Deirdre C. Lyons

The significance and scope of evolutionary developmental biology: A vision for the 21st century

Evolutionary developmental biology (evo‐devo) has undergone dramatic transformations since its emergence as a distinct discipline. This paper aims to highlight the scope, power, and future promise of evo‐devo to transform and unify diverse aspects of biology. We articulate key questions at the core of eleven biological disciplines—from Evolution, Development, Paleontology, and Neurobiology to Cellular and Molecular Biology, Quantitative Genetics, Human Diseases, Ecology, Agriculture and Science Education, and lastly, Evolutionary Developmental Biology itself—and discuss why evo‐devo is uniquely situated to substantially improve our ability to find meaningful answers to these fundamental questions. We posit that the tools, concepts, and ways of thinking developed by evo‐devo have profound potential to advance, integrate, and unify biological sciences as well as inform policy decisions and illuminate science education. We look to the next generation of evolutionary developmental biologists to help shape this process as we confront the scientific challenges of the 21st century.

The significance and scope of evolutionary developmental biology

Evolutionary developmental biology (evo‐devo) has undergone dramatic transformations since its emergence as a distinct discipline. This paper aims to highlight the scope, power, and future promise of evo‐devo to transform and unify diverse aspects of biology. We articulate key questions at the core of eleven biological disciplines—from Evolution, Development, Paleontology, and Neurobiology to Cellular and Molecular Biology, Quantitative Genetics, Human Diseases, Ecology, Agriculture and Science Education, and lastly, Evolutionary Developmental Biology itself—and discuss why evo‐devo is uniquely situated to substantially improve our ability to find meaningful answers to these fundamental questions. We posit that the tools, concepts, and ways of thinking developed by evo‐devo have profound potential to advance, integrate, and unify biological sciences as well as inform policy decisions and illuminate science education. We look to the next generation of evolutionary developmental biologists to help shape this process as we confront the scientific challenges of the 21st century.

Cleavage pattern and fate map of the mesentoblast, 4d, in the gastropod Crepidula: a hallmark of spiralian development

BackgroundAnimals with a spiral cleavage program, such as mollusks and annelids, make up the majority of the superphylum Lophotrochozoa. The great diversity of larval and adult body plans in this group emerges from this highly conserved developmental program. The 4d micromere is one of the most conserved aspects of spiralian development. Unlike the preceding pattern of spiral divisions, cleavages within the 4d teloblastic sublineages are bilateral, representing a critical transition towards constructing the bilaterian body plan. These cells give rise to the visceral mesoderm in virtually all spiralians examined and in many species they also contribute to the endodermal intestine. Hence, the 4d lineage is an ideal one for studying the evolution and diversification of the bipotential endomesodermal germ layer in protostomes at the level of individual cells. Little is known of how division patterns are controlled or how mesodermal and endodermal sublineages diverge in spiralians. Detailed modern fate maps for 4d exist in only a few species of clitellate annelids, specifically in glossiphoniid leeches and the sludge worm Tubifex. We investigated the 4d lineage in the gastropod Crepidula fornicata, an established model system for spiralian biology, and in a closely related direct-developing species, C. convexa.ResultsHigh-resolution cell lineage tracing techniques were used to study the 4d lineage of C. fornicata and C. convexa. We present a new nomenclature to name the progeny of 4d, and report the fate map for the sublineages up through the birth of the first five pairs of teloblast daughter cells (when 28 cells are present in the 4d sublineage), and describe each clone’s behavior during gastrulation and later stages as these undergo differentiation. We identify the precise origin of the intestine, two cells of the larval kidney complex, the larval retractor muscles and the presumptive germ cells, among others. Other tissues that arise later in the 4d lineage include the adult heart, internal foot tissues, and additional muscle and mesenchymal cells derived from later-born progeny of the left and right teloblasts. To test whether other cells can compensate for the loss of these tissues (that is, undergo regulation), specific cells were ablated in C. fornicata.ConclusionsOur results present the first fate map of the 4d micromere sublineages in a mollusk. The fate map reveals that endodermal and mesodermal fates segregate much later than previously thought. We observed little evidence of regulation between sublineages, consistent with a lineage-driven cell specification process. Our results provide a framework for comparisons with other spiralians and lay the groundwork for investigation of the molecular mechanisms of endomesoderm formation, germ line segregation and bilateral differentiation in Crepidula.

