Adam Skinner

Rapid and repeated limb loss in a clade of scincid lizards

BackgroundThe 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.ResultsThe 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.ConclusionThe 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.

Rate Heterogeneity, Ancestral Character State Reconstruction, and the Evolution of Limb Morphology in Lerista (Scincidae, Squamata)

Rates of phenotypic evolution derive from numerous interrelated processes acting at varying spatial and temporal scales and frequently differ substantially among lineages. Although current models employed in reconstructing ancestral character states permit independent rates for distinct types of transition (forward and reverse transitions and transitions between different states), these rates are typically assumed to be identical for all branches in a phylogeny. In this paper, I present a general model of character evolution enabling rate heterogeneity among branches. This model is employed in assessing the extent to which the assumption of uniform transition rates affects reconstructions of ancestral limb morphology in the scincid lizard clade Lerista and, accordingly, the potential for rate variability to mislead inferences of evolutionary patterns. Permitting rate variation among branches significantly improves model fit for both the manus and the pes. A constrained model in which the rate of digit acquisition is assumed to be effectively zero is strongly supported in each case; when compared with a model assuming unconstrained transition rates, this model provides a substantially better fit for the manus and a nearly identical fit for the pes. Ancestral states reconstructed assuming the constrained model imply patterns of limb evolution differing significantly from those implied by reconstructions for uniform-rate models, particularly for the pes; whereas ancestral states for the uniform-rate models consistently entail the reacquisition of pedal digits, those for the model incorporating among-lineage rate heterogeneity imply repeated, unreversed digit loss. These results indicate that the assumption of identical transition rates for all branches in a phylogeny may be inappropriate in modeling the evolution of phenotypic traits and emphasize the need for careful evaluation of phylogenetic tests of Dollos law.

Tikiguania and the antiquity of squamate reptiles (lizards and snakes)

Tikiguania estesi is widely accepted to be the earliest member of Squamata, the reptile group that includes lizards and snakes. It is based on a lower jaw from the Late Triassic of India, described as a primitive lizard related to agamids and chamaeleons. However, Tikiguania is almost indistinguishable from living agamids; a combined phylogenetic analysis of morphological and molecular data places it with draconines, a prominent component of the modern Asian herpetofauna. It is unlikely that living agamids have retained the Tikiguania morphotype unchanged for over 216 Myr; it is much more conceivable that Tikiguania is a Quaternary or Late Tertiary agamid that was preserved in sediments derived from the Triassic beds that have a broad superficial exposure. This removes the only fossil evidence for lizards in the Triassic. Studies that have employed Tikiguana for evolutionary, biogeographical and molecular dating inferences need to be reassessed.

Testing fossil calibrations for vertebrate molecular trees

Lee, M. S. Y. & Skinner, A. (2011). Testing fossil calibrations for vertebrate molecular trees. —Zoologica Scripta, 40, 538–543.

Body-form Evolution in the Scincid Lizard Clade Lerista and the Mode of Macroevolutionary Transitions

The scincid lizard clade Lerista provides an exceptional model for studying the mode of substantial evolutionary transformations, comprising more than 90 species displaying a remarkable variety of body forms. Patterns of character evolution in this clade, inferred from reconstructed ancestral states, are at least partly consistent with the correlated progression model of macroevolutionary change. At each stage in the transition to a highly elongate, limb-reduced body plan, alterations to the lengths of the forelimb and hind limb are accompanied by compensatory changes in snout-vent length (or vice versa), preserving locomotory ability. Nonetheless, there is evidence for moderate dissociation of hind limb evolution in some lineages, while tail length has evolved effectively independently of the substantial alterations to the lengths of the body and limbs. This indicates a significant role of evolutionary and developmental modularity in the divergence of body form within Lerista, and emphasises the potential variability of the strength of functional constraints within organisms and among lineages. Trends toward a highly elongate, functionally limbless body plan may be attributed primarily to a combination of the interdependence of changes in snout-vent length and limb lengths and the very low probability of re-elaborating structurally reduced limbs. Similar asymmetries in the probabilities of interrelated phenotypic changes may be a significant cause of evolutionary trends resulting in the emergence of higher taxa.

Plausibility of inferred ancestral phenotypes and the evaluation of alternative models of limb evolution in scincid lizards.

Phylogenetic approaches to inferring ancestral character states are becoming increasingly sophisticated; however, the potential remains for available methods to yield strongly supported but inaccurate ancestral state estimates. The consistency of ancestral states inferred for two or more characters affords a useful criterion for evaluating ancestral trait reconstructions. Ancestral state estimates for multiple characters that entail plausible phenotypes when considered together may reasonably be assumed to be reliable. However, the accuracy of inferred ancestral states for one or more characters may be questionable where combined reconstructions imply implausible phenotypes for a proportion of internal nodes. This criterion for assessing reconstructed ancestral states is applied here in evaluating inferences of ancestral limb morphology in the scincid lizard clade Lerista. Ancestral numbers of digits for the manus and pes inferred assuming the models that best fit the data entail ancestral digit configurations for many nodes that differ fundamentally from configurations observed among known species. However, when an alternative model is assumed for the pes, inferred ancestral digit configurations are invariably represented among observed phenotypes. This indicates that a suboptimal model for the pes (and not the model providing the best fit to the data) yields accurate ancestral state estimates.

