SUMMARYNeural crest cells (NCCs) comprise a multipotent, migratory cell population that generates a diverse array of cell and tissue types during vertebrate development. These include cartilage and bone, tendons, and connective tissue, as well as neurons, glia, melanocytes, and endocrine and adipose cells; this remarkable lineage potential persists into adult life. Taken together with a limited capacity for self-renewal, neural crest cells bear the hallmarks of stem and progenitor cells and are considered to be synonymous with vertebrate evolution. The neural crest has provided a system for exploring the mechanisms that govern developmental processes such as morphogenetic induction, cell migration, and fate determination. Today, much of the focus on neural crest cells revolves around their stem cell-like characteristics and potential for use in regenerative medicine. A thorough understanding of the signals and switches that govern mammalian neural crest patterning is central to potential therapeutic application of these cells and better appreciation of the role that neural crest cells play in vertebrate evolution, development, and disease.

A central issue in biology concerns the presence, timing and nature of phylotypic periods of development, but whether, when and why species exhibit conserved morphologies remains unresolved. Here, we construct a developmental morphospace to show that amniote faces share a period of reduced shape variance and convergent growth trajectories from prominence formation through fusion, after which phenotypic diversity sharply increases. We predict in silico the phenotypic outcomes of unoccupied morphospaces and experimentally validate in vivo that observed convergence is not due to developmental limits on variation but instead from selection against novel trajectories that result in maladaptive facial clefts. These results illustrate how epigenetic factors such as organismal geometry and shape impact facial morphogenesis and alter the locus of adaptive selection to variation in later developmental events.

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.