Branching out: origins of the sea urchin larval skeleton in development and evolution.

It is a challenge to understand how the information encoded in DNA is used to build a three‐dimensional structure. To explore how this works the assembly of a relatively simple skeleton has been examined at multiple control levels. The skeleton of the sea urchin embryo consists of a number of calcite rods produced by 64 skeletogenic cells. The ectoderm supplies spatial cues for patterning, essentially telling the skeletogenic cells where to position themselves and providing the factors for skeletal growth. Here, we describe the information known about how this works. First the ectoderm must be patterned so that the signaling cues are released from precise positions. The skeletogenic cells respond by initiating skeletogenesis immediately beneath two regions (one on the right and the other on the left side). Growth of the skeletal rods requires additional signaling from defined ectodermal locations, and the skeletogenic cells respond to produce a membrane‐bound template in which the calcite crystal grows. Important in this process are three signals, fibroblast growth factor, vascular endothelial growth factor, and Wnt5. Each is necessary for explicit tasks in skeleton production. genesis 52:173–185.

Morphogenesis in sea urchin embryos: linking cellular events to gene regulatory network states

Gastrulation in the sea urchin begins with ingression of the primary mesenchyme cells (PMCs) at the vegetal pole of the embryo. After entering the blastocoel the PMCs migrate, form a syncitium, and synthesize the skeleton of the embryo. Several hours after the PMCs ingress the vegetal plate buckles to initiate invagination of the archenteron. That morphogenetic process occurs in several steps. The nonskeletogenic cells produce the initial inbending of the vegetal plate. Endoderm cells then rearrange and extend the length of the gut across the blastocoel to a target near the animal pole. Finally, cells that will form part of the midgut and hindgut are added to complete gastrulation. Later, the stomodeum invaginates from the oral ectoderm and fuses with the foregut to complete the archenteron.

Deployment of regulatory genes during gastrulation and germ layer specification in a model spiralian mollusc Crepidula

Background: During gastrulation, endoderm and mesoderm are specified from a bipotential precursor (endomesoderm) that is argued to be homologous across bilaterians. Spiralians also generate mesoderm from ectodermal precursors (ectomesoderm), which arises near the blastopore. While a conserved gene regulatory network controls specification of endomesoderm in deuterostomes and ecdysozoans, little is known about genes controlling specification or behavior of either source of spiralian mesoderm or the digestive tract. Results: Using the mollusc Crepidula, we examined conserved regulatory factors and compared their expression to fate maps to score expression in the germ layers, blastopore lip, and digestive tract. Many genes were expressed in both ecto‐ and endomesoderm, but only five were expressed in ectomesoderm exclusively. The latter may contribute to epithelial‐to‐mesenchymal transition seen in ectomesoderm. Conclusions: We present the first comparison of genes expressed during spiralian gastrulation in the context of high‐resolution fate maps. We found variation of genes expressed in the blastopore lip, mouth, and cells that will form the anus. Shared expression of many genes in both mesodermal sources suggests that components of the conserved endomesoderm program were either co‐opted for ectomesoderm formation or that ecto‐ and endomesoderm are derived from a common mesodermal precursor that became subdivided into distinct domains during evolution. Developmental Dynamics 244:1215–1248, 2015.

Spiralian gastrulation: germ layer formation, morphogenesis, and fate of the blastopore in the slipper snail Crepidula fornicata

BackgroundGastrulation is a critical step in bilaterian development, directly linked to the segregation of germ layers, establishment of axes, and emergence of the through-gut. Theories about the evolution of gastrulation often concern the fate of the blastopore (site of endomesoderm internalization), which varies widely in a major branch of bilaterians, the Spiralia. In this group, the blastopore has been said to become the mouth, the anus, both, or neither. Different developmental explanations for this variation exist, yet no modern lineage tracing study has ever correlated the position of cells surrounding the blastopore with their contribution to tissues of the mouth, foregut, and anus in a spiralian. This is the first study to do so, using the gastropod Crepidula fornicata.ResultsCrepidula gastrulation occurs by epiboly: the first through third quartet micromeres form an epithelial animal cap that expands to cover vegetal endomesodermal precursors. Initially, descendants of the second and third quartet micromeres (2a–2d, 3a–3d) occupy a portion of the blastopore lip. As the blastopore narrows, the micromeres’ progeny exhibit lineage-specific behaviors that result in certain sublineages leaving the lip’s edge. Anteriorly, cells derived from 3a2 and 3b2 undergo a unique epithelial-to-mesenchymal transition involving proliferation and a collective movement of cells into the archenteron. These cells make a novel spiralian germ layer, the ectomesoderm. Posteriorly, cells derived from 3c2 and 3d2 undergo a form of convergence and extension that involves zippering of cells and their intercalation across the ventral midline. During this process, several of these cells, as well as the 2d clone, become displaced posteriorly, away from the blastopore. Progeny of 2a-2c and 3a-3d make the mouth and foregut, and the blastopore becomes the opening to the mouth. The anus forms days later, as a secondary opening within the 2d2 clone, and not from the classically described “anal cells”, which we identify as the 3c221 and 3d221 cells.ConclusionsOur analysis of Crepidula gastrulation constitutes the first description of blastopore lip morphogenesis and fates using lineage tracing and live imaging. These data have profound implications for hypotheses about the evolution of the bilaterian gut and help explain observed variation in blastopore morphogenesis among spiralians.

Ins and outs of Spiralian gastrulation

Gastrulation is a critical stage of metazoan development during which endodermal and mesodermal tissues are internalized, and morphogenesis transforms the early embryo into each animals unique body-plan. While gastrulation has been studied extensively in classic model systems such as flies, worms, and vertebrates, less is known about gastrulation at a mechanistic level in other taxa. Surprisingly, one particularly neglected group constitutes a major branch of animals: the Spiralia. A unique feature of spiralian development is that taxa with diverse adult body-plans, such as annelids, molluscs, nemerteans and platyhelminths all share a highly stereotyped suite of characters during embryogenesis called spiral cleavage. The spiral cleavage program makes it possible to compare distantly related embryos using not only morphological features, and gene expression patterns, but also homologous cell lineages. Having all three criteria available for comparison is especially critical for understanding the evolution of a complex process like gastrulation. Thus studying gastrulation in spiralians is likely to lead to novel insights about the evolution of body-plans, and the evolution of morphogenesis itself. Here we review relevant literature about gastrulation in spiralians and frame questions for future studies. We describe the internalization of the endoderm, endomesoderm and ectomesoderm; where known, we review data on the cellular and molecular control of those processes. We also discuss several morphogenetic events that are tied to gastrulation including: axial elongation, origins of the mouth and anus, and the fate of the blastopore. Since spiral cleavage is ancestral for a major branch of bilaterians, understanding gastrulation in spiralians will contribute more broadly to ongoing debates about animal body-plan divergence, such as: the origin of the through-gut, the emergence of indirect versus direct development, and the evolution of gene-regulatory networks that specify endomesoderm. We emphasize the fact that spiralian gastrulation provides the unique opportunity to connect well-defined embryonic cell lineages to variation in cell fate and cell behavior, making it an exceptional case study for evo-devo.

Specification to Biomineralization: Following a Single Cell Type as It Constructs a Skeleton

The sea urchin larva is shaped by a calcite endoskeleton. That skeleton is built by 64 primary mesenchyme cells (PMCs) in Lytechinus variegatus. The PMCs originate as micromeres due to an unequal fourth cleavage in the embryo. Micromeres are specified in a well-described molecular sequence and enter the blastocoel at a precise time using a classic epithelial-mesenchymal transition. To make the skeleton, the PMCs receive signaling inputs from the overlying ectoderm, which provides positional information as well as control of the growth of initial skeletal tri-radiates. The patterning of the skeleton is the result both of autonomous inputs from PMCs, including production of proteins that are included in the skeletal matrix, and of non-autonomous dynamic information from the ectoderm. Here, we summarize the wealth of information known about how a PMC contributes to the skeletal structure. The larval skeleton is a model for understanding how information encoded in DNA is translated into a three-dimensional crystalline structure.

Left-right asymmetry in the sea urchin embryo: BMP and the asymmetrical origins of the adult.

The entire adult sea urchin develops on the left side of the larva. This Primer discusses a new study that reports that BMP signalling activates this process while Nodal signalling inhibits it on the larvas right side.