Differential gene expression is the core of development, mediating the genetic changes necessary for determining cell identity. The regulation of gene activity by cis-acting elements (e.g., ...enhancers) is a crucial mechanism for determining differential gene activity by precise control of gene expression in embryonic space and time. Modifications to regulatory regions can have profound impacts on phenotype, and therefore developmental and evolutionary biologists have increasingly focused on elucidating the transcriptional control of genes that build and pattern body plans. Here, we trace the evolutionary history of transcriptional control of three loci key to vertebrate appendage development (Fgf8, Shh, and HoxD/A). Within and across these regulatory modules, we find both complex and flexible regulation in contrast with more fixed enhancers that appear unchanged over vast timescales of vertebrate evolution. The transcriptional control of vertebrate appendage development was likely already incredibly complex in the common ancestor of fish, implying that subtle changes to regulatory networks were more likely responsible for alterations in phenotype rather than the de novo addition of whole regulatory domains. Finally, we discuss the dangers of relying on inter-species transgenesis when testing enhancer function, and call for more controlled regulatory swap experiments when inferring the evolutionary history of enhancer elements.
A Jurassic salamander, Beiyanerpeton jianpingensis (gen. et sp. nov.), from a recently found site in western Liaoning Province, China is the earliest known record of Salamandroidea. As a Late ...Jurassic record of the group, it extends the range of the clade by approximately 40 Ma. The Late Jurassic taxon is neotenic and represented by exceptionally preserved specimens, including fully articulated cranial and postcranial skeletons and bony gill structures close to the cheek region. The fossil beds, consisting of dark-brown volcanic ash shales of the Upper Jurassic Tiaojishan (Lanqi) Formation (Oxfordian), underlie trachyandesite rocks that have yielded a SHRIMP zircon U-Pb date of 157 ± 3 Ma. The fossiliferous beds are substantially older than the Jehol Group, including the Yixian Formation (40Ar/39Ar dates of 122–129 Ma), but slightly younger than the Middle Jurassic Daohugou horizon (40Ar/39Ar date of 164 ± 4 Ma). The early fossil taxon shares with extant salamandroids derived character states, including: separated nasals lacking a midline contact, angular fused to the prearticular in the lower jaw, and double-headed ribs on the presacral vertebrae. In contrast to extant salamandroids, however, the salamander shows a discrete and tooth-bearing palatine, and unequivocally nonpedicellate and monocuspid marginal teeth in large and presumably mature individuals. The finding provides insights into the evolution of key characters of salamanders, and also provides direct evidence supporting the hypothesis that the split between Cryptobranchoidea and Salamandroidea had taken placed before the Late Jurassic Oxfordian time. In this aspect, both paleontological and molecular data now come to agree.
To connect human biology to fish biomedical models, we sequenced the genome of spotted gar (Lepisosteus oculatus), whose lineage diverged from teleosts before teleost genome duplication (TGD). The ...slowly evolving gar genome has conserved in content and size many entire chromosomes from bony vertebrate ancestors. Gar bridges teleosts to tetrapods by illuminating the evolution of immunity, mineralization and development (mediated, for example, by Hox, ParaHox and microRNA genes). Numerous conserved noncoding elements (CNEs; often cis regulatory) undetectable in direct human-teleost comparisons become apparent using gar: functional studies uncovered conserved roles for such cryptic CNEs, facilitating annotation of sequences identified in human genome-wide association studies. Transcriptomic analyses showed that the sums of expression domains and expression levels for duplicated teleost genes often approximate the patterns and levels of expression for gar genes, consistent with subfunctionalization. The gar genome provides a resource for understanding evolution after genome duplication, the origin of vertebrate genomes and the function of human regulatory sequences.
Deep conservation of wrist and digit enhancers in fish Gehrke, Andrew R.; Schneider, Igor; de la Calle-Mustienes, Elisa ...
Proceedings of the National Academy of Sciences - PNAS,
01/2015, Letnik:
112, Številka:
3
Journal Article
Recenzirano
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Significance The fossil record shows that the wrist and digits have an aquatic origin, becoming recognizable in a group of (mostly extinct) fish that contained robust fins. Do the fins of living ...fishes have the equivalent of these structures? Because comparisons of fin and limb morphology have been inconclusive, we sought to investigate this question using developmental and molecular data. By utilizing a nonmodel fish (the spotted gar), we find that the regulatory networks that control “wrist and digit”-building genes ( Hox ) are deeply conserved between fish and tetrapods. The genomic architecture described here defines Hox gene activity in fins and limbs as equivalent, in turn suggesting equivalence between the distal bones of fish fins and the wrist and/or digits of tetrapods.
There is no obvious morphological counterpart of the autopod (wrist/ankle and digits) in living fishes. Comparative molecular data may provide insight into understanding both the homology of elements and the evolutionary developmental mechanisms behind the fin to limb transition. In mouse limbs the autopod is built by a “late” phase of Hoxd and Hoxa gene expression, orchestrated by a set of enhancers located at the 5′ end of each cluster. Despite a detailed mechanistic understanding of mouse limb development, interpretation of Hox expression patterns and their regulation in fish has spawned multiple hypotheses as to the origin and function of “autopod” enhancers throughout evolution. Using phylogenetic footprinting, epigenetic profiling, and transgenic reporters, we have identified and functionally characterized hoxD and hoxA enhancers in the genomes of zebrafish and the spotted gar, Lepisosteus oculatus , a fish lacking the whole genome duplication of teleosts. Gar and zebrafish “autopod” enhancers drive expression in the distal portion of developing zebrafish pectoral fins, and respond to the same functional cues as their murine orthologs. Moreover, gar enhancers drive reporter gene expression in both the wrist and digits of mouse embryos in patterns that are nearly indistinguishable from their murine counterparts. These functional genomic data support the hypothesis that the distal radials of bony fish are homologous to the wrist and/or digits of tetrapods.
The diversification of paired appendages has been a major factor in the evolutionary radiation of vertebrates. Despite its importance, an understanding of the origin of paired appendages has remained ...elusive. To address this problem, we focused on T-box transcription factor 5 (Tbx5), a gene indispensable for pectoral appendage initiation and development. Comparison of gene expression in jawless and jawed vertebrates reveals that the Tbx5 expression in jawed vertebrates is derived in having an expression domain that extends caudal to the heart and gills. Chromatin profiling, phylogenetic footprinting, and functional assays enabled the identification of a Tbx5 fin enhancer associated with this apomorphic pattern of expression. Comparative functional analysis of reporter constructs reveals that this enhancer activity is evolutionarily conserved among jawed vertebrates and is able to rescue the finless phenotype of tbx5a mutant zebrafish. Taking paleontological evidence of early vertebrates into account, our results suggest that the gain of apomorphic patterns of Tbx5 expression and regulation likely contributed to the morphological transition from a finless to finned condition at the base of the vertebrate lineage.
Pelvic girdle and fin of Tiktaalik roseae Shubin, Neil H.; Daeschler, Edward B.; Jenkins, Farish A.
Proceedings of the National Academy of Sciences - PNAS,
01/2014, Letnik:
111, Številka:
3
Journal Article
Recenzirano
Odprti dostop
A major challenge in understanding the origin of terrestrial vertebrates has been knowledge of the pelvis and hind appendage of their closest fish relatives. The pelvic girdle and appendage of ...tetrapods is dramatically larger and more robust than that of fish and contains a number of structures that provide greater musculoskeletal support for posture and locomotion. The discovery of pelvic material of the finned elpistostegalian, Tiktaalik roseae , bridges some of these differences. Multiple isolated pelves have been recovered, each of which has been prepared in three dimensions. Likewise, a complete pelvis and partial pelvic fin have been recovered in association with the type specimen. The pelves of Tiktaalik are paired and have broad iliac processes, flat and elongate pubes, and acetabulae that form a deep socket rimmed by a robust lip of bone. The pelvis is greatly enlarged relative to other finned tetrapodomorphs. Despite the enlargement and robusticity of the pelvis of Tiktaalik , it retains primitive features such as the lack of both an attachment for the sacral rib and an ischium. The pelvic fin of Tiktaalik (NUFV 108) is represented by fin rays and three endochondral elements: other elements are not preserved. The mosaic of primitive and derived features in Tiktaalik reveals that the enhancement of the pelvic appendage of tetrapods and, indeed, a trend toward hind limb-based propulsion have antecedents in the fins of their closest relatives.
