Jeffrey R. Thompson

Reorganization of sea urchin gene regulatory networks at least 268 million years ago as revealed by oldest fossil cidaroid echinoid

Echinoids, or sea urchins, are rare in the Palaeozoic fossil record, and thus the details regarding the early diversification of crown group echinoids are unclear. Here we report on the earliest probable crown group echinoid from the fossil record, recovered from Permian (Roadian-Capitanian) rocks of west Texas, which has important implications for the timing of the divergence of crown group echinoids. The presence of apophyses and rigidly sutured interambulacral areas with two columns of plates indicates this species is a cidaroid echinoid. The species, Eotiaris guadalupensis, n. sp. is therefore the earliest stem group cidaroid. The occurrence of this species in Roadian strata pushes back the divergence of cidaroids and euechinoids, the clades that comprise all living echinoids, to at least 268.8 Ma, ten million years older than the previously oldest known cidaroid. Furthermore, the genomic regulation of development in echinoids is amongst the best known, and this new species informs the timing of large-scale reorganization in echinoid gene regulatory networks that occurred at the cidaroid-euechinoid divergence, indicating that these changes took place by the Roadian stage of the Permian.

Juvenile skeletogenesis in anciently diverged sea urchin clades

Mechanistic understanding of evolutionary divergence in animal body plans devolves from analysis of those developmental processes that, in forms descendant from a common ancestor, are responsible for their morphological differences. The last common ancestor of the two extant subclasses of sea urchins, i.e., euechinoids and cidaroids, existed well before the Permian/Triassic extinction (252 mya). Subsequent evolutionary divergence of these clades offers in principle a rare opportunity to solve the developmental regulatory events underlying a defined evolutionary divergence process. Thus (i) there is an excellent and fairly dense (if yet incompletely analyzed) fossil record; (ii) cladistically confined features of the skeletal structures of modern euechinoid and cidaroid sea urchins are preserved in fossils of ancestral forms; (iii) euechinoids and cidaroids are among current laboratory model systems in molecular developmental biology (here Strongylocentrotus purpuratus [Sp] and Eucidaris tribuloides [Et]); (iv) skeletogenic specification in sea urchins is uncommonly well understood at the causal level of interactions of regulatory genes with one another, and with known skeletogenic effector genes, providing a ready arsenal of available molecular tools. Here we focus on differences in test and perignathic girdle skeletal morphology that distinguish all modern euechinoid from all modern cidaroid sea urchins. We demonstrate distinct canonical test and girdle morphologies in juveniles of both species by use of SEM and X-ray microtomography. Among the sharply distinct morphological features of these clades are the internal skeletal structures of the perignathic girdle to which attach homologous muscles utilized for retraction and protraction of Aristotles׳ lantern and its teeth. We demonstrate that these structures develop de novo between one and four weeks after metamorphosis. In order to study the underlying developmental processes, a method of section whole mount in situ hybridization was adapted. This method displays current gene expression in the developing test and perignathic girdle skeletal elements of both Sp and Et juveniles. Active, specific expression of the sm37 biomineralization gene in these muscle attachment structures accompanies morphogenetic development of these clade-specific features in juveniles of both species. Skeletogenesis at these clade-specific muscle attachment structures displays molecular earmarks of the well understood embryonic skeletogenic GRN: thus the upstream regulatory gene alx1 and the gene encoding the vegfR signaling receptor are both expressed at the sites where they are formed. This work opens the way to analysis of the alternative spatial specification processes that were installed at the evolutionary divergence of the two extant subclasses of sea urchins.

Facies distribution and taphonomy of echinoids from the Fort Payne Formation (late osagean, early Viséan, Mississippian) of Kentucky

Abstract. Paleozoic echinoids are exceptionally rare, and little is known of their paleoenvironmental distribution. The echinoid fauna of the Fort Payne Formation (Late Osagean, Early Viséan) of south-central Kentucky is documented. Four genera, ?Archaeocidaris, Lepidocidaris, ?Lepidesthes, and an unidentified lepidocentrid, were recovered and represent three different families. This fauna, and their associated paleoenvironments, give important new insights into the facies distribution of Paleozoic echinoids and the taphonomic biases that affect this distribution. Lepidocidaris is known from the green shale facies, which comprises the core of Fort Paynes carbonate buildups. ?Archaeocidaris and the lepidocentrid are known from the wackestone buildups and crinoidal packstone buildups. ?Lepidesthes is also known from crinoidal packstone and wackestone buildups, which argues against a semi-infaunal life mode for this taxon. All relatively semiarticulated echinoids were known from autochthonous facies, whereas the only echinoids from the allochthonous facies were disarticulated hemipyramids. Furthermore, deeper-water carbonate buildups were apparently capable of supporting diverse echinoid faunas during the Viséan.

