Abstract
BackgroundOne of the most distinctive traits found within Chamaeleonidae is their split/cleft autopodia and the simplified and divergent morphology of the mesopodial skeleton. These anatomical characteristics have facilitated the adaptive radiation of chameleons to arboreal niches. To better understand the homology of chameleon carpal and tarsal elements, the process of syndactyly, cleft formation, and how modification of the mesopodial skeleton has played a role in the evolution and diversification of chameleons, we have studied the Veiled Chameleon (Chamaeleo calyptratus). We analysed limb patterning and morphogenesis through in situ hybridization, in vitro whole embryo culture and pharmacological perturbation, scoring for apoptosis, clefting, and skeletogenesis. Furthermore, we framed our data within a phylogenetic context by performing comparative skeletal analyses in 8 of the 12 currently recognized genera of extant chameleons.ResultsOur study uncovered a previously underappreciated degree of mesopodial skeletal diversity in chameleons. Phylogenetically derived chameleons exhibit a ‘typical’ outgroup complement of mesopodial elements (with the exception of centralia), with twice the number of currently recognized carpal and tarsal elements considered for this clade. In contrast to avians and rodents, mesenchymal clefting in chameleons commences in spite of the maintenance of a robust apical ectodermal ridge (AER). Furthermore, Bmp signaling appears to be important for cleft initiation but not for maintenance of apoptosis. Interdigital cell death therefore may be an ancestral characteristic of the autopodium, however syndactyly is an evolutionary novelty. In addition, we find that the pisiform segments from the ulnare and that chameleons lack an astragalus-calcaneum complex typical of amniotes and have evolved an ankle architecture convergent with amphibians in phylogenetically higher chameleons.ConclusionOur data underscores the importance of comparative and phylogenetic approaches when studying development. Body size may have played a role in the characteristic mesopodial skeletal architecture of chameleons by constraining deployment of the skeletogenic program in the smaller and earliest diverged and basal taxa. Our study challenges the ‘re-evolution’ of osteological features by showing that ‘re-evolving’ a ‘lost’ feature de novo (contrary to Dollo’s Law) may instead be due to so called ‘missing structures’ being present but underdeveloped and/or fused to other adjacent elements (cryptic features) whose independence may be re-established under changes in adaptive selective pressure.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-015-0464-4) contains supplementary material, which is available to authorized users.
Highlights
One of the most distinctive traits found within Chamaeleonidae is their split/cleft autopodia and the simplified and divergent morphology of the mesopodial skeleton
Interdigital clefting is independent of a robust Apical Ectodermal Ridge (AER) To begin to understand the mechanisms governing the modified hand and foot morphology of chameleons, we compared autopodial development in the Veiled Chameleon to the Desert Grassland Whiptail Lizard (Teiidae: Aspidoscelis uniparens), which serves as a reference species due to its overall ‘typical’ lizard limb and body plan
It takes approximately 10 days for limb development to progress from a round digital plate to the typical pentadactyl pattern which coincides with the onset of interdigital cell death (ICD) (Fig. 2a-c, j-l)
Summary
One of the most distinctive traits found within Chamaeleonidae is their split/cleft autopodia and the simplified and divergent morphology of the mesopodial skeleton These anatomical characteristics have facilitated the adaptive radiation of chameleons to arboreal niches. Chamaeleonidae limbs have been modified from the generalized terrestrial tetrapod plan to exhibit an architecture highly adapted for an arboreal lifestyle This was facilitated through evolution of a midline autopodial cleft (ectrodactyly; Fig. 1a) and two opposable syndactylous bundles (different finger clusters between hands and feet that retain interdigital tissue) of digits that are highly mobile (zygodactyly; Fig. 1b and c). The proximal skeleton of the autopodium (the wrist and ankle, or mesopodia) was modified through a reduction in the number of bone elements Those elements that remain are enlarged and form a ball-and-socket joint between the autopodium and forearm (zeugopodium). While other lizards are arboreal (i.e., geckos, anoles), chameleons differ by using zygodactyly and gripping of branches rather than depending on claws and epidermal modifications (Fig. 1d)
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