Digit evolution in gymnophthalmid lizards

Abstract

Background The tetrapod limb is a highly diverse structure, and reduction of the limbs accounts for much of the phenotypes observed within species. Squamate reptiles represent one of the many lineages in which the limbs have been greatly modified from the pentadactyl generalized pattern; within the group, limb-reduced morphologies can vary from minor reductions in size of elements to complete limblessness, with several intermediate forms in between. Even though limb reduction is widespread, it is not clear what are the evolutionary and developmental mechanisms involved in the formation of reduced limb morphologies. Methods In this study, we present an overview of limb morphology within the microteiid lizard group Gymnophthalmidae, focusing on digit number. Results We show that there are two major groups of limb-reduced gymnophthalmids. The first group is formed by lizard-like - and frequently pentadactyl - species, in which minor reductions (such as the loss of 1-2 phalanges mainly in digits I and V) are the rule; these morphologies generally correspond to those seen in other squamates. The second group is formed by species showing more drastic losses, which can include the absence of an externally distinct limb in adults. We also show the expression patterns of Sonic Hedgehog (Shh) in the greatly reduced fore and hindlimb of a serpentiform gymnophthalmid. Conclusions Our discussion focus on identifying shared patterns of limb reduction among tetrapods, and explaining these patterns and the morphological variation within the gymnophthalmids based on the current knowledge of the molecular signaling pathways that coordinate limb development.

Convergent and lineage-specific genomic differences in limb regulatory elements in limbless reptile lineages

“…To increase the power to analyze genomic changes associated with limb loss in reptiles, we sequenced the genomes of a pair of Gymnophthalmidae lizards. Gymnophthalmid lizards are endemic to Central and South America and exhibit limb morphologies ranging from fully developed limbs to varied degrees of digit and fore/hindlimb reductions and, finally, to complete loss of limbs (Brandley et al, 2008;Roscito et al, 2014). For sequencing, we selected Calyptommatus sinebrachiatus (sand microteiid), a lizard showing no external forelimbs and only a vestigial, single-digit hindlimb, and Tretioscincus oriximinensis (Oriximina lizard), a species that exhibits fully developed pentadactyl limbs (Figure 1A).…”

“…Few of these enhancers show lineage-specific divergence at the sequence and the TFBS level (indicated by an asterisk in Figures 4B and 4C). Interestingly, among the limb enhancers diverged in the sand microteiid, which lacks external forelimbs (Roscito et al, 2014), is an enhancer associated with TBX5 (Figure 5), a gene required for forelimb development (Agarwal et al, 2003).…”

Evolutionary Developmental Biology (Evo‐Devo) Research in Latin America

“…Another example of extreme body shape transformation that has been studied using nonmodel organisms is the convergent evolution of snakelike forms in Neotropical Squamata (lizards, snakes, and amphisbaenians), which involve limb reduction or loss along with an increase in the number of trunk vertebrae. Comparative anatomical and molecular studies suggest that convergent forms do not necessarily involve the same evolutionary changes in developmental processes and genetic pathways (Waters, ; Roscito et al., ; Singarete et al., ). Changes in the anatomy of the musculoskeletal system associated with limbless morphologies and epigenetic effects of reduced mobility on limb development have also been studied for anurans (Abdala and Ponssa, ; Abdala et al., ).…”

“…Studies related to heterochrony, allometry, and modularity include geographic variations of body size adapted to local climate or habitat in gymnophthalmid lizards (Grizante et al., ), evolution of larval and juvenile development and allometry in secondary sexual characters of crabs (Flores et al., ; Flores and Negreiros‐Fransozo, ; Negreiros‐Fransozo et al., ), digit length ratios, locomotor performance, and sexual dimorphism in iguanian lizards (Gomes and Kohlsdorf, ), modulatory gene network regulation of tooth number in mammalian dentition (Line, ), variation of cranial shape and structure number in mammals (Monteiro et al., ; Shirai and Marroig, ; Giannini, ; Koyabu et al., ), muscle identity and attachments during human digit evolution and development (Diogo et al., ), or mammalian cortical development and brain size evolution (Montiel et al., , ). Studies related to evolutionary novelties or losses include evolution of transparent eyelids in lizards (Guerra‐Fuentes et al., ), evolution of jaw abductor muscles, tooth variation, and limblessness in snakes (Zaher, ; Zaher and Prudente, ; Zaher and Rieppel, ; Apesteguía and Zaher ; Zaher et al., ), evolution of limb bone elements in turtles (Fabrezi et al., ), or loss of digits and limb reduction in gymnophthalmid lizards (Roscito and Rodrigues, ; Roscito et al., ). Separate but often complementary lines of research take advantage of the growing wealth of genomic data to explore the molecular evolution of different gene families and their role in morphological and physiological adaptation, such as evolution of Hox genes and the origins of limbless morphologies in amphibians and reptiles (Singarete et al., ), origin and evolvability in PAX genes involved in embryonic development and organogenesis (Paixao‐Cortes et al., , ), nonvertebrate origins of retinoic acid involved in vertebrate development and homeostasis (Simoes‐Costa et al., ), genes involved in olfactory behaviors (Lavagnino et al., ) or in hybrid incompatibility (Mensch et al., ) in flies, hemoglobin diversification in teleost fish (Opazo et al., ), and comparative genomics of cetaceans (Nery et al., ).…”

You Can't Run, but You Can Hide: The Skeleton of the Sand‐Swimmer LizardCalyptommatus leiolepis(Squamata: Gymnophthalmidae)

“…Among gymnophthalmids that show limb reduction, there are two extreme morphologies when considering tail length: (1) forelimbs greater in size than the hind limbs and with a very long tail (e.g., Bachia ) and (2) forelimbs missing and hindlimbs reduced, and with a short tail (e.g., Calyptommatus ) (Rodrigues, ; Pellegrino et al, ; Jerez et al, ). In between these extremes, there is a wide range of variation on digit morphology and phalangeal formulae (Roscito et al, ), and limb attenuation, especially in the genus Bachia , which is strongly correlated with the increase of presacral vertebrae (i.e., forelimb and hindlimbs become shorter as the number of presacral vertebrae increases, Presh, ).…”