Ancestral state reconstruction by comparative analysis of a GRN kernel operating in echinoderms

Diverse sampling of organisms across the five major classes in the phylum Echinodermata is beginning to reveal much about the structure and function of gene regulatory networks (GRNs) in development and evolution. Sea urchins are the most studied clade within this phylum, and recent work suggests there has been dramatic rewiring at the top of the skeletogenic GRN along the lineage leading to extant members of the euechinoid sea urchins. Such rewiring likely accounts for some of the observed developmental differences between the two major subclasses of sea urchins—cidaroids and euechinoids. To address effects of topmost rewiring on downstream GRN events, we cloned four downstream regulatory genes within the skeletogenic GRN and surveyed their spatiotemporal expression patterns in the cidaroid Eucidaris tribuloides. We performed phylogenetic analyses with homologs from other non-vertebrate deuterostomes and characterized their spatiotemporal expression by quantitative polymerase chain reaction (qPCR) and whole-mount in situ hybridization (WMISH). Our data suggest the erg–hex–tgif subcircuit, a putative GRN kernel, exhibits a mesoderm-specific expression pattern early in Eucidaris development that is directly downstream of the initial mesodermal GRN circuitry. Comparative analysis of the expression of this subcircuit in four echinoderm taxa allowed robust ancestral state reconstruction, supporting hypotheses that its ancestral function was to stabilize the mesodermal regulatory state and that it has been co-opted and deployed as a unit in mesodermal subdomains in distantly diverged echinoderms. Importantly, our study supports the notion that GRN kernels exhibit structural and functional modularity, locking down and stabilizing clade-specific, embryonic regulatory states.

A diverse assemblage of Permian echinoids (Echinodermata, Echinoidea) and implications for character evolution in early crown group echinoids

Abstract. The Permian is regarded as one of the most crucial intervals during echinoid evolution because crown group echinoids are first widely known from the Permian. New faunas provide important information regarding the diversity of echinoids during this significant interval as well as the morphological characterization of the earliest crown group and latest stem group echinoids. A new fauna from the Capitanian Lamar Member of the Bell Canyon Formation in the Guadalupe Mountains of West Texas comprises at least three new taxa, including Eotiaris guadalupensis Thompson n. sp. an indeterminate archaeocidarid, and Pronechinus? sp. All specimens represented are silicified and known from disarticulated or semiarticulated interambulacral and ambulacral plates and spines. This assemblage is one of the most diverse echinoid assemblages known from the Permian and, as such, informs the paleoecological setting in which the earliest crown group echinoids lived. This new fauna indicates that crown group echinoids occupied the same environments as stem group echinoids of the Archaeocidaridae and Proterocidaridae. Furthermore, the echinoids described herein begin to elucidate the order of character transitions that likely took place between stem group and crown group echinoids. At least one of the morphological innovations once thought to be characteristic of early crown group echinoids, crenulate tubercles, was in fact widespread in a number of stem group taxa from the Permian as well. Crenulate tubercles are reported from two taxa, and putative cidaroid style U-shaped teeth are present in the fauna. The presence of crenulate tubercles in the archaeocidarid indicates that crenulate tubercles were present in stem group echinoids, and thus the evolution of this character likely preceded the evolution of many of the synapomorphies that define the echinoid crown group.

Paleogenomics of echinoids reveals an ancient origin for the double-negative specification of micromeres in sea urchins

Establishing a timeline for the evolution of novelties is a common, unifying goal at the intersection of evolutionary and developmental biology. Analyses of gene regulatory networks (GRNs) provide the ability to understand the underlying genetic and developmental mechanisms responsible for the origin of morphological structures both in the development of an individual and across entire evolutionary lineages. Accurately dating GRN novelties, thereby establishing a timeline for GRN evolution, is necessary to answer questions about the rate at which GRNs and their subcircuits evolve, and to tie their evolution to paleoenvironmental and paleoecological changes. Paleogenomics unites the fossil record and all aspects of deep time, with modern genomics and developmental biology to understand the evolution of genomes in evolutionary time. Recent work on the regulatory genomic basis of development in cidaroid echinoids, sand dollars, heart urchins, and other nonmodel echinoderms provides an ideal dataset with which to explore GRN evolution in a comparative framework. Using divergence time estimation and ancestral state reconstructions, we have determined the age of the double-negative gate (DNG), the subcircuit which specifies micromeres and skeletogenic cells in Strongylocentrotus purpuratus. We have determined that the DNG has likely been used for euechinoid echinoid micromere specification since at least the Late Triassic. The innovation of the DNG thus predates the burst of post-Paleozoic echinoid morphological diversification that began in the Early Jurassic. Paleogenomics has wide applicability for the integration of deep time and molecular developmental data, and has wide utility in rigorously establishing timelines for GRN evolution.

A new stem group echinoid from the Triassic of China leads to a revised macroevolutionary history of echinoids during the end-Permian mass extinction

The Permian–Triassic bottleneck has long been thought to have drastically altered the course of echinoid evolution, with the extinction of the entire echinoid stem group having taken place during the end-Permian mass extinction. The Early Triassic fossil record of echinoids is, however, sparse, and new fossils are paving the way for a revised interpretation of the evolutionary history of echinoids during the Permian–Triassic crisis and Early Mesozoic. A new species of echinoid, Yunnanechinus luopingensis n. sp. recovered from the Middle Triassic (Anisian) Luoping Biota fossil Lagerstätte of South China, displays morphologies that are not characteristic of the echinoid crown group. We have used phylogenetic analyses to further demonstrate that Yunnanechinus is not a member of the echinoid crown group. Thus a clade of stem group echinoids survived into the Middle Triassic, enduring the global crisis that characterized the end-Permian and Early Triassic. Therefore, stem group echinoids did not go extinct during the Palaeozoic, as previously thought, and appear to have coexisted with the echinoid crown group for at least 23 million years. Stem group echinoids thus exhibited the Lazarus effect during the latest Permian and Early Triassic, while crown group echinoids did not.