Wrists, ankles and digits distinguish tetrapod limbs from fins, but direct evidence on the origin of these features has been unavailable. Here we describe the pectoral appendage of a member of the ...sister group of tetrapods, Tiktaalik roseae, which is morphologically and functionally transitional between a fin and a limb. The expanded array of distal endochondral bones and synovial joints in the fin of Tiktaalik is similar to the distal limb pattern of basal tetrapods. The fin of Tiktaalik was capable of a range of postures, including a limb-like substrate-supported stance in which the shoulder and elbow were flexed and the distal skeleton extended. The origin of limbs probably involved the elaboration and proliferation of features already present in the fins of fish such as Tiktaalik.
Tetrapods evolved from sarcopterygian fishes in the Devonian and were the first vertebrates to colonize land. The locomotor component of this transition can be divided into four major events: ...terrestriality, the origins of digited limbs, solid substrate-based locomotion, and alternating gaits that use pelvic appendages as major propulsors. As the sister group to tetrapods, lungfish are a morphologically and phylogenetically relevant sarcopterygian taxon for understanding the order in which these events occurred. We found that a species of African lungfish (Protopterus annectens) uses a range of pelvic fin-driven, tetrapod-like gaits, including walking and bounding, in an aquatic environment, despite having a derived limb endoskeleton and primitively small, muscularly supported pelvis. Surprisingly, given these morphological traits, P. annectens also lifts its body clear of the substrate using its pelvic fins, an ability thought to be a tetrapod innovation. Our findings suggest that some fundamental features of tetrapod locomotion, including pelvic limb gait patterns and substrate association, probably arose in sarcopterygians before the origin of digited limbs or terrestriality. It follows that the attribution of some of the nondigited Devonian fossil trackways to limbed tetrapods may need to be revisited.
The axial skeleton of Tiktaalik roseae Stewart, Thomas A; Lemberg, Justin B; Hillan, Emily J ...
Proceedings of the National Academy of Sciences - PNAS,
2024-Apr-09, Letnik:
121, Številka:
15
Journal Article
Recenzirano
Odprti dostop
The axial columns of the earliest limbed vertebrates show distinct patterns of regionalization as compared to early tetrapodomorphs. Included among their novel features are sacral ribs, which provide ...linkage between the vertebral column and pelvis, contributing to body support and propulsion by the hindlimb. Data on the axial skeletons of the closest relatives of limbed vertebrates are sparce, with key features of specimens potentially covered by matrix. Therefore, it is unclear in what sequence and under what functional context specializations in the axial skeletons of tetrapods arose. Here, we describe the axial skeleton of the elpistostegalian
and show that transformations to the axial column for head mobility, body support, and pelvic fin buttressing evolved in finned vertebrates prior to the origin of limbs. No atlas-axis complex is observed; however, an independent basioccipital-exoccipital complex suggests increased mobility at the occipital vertebral junction. While the construction of vertebrae in
is similar to early tetrapodomorphs, its ribs possess a specialized sacral domain. Sacral ribs are expanded and ventrally curved, indicating likely attachment to the expanded iliac blade of the pelvis by ligamentous connection. Thus, the origin of novel rib types preceded major alterations to trunk vertebrae, and linkage between pelvic fins and axial column preceded the origin of limbs. These data reveal an unexpected combination of post-cranial skeletal characters, informing hypotheses of body posture and movement in the closest relatives of limbed vertebrates.