Changes in Hox genes’ structure and function during the evolution of the squamate body plan (original) (raw)
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Developmental Biology, 2009
It is generally assumed that the characteristic deregionalized body plan of species with a snake-like morphology evolved through a corresponding homogenization of Hox gene expression domains along the primary axis. Here, we examine the expression of Hox genes in snake embryos and show that a collinear pattern of Hox expression is retained within the paraxial mesoderm of the trunk. Genes expressed at the anterior and most posterior, regionalized, parts of the skeleton correspond to the expected anatomical boundaries. Unexpectedly however, also the dorsal (thoracic), homogenous rib-bearing region of trunk, is regionalized by unconventional gradual anterior limits of Hox expression that are not obviously reflected in the skeletal anatomy. In the lateral plate mesoderm we also detect regionalized Hox expression yet the forelimb marker Tbx5 is not restricted to a rudimentary forelimb domain but is expressed throughout the entire flank region. Analysis of several Hox genes in a caecilian amphibian, which convergently evolved a deregionalized body plan, reveals a similar global collinear pattern of Hox expression. The differential expression of posterior, vertebra-modifying or even rib-suppressing Hox genes within the dorsal region is inconsistent with the homogeneity in vertebral identity. Our results suggest that the evolution of a deregionalized, snake-like body involved not only alterations in Hox gene cis-regulation but also a different downstream interpretation of the Hox code.
Evolution of the snake body form reveals homoplasy in amniote Hox gene function
Hox genes regulate regionalization of the axial skeleton of vertebrates, and changes in their expression have been proposed to be a fundamental mechanism driving the evolution of new body forms. The origin of the snake-like body form, with its deregionalized pre-cloacal axial skeleton, has been explained as either homogenization of Hox gene expression domains, or retention of standard vertebrate Hox domains with alteration of downstream expression that suppresses development of distinct regions. Both models assume a highly regionalized ancestor, but the extent of deregionalization of the primaxial domain (vertebrae, dorsal ribs) of the skeleton in snake-like body forms has never been analyzed. Here we combine geometric morphometrics and maximum likelihood to show that the pre-cloacal primaxial domain of elongate, limb-reduced lizards and snakes is not deregionalized compared to limbed taxa, and the phylogenetic structure of primaxial morphology in reptiles does not support a loss of regionalization in the evolution of snakes. We demonstrate that morphometric regional boundaries correspond to mapped gene expression domains in snakes, suggesting their primaxial domain is patterned by a normally functional Hox code. Comparison of primaxial osteology in fossil and modern amniotes with Hox gene distributions within Amniota indicates that a functional, sequentially expressed Hox code patterned a subtle morphological gradient along the anterior-posterior axis in stem members of amniote clades and extant lizards, including snakes. The highly regionalized skeletons of extant archosaurs and mammals result from independent evolution in the Hox code and do not represent ancestral conditions for clades with snake-like body forms. The developmental origin of snakes is best explained by decoupling of the primaxial and abaxial domains and increases in somite number, not by changes in function of primaxial Hox genes.
Deep time perspective on turtle neck evolution: chasing the Hox code by vertebral morphology
The unparalleled ability of turtle neck retraction is possible in three different modes, which characterize stem turtles, living side-necked (Pleurodira), and hidden-necked (Cryptodira) turtles, respectively. Despite the conservatism in vertebral count among turtles, there is significant functional and morphological regionalization in the cervical vertebral column. Since Hox genes play a fundamental role in determining the differentiation in vertebra morphology and based on our reconstruction of evolutionary genetics in deep time, we hypothesize genetic differences among the turtle groups and between turtles and other land vertebrates. We correlated anterior Hox gene expression and the quantifiable shape of the vertebrae to investigate the morphological modularity in the neck across living and extinct turtles. This permitted the reconstruction of the hypothetical ancestral Hox code pattern of the whole turtle clade. The scenario of the evolution of axial patterning in turtles indicates shifts in the spatial expression of HoxA-5 in relation to the reduction of cervical ribs in modern turtles and of HoxB-5 linked with a lower morphological differentiation between the anterior cervical vertebrae observed in cryptodirans. By comparison with the mammalian pattern, we illustrate how the fixed count of eight cervical vertebrae in turtles resulted from the emergence of the unique turtle shell.