Hierarchy and monophyly

In a series of recent papers, Pleijel (1999) and Pleijel and Rouse (2000a,b, 2003) have proposed that systematists should disregard species, advocating a nomenclatural system in which the smallest recoverable clades (termed least-inclusive taxonomic units, or LITUs) are recognized as basic taxonomic entities. Among the arguments presented in support of their proposal, Pleijel and Rouse contend that most contemporary species definitions are inappropriate in systematics as they permit species to be non-monophyletic. As an example, they cite the finding of Talbot and Shields (1996) that Ursus maritimus has a sister-group relationship to some insular demes of U. arctos. Pleijel and Rouse (2000a; p. 628) regard arctos as paraphyletic (since it does not include all descendants of an ancestral deme) and argue that in recognizing arctos and maritimus as separate (exclusive) taxa, systematists unacceptably neglect historical information. The issue of monophyly has figured prominently in discussion on the species category, with several earlier authors (e.g., Rosen, 1979; Mishler and Brandon, 1987; de Queiroz and Donoghue, 1988) having suggested that monophyly could (or should) be employed exclusively as a criterion for recognizing taxa. These authors often have appealed to the possibility of non-monophyletic species as an argument against the use of criteria such as reproductive isolation, diagnosability, etc. in species definitions (however, see de Queiroz and Donoghue, 1988 for an exception). Here, I argue that the opposition to non-monophyletic species is unfounded, stemming from a lack of consideration of the hierarchical organization of genealogical entities and their historical relations. As Grene (1969) noted, the term hierarchy has been used to denote several related but distinct concepts. For the purpose of this note, I regard as hierarchical entities or systems that may be considered to consist of a series of compositional levels, that is, ‘‘divisions of stuff ... organized by part-whole relations, in which wholes at one level function as parts at the next (and at all higher) levels’’ (Wimsatt, 1994; p. 222). An example of such a series of levels is provided by the familiar somatic hierarchy of cells, tissues, organs, and organisms; entities occupying levels earlier in this series (i.e., particular cells, tissues, etc.) constitute parts of entities occupying later levels. This use of the term hierarchy corresponds with that of ‘‘constitutive hierarchy’’ by Mayr (1982), ‘‘scalar hierarchy’’ by Salthe (1985), and ‘‘incorporative hierarchy’’ by Ghiselin (1997). There have been several hierarchies expounded in the biological literature (for a critical review, see Salthe, 1985; pp. 175–180), differing according to authors’ interests. Of concern here is the genealogical hierarchy of genes, cells, organisms, demes, and species (Eldredge and Salthe, 1984; Vrba and Eldredge, 1984; Salthe, 1985). The part-whole relations of entities at lower levels in this hierarchy, specifically those of genes, cells, and organisms, are well known; it is axiomatic that, in general, organisms have cells as parts and cells have genes as parts. The part-whole relations of demes and species, however, are more obscure. Frost and Kluge (1994) have argued cogently that species should be equated with largest population lineages, integrated by interbreeding and isolated reproductively (whether extrinsically or intrinsically) from other lineages. According to this view, species are ‘‘composed of reticulating sublineages [i.e., demes] and toko-genetically related organisms’’ (Frost and Kluge, 1994; p. 275) unified by interbreeding, and thus occupy a compositional level above demic and organismal levels. The part-whole relations of organisms, demes, and species conceived of are illustrated (fortuitously) by Simpson’s (1955) ‘‘diagram of phylogenetic patterns’’ (his fig. 48). At each level in the genealogical hierarchy entities share historical (genealogical) relations as a result of The applicability of the concept of monophyly to systems in which relationships are to a significant extent reticulating, specifically those based on the descent of biparental organisms and demes, has been a topic of substantial disagreement among systematists (compare, for example, the views of de Queiroz and Donoghue, 1990 and Nixon and Wheeler, 1990). If we consider that monophyly is the relation obtaining among an ancestor and all of its descendants, then ‘‘anything that has descendants [including biparental organisms and demes] ... is the originator of a monophyletic entity’’ (de Queiroz and Donoghue, 1990; p. 70). This perspective, adopted here, implies that monophyletic groups may intersect where relationships are reticulating. E-mail address: skinner.adam@saugov.sa.gov.au Cladistics 20 (2004) 498–500 Cladistics

Limb Abnormalities in Two Species of Lerista (Scincidae, Squamata)

This article presents a survey of phenotypic variation in the limbs of two species of Lerista, a diverse clade of Australian scincid lizards widely considered to provide the best available model for studying squamate limb reduction and loss. Abnormalities were observed in 4.1% of forelimbs and 5.4% of hind limbs in the tetradactyl species L. dorsalis, and 4.5% of forelimbs and 2.4% of hind limbs in the tridactyl species L. timida. Substantial malformation of the manus or pes, involving the complete absence or severe reduction of all digits, accounts for a considerable proportion of anomalies in both species. Almost all remaining anomalies involve the absence or severe reduction of one or two digits. Despite the moderate frequency of limb abnormalities recorded, no cases of supernumerary digits were observed. Patterns of phenotypic variation in both species are consistent with the conventional perspective that substantial limb reduction is effectively irreversible, and provide support for the conclusion that structurally reduced limbs have not been re-elaborated in Lerista.