, with a further seven reductions proceeding independently from a tetradactyl condition derived from one of these reductions. Four independent losses of all digits are inferred, three from pentadactyl or tetradactyl conditions. These conclusions are not substantially affected by uncertainty in assumed rates of character state transition or the phylogeny. An estimated age of 13.4 million years for Lerista entails that limb reduction has occurred not only repeatedly, but also very rapidly. At the highest rate, complete loss of digits from a pentadactyl condition is estimated to have occurred within 3.6 million years.

Conclusion: The exceptionally high frequency and rate of limb reduction inferred for Lerista emphasise the potential for rapid and substantial alteration of body form in squamates. An absence of compelling evidence for reversals of digit loss contrasts with a recent proposal that digits have been regained in some species of the gymnophthalmid clade Bachia, possibly reflecting an influence of differing environmental and genetic contexts on the evolution of limb morphology in these clades. Future study of the genetic, developmental, and ecological bases of limb reduction and loss in Lerista promises the elucidation of not only this phenomenon in squamates, but also the dramatic evolutionary transformations of body form that have produced the extraordinary diversity of multicellular organisms.

Figure 1

Majority-rule consensus of 5000 trees sampled after attaining stationarity in a Bayesian analysis of nucleotide sequences for 72 species of Lerista. Mean branch lengths from the Bayesian analysis have been modified via penalised likelihood rate smoothing to produce an ultrametric tree. Posterior probabilities ≥ 0.50 followed by maximum likelihood numbers of digits for the manus and pes are shown adjacent to internal nodes. Ancestral states for the manus were reconstructed assuming maximum likelihood rates of digit gain and loss; for the pes, ancestral states are those inferred assuming the maximum likelihood rate of digit loss and rates of digit gain of 0.020–0.025 (see text). Alternative numbers of pedal digits yielding a log-likelihood within two units of the optimal value (i.e., that for the maximum likelihood estimate) are presented in parentheses for ancestral digit configurations not observed among nominal species of Lerista. Modal digit configurations follow species names. Branches are coloured according to digit configuration: dark blue, 5, 5; light blue, 4, 4; light blue-green, 3, 3; green, 2, 3; light yellow-green, 2, 2; yellow, 1, 3 and 1, 2; light orange, 0, 2; dark orange, 0, 1; red, 0, 0.

Figure 2

Numbers of manual and pedal digits lost in all inferred reductions from a pentadactyl or tetradactyl condition. Each point represents the number of manual or pedal digits initially lost by an inferred pentadactyl or tetradactyl ancestor; subsequent reductions (e.g., from a tridactyl condition produced as a consequence of the initial reduction) are not presented. 'Total number of digits lost' is the number of manual and pedal digits lost in an inferred reduction. Note the overlapping symbols at (2, 1) and (4, 2).