Somitogenesis and Axial Development in Reptiles
Methods in molecular biology (Clifton, N.J.), 2017
Among amniote vertebrates, reptiles display the greatest variation in axial skeleton morphology. Only recently have they been used in gene expression studies of somitogenesis , challenging previous assumptions about the segmentation clock and axial patterning. An increasing number of reptile genomes and transcriptomes are becoming available as next-generation sequencing becomes more affordable. Information regarding gene sequence and structure can be used to design and synthesize labeled riboprobes by in vitro transcription for gene expression analysis by in situ hybridization, thus, enabling the characterization of spatial and temporal expression patterns of genes involved in somitogenesis, a topic of great interest within evolutionary developmental studies of vertebrates.
Homeotic shift at the dawn of the turtle evolution
All derived turtles are characterized by one of the strongest reductions of the dorsal elements among Amniota, and have only 10 dorsal and eight cervical vertebrae. I demonstrate that the Late Triassic turtles, which represent successive stages of the shell evolution, indicate that the shift of the boundary between the cervical and dorsal sections of the vertebral column occurred over the course of several million years after the formation of complete carapace. The more generalized reptilian formula of at most seven cervicals and at least 11 dorsals is thus plesiomorphic for Testudinata. The morphological modifications associated with an anterior homeotic change of the first dorsal vertebra towards the last cervical vertebra in the Triassic turtles are partially recapitulated by the reduction of the first dorsal vertebra in crown-group Testudines, and they resemble the morphologies observed under laboratory conditions resulting from the experimental changes of Hox gene expression patterns. This homeotic shift hypothesis is supported by the, unique to turtles, restriction of Hox-5 expression domains, somitic precursors of scapula, and brachial plexus branches to the cervical region, by the number of the marginal scute-forming placodes, which was larger in the Triassic than in modern turtles, and by phylogenetic analyses.
Turtle isochore structure is intermediate between amphibians and other amniotes
Integrative and Comparative Biology, 2008
Synopsis Vertebrate genomes are comprised of isochores that are relatively long (4100 kb) regions with a relatively homogenous (either GC-rich or AT-rich) base composition and with rather sharp boundaries with neighboring isochores. Mammals and living archosaurs (birds and crocodilians) have heterogeneous genomes that include very GC-rich isochores. In sharp contrast, the genomes of amphibians and fishes are more homogeneous and they have a lower overall GC content. Because DNA with higher GC content is more thermostable, the elevated GC content of mammalian and archosaurian DNA has been hypothesized to be an adaptation to higher body temperatures. This hypothesis can be tested by examining structure of isochores across the reptilian clade, which includes the archosaurs, testudines (turtles), and lepidosaurs (lizards and snakes), because reptiles exhibit diverse body sizes, metabolic rates, and patterns of thermoregulation. This study focuses on a comparative analysis of a new set of expressed genes of the red-eared slider turtle and orthologs of the turtle genes in mammalian (human, mouse, dog, and opossum), archosaurian (chicken and alligator), and amphibian (western clawed frog) genomes. EST (expressed sequence tag) data from a turtle cDNA library enriched for genes that have specialized functions (developmental genes) revealed using the GC content of the thirdcodon-position to examine isochore structure requires careful consideration of the types of genes examined. The more highly expressed genes (e.g., housekeeping genes) are more likely to be GC-rich than are genes with specialized functions. However, the set of highly expressed turtle genes demonstrated that the turtle genome has a GC content that is intermediate between the GC-poor amphibians and the GC-rich mammals and archosaurs. There was a strong correlation between the GC content of all turtle genes and the GC content of other vertebrate genes, with the slope of the line describing this relationship also indicating that the isochore structure of turtles is intermediate between that of amphibians and other amniotes. These data are consistent with some thermal hypotheses of isochore evolution, but we believe that the credible set of models for isochore evolution still includes a variety of models. These data expand the amount of genomic data available from reptiles upon which future studies of reptilian genomics can build. From the symposium ''Reptile Genomics and Evolutionary Genetics'' presented at the annual meeting of the Society for Integrative and