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Developmental biology, the stem cell of biological disciplines

* E-mail: [email protected]

Affiliation Department of Biology, Swarthmore College, Swarthmore, Pennsylvania, United States of America

• Scott F. Gilbert

Published: December 28, 2017

• https://doi.org/10.1371/journal.pbio.2003691
• Reader Comments

Developmental biology (including embryology) is proposed as "the stem cell of biological disciplines.” Genetics, cell biology, oncology, immunology, evolutionary mechanisms, neurobiology, and systems biology each has its ancestry in developmental biology. Moreover, developmental biology continues to roll on, budding off more disciplines, while retaining its own identity. While its descendant disciplines differentiate into sciences with a restricted set of paradigms, examples, and techniques, developmental biology remains vigorous, pluripotent, and relatively undifferentiated. In many disciplines, especially in evolutionary biology and oncology, the developmental perspective is being reasserted as an important research program.

Citation: Gilbert SF (2017) Developmental biology, the stem cell of biological disciplines. PLoS Biol 15(12): e2003691. https://doi.org/10.1371/journal.pbio.2003691

Copyright: © 2017 Scott F. Gilbert. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: National Science Foundation https://www.nsf.gov/ (grant number IOS-145177). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: As the author of a developmental biology textbook, I acknowledge that I desire courses in developmental biology to be mandatory for all biology majors and pre-meds.

Abbreviations: iPSC, induced pluripotential stem cell; SMT, somatic mutation theory

Provenance: Commissioned; externally peer reviewed

We were finishing dinner at a conference on evolutionary developmental biology when a graduate student asked me to explain some comments I’d made during a question and answer session. I had disagreed with a colleague’s reliance on citation analysis to present a history of evolutionary developmental biology. Citation lists are political documents, I had argued. Citations don’t reveal whether a paper had influenced the author, or even whether the author had read it. Furthermore, a history of a new field should explain why the field arose. It might even have a mythos, a narrative theme for its origin story.

The student asked if my account of the history of evolutionary developmental biology had an underlying narrative and, if so, what it was. I told him something like, “Yes. If you analyze my accounts, you’ll find that there is an underlying narrative, and that narrative is ‘the return of the rightful sovereign.’ Development was originally seen as the motor of evolution, and the principal way of explaining evolution was through embryology. In fact, in the late 1800s, the word ‘evolution’ could mean either phylogenetic or embryological development. But genetics arose out of embryology, and eventually, evolution came to be seen as a proper subset of population genetics. Genetics displaced development as the way to study evolution. In my narrative, evo-devo represents the return of developmental biology to its rightful place as the means to study evolution.”

Sensing he didn’t get the connection, I continued. “The return of the rightful sovereign. Remember Errol Flynn’s Robin Hood , in which the captured monk dramatically sheds his clerical garb to reveal himself as King Richard, returned to England to correct John’s injustices?”

My dated allusion was not getting through, either. “ Game of Thrones ,” I hazarded.

“Yes!” he exclaimed, “I get it. Evo-Devo and Game of Thrones !”

As I recalled my version of developmental biology’s origin story, I pondered a larger question, which others had also noted [ 1 ]: Why and how has developmental biology, once a central focus of biology, been marginalized in our curriculum? Nobel Prizes and other awards for discoveries in developmental biology are often cast (even in scientific journals) as breakthroughs in genetics or in stem cell biology. Journal articles pertaining directly to developmental biology are often catalogued under “cancer biology,” “evolution,” or “neurobiology.” Developmental biology has even been disparaged as “old fashioned” by experts in the field who are doing it excellently, but who prefer to call it something else. In the most recent meeting of the Society for Developmental Biology, the president of the society, Blanche Capel [ 2 ], asked in her presidential address, “Did you ever think, like me, that Developmental Biology does not get the credit it deserves for its contributions to understanding the natural world?”

As should be clear by now, I have indeed wondered why developmental biology has been overlooked and am playing with a hypothesis to explain why. I propose that developmental biology (and its parent discipline, embryology) has been the stem cell of biological disciplines. It is not a “differentiated” discipline, but the pluripotent discipline that generates disciplines like genetics and immunology, all the while retaining its own identity.

(Developmental biology, it should be noted, is a twice-named discipline. In the 1950s, the term was coined by Paul Weiss and N. J. Berrill to include the parent discipline, embryology, as well as the study of adult stem cells and nonembryonic development, such as budding and regeneration. This was the impetus for the journal Developmental Biology . It was named again in the 1970s, for the annual series, Current Topics in Developmental Biology , where it was seen as the molecular approach to embryology. In both cases, “developmental biology” was viewed as the modernization and extension of embryology [ 3 ].)

So, let us begin with the cell theory. In the mid-1800s, the study of embryos gave rise to various theories of cell formation. Schleiden, Schwann, and Remak formed their cell theories to answer the question of how multicellular embryos emerged, and thus gave rise to the discipline of cytology/cell biology [ 4 – 6 ]. Today’s cell theory is largely based on the 1862 hypothesis of Robert Remak [ 7 ], who first figured out that the embryo is constructed by cell division and that all the cells of the body are descendants of the zygote. But where do these cells form? By the turn of that century, Eli Metchnikoff and other embryologists, looking for the sources and roles of the mesoderm (the middle cell layer of embryonic embryo), formulated the first approaches to immunology. Metchnikoff had found that the mesodermal cells of the starfish embryo budded off from the gut-producing endoderm and were capable of their own intracellular digestion, phagocytizing foreign bodies inserted into the larvae. His discovery led to the first hypotheses of cellular immunity [ 8 ]. Thus, by 1900, embryology had already given rise to cell biology and immunology.

Shortly thereafter, the gene theory was constructed by embryologists who had been embroiled in debates over what part of the embryo—the nucleus or the cytoplasm—controlled development. In the early 1900s, embryologists Theodor Boveri and E. B. Wilson believed that the nucleus, especially the nuclear chromosomes, carried the instructions for organismal development. In contrast, embryologist Thomas Hunt Morgan (who had written a monograph on the embryology of the frog egg) favored the cytoplasm [ 9 ]. By 1915, Morgan [ 10 ] inadvertently obtained the evidence that chromosomal genes were necessary for the production of inherited traits. (He had hoped to prove otherwise). Another embryologist, William Bateson, would later call this new field “genetics,” and Morgan [ 11 ] would formally separate the two fields, saying that genetics studied the transmission of inherited traits, whereas embryology studied their expression. While earlier genetics (the “assortment” phase) had been suggested by breeders such as Mendel, the field we now know as genetics (studying traits whose segregation and assortment can be explained by the locations of specific genes on particular chromosomes) came from the chromosomal studies of embryologists such as Morgan and Wilson, supplemented by the theoretical discussions and analyses of embryologist Theodor Boveri and Wilson’s graduate student, Walter Sutton.

As a student of both biology and religion in college, it struck me how the rise and separation of genetics from embryology, and the disparagement of the parent discipline by some of the acolytes of the new discipline, echoed the supersessionist rhetoric of Christianity as it separated from Judaism. Even more interestingly, some of the founders and critics of early genetics seemed to think so, too [ 12 ]. Morgan claimed that while geneticists kept the faith, embryologists had “run after false gods” [ 13 ]. Genetics was to replace embryology. There were many reasons for the dominance of genetics during the 20th century, not the least of which were the destruction of the Continental European laboratories during the two World Wars and the fear of mutations caused by the detonation and testing of atomic bombs [ 14 , 15 ].

As English replaced German as the language of science, so genetics replaced physiology and development, including theories of development as the motor of evolution. Early evolutionary theories, such as those of Robert Chambers and Charles Darwin’s grandfather, Erasmus, were based on embryonic development, especially developmental morphology. Chamber’s sensational and widely selling Vestiges of the Natural History of Creation was the first book “to link a developmental view of the world with evolution” [ 16 ]. Using von Baer’s principles of development, Chambers [ 17 ] argued that animal biodiversity was caused by alterations of embryonic development. In fact, Darwin explicitly viewed plant biodiversity as being predicated by alterations of floral development [ 18 ]. He also noted that natural selection could not produce the variations that provided the raw material for natural selection [ 18 – 20 ]. When Darwin’s theory was published, his contemporaries assumed that development was the motor that generated the variations that could be selected. Darwin’s continental champion, Ernst Haeckel [ 21 ] made embryology the key to phylogeny, and Darwin’s aggressive British champion, Thomas Huxley, wrote to Darwin that the differences between species could be traced back to the modifications of development. Evolutionary biologists such as Huxley and Herbert Spencer were greatly influenced by embryologist K. E. von Baer’s theories of development [ 22 , 23 ]. Indeed, when Huxley was writing [ 24 ], the word “evolution” could be used for both the individual or the species.

That view shifted with the advent of genetics. Rather than viewing evolutionary biology as the study of macroevolution, Morgan [ 11 , 25 , 26 ] would claim that only the study of intraspecies genetics was the “scientific” approach to evolution and that anything else (embryology and paleontology, to be sure) was “unscientific” and “philosophical.” He and his students carried the day (except in Russia, which viewed genetics as bourgeois metaphysics and retained an embryological view of evolution). In 1959, the centenary of Darwin’s volume, the Genetics Society of America undertook a public relations campaign to promulgate the message that Darwinism was correct because it could be fully explained by genetics. This was important because it would quiet both the Creationists in America and those scientists who favored Lysenko, the leader of Soviet biology, who embraced a Lamarckian theory of acquired heritability [ 27 ]. Embryology had given rise to the first mechanistic theories of evolution, only to be usurped by its rebellious child, genetics. Evolutionary developmental biology is now emphasizing that the emergence of new phenotypes occurs during embryonic development, and that developmental regulatory genes are crucial for evolution. Evolutionary biology cannot explain evolution by population genetics, alone. Knowledge of development is critical in explaining the origins of species. And this, as I explained to the graduate student, is the return of the rightful sovereign.

Neurobiology similarly has an embryological pedigree, and in the early 1900s, one of its biggest concerns was whether the axon was really a cellular process that extended meters in the body. Ross Granville Harrison’s inaugural tissue culture experiments [ 28 ] solved the problem by showing that the developing frog soma extended an enormous neurite. He and others also demonstrated signaling’s role in completing synapse formation and mediating the embryonic cues that guide axons from the original cell to its destined target. Through these studies of neural development, Harrison solved the problem that had so perplexed Ramón y Cajal and others who had sought to explain the patterns of neural connections in the adult body [ 29 , 30 ].

In 1859, the same year Darwin’s On the Origin of Species was published, Rudolf Virchow’s classic volume, Cellular Pathology , drew on embryology to explain pathology. Cancers, he argued, should be studied as errors of development because tumors appeared “by the same law, which regulated embryonic development” [ 31 ]. In the 1920s and 1930s, those embryonic laws were beginning to be explained by morphogenetic fields, and as early as 1935, C. H. Waddington [ 32 ] claimed that cancers could be studied as derangements of morphological fields established in the embryo. Tumors were seen as recapitulations of or truncated stages of normal development, and oncology emerged from the work of developmental biologists studying how misregulation leads to aberrant growth. During the mid-to-late 20th century, there was a fascinating reciprocal interaction between the two disciplines, as developmental biology provided mechanisms for cancer growth and cancer biology became a niche in which developmental biology could be nourished (i.e., get funding) [ 33 , 34 ]. Scientists such as T. Boveri, G. B. Pierce, and R. Auerbach used embryological means to study tumors and used tumors to study embryology. The breakthroughs in cloning were done on cancer grants to study gene regulation [ 35 ].

Yet, genetics soon assumed dominance over the field of cancer research just as it had with evolutionary biology (whose paradigms cancer biologists often propose for their own field). The founding document of the genetic (somatic mutation) theory of cancer appears to be that of Boveri [ 36 ]. Boveri was very much a cytologist and an embryologist, and he related the anomalies of cancer to those developmental anomalies caused by polyspermy and by chromosome elimination during nematode development, noting that such chromosomal rearrangements might be the cause of cancer. (Indeed, as Wunderlich [ 37 ] has shown, Boveri seems to be totally unaware of Morgan’s data for genes and did not use the term “mutation” at all. This was a later addition, probably by Morgan). The somatic mutation theory (SMT) still holds sway, claiming that cancer was due to mutations in the premalignant cell. Reviewing the embryological mechanisms of cancer, Cofre and Abdelhay [ 38 ] have recently written that “embryologists have expressed timidly” the idea that cancer can be seen as alterations of normal development and have met “with little success in leveraging the discussion that cancer could involve a set of conventional interactions used to build the embryo during morphogenesis.” However, I cannot view Barry Pierce’s [ 39 ] article “Carcinoma is to embryology as mutation is to genetics” as timid (it demands changes in the college curriculum), nor do Carlos Sonnenschein and Ana Soto, the founders of the Tissue Organizational Field Theory [ 40 , 41 ], hide the light of developmental cancer origins under a bushel. This failure to gain traction for a developmental approach to cancer is more likely due to the inability of the target to respond. But things may be changing. The basis for the allele-oriented SMT has recently been questioned [ 39 – 41 ], and the relevance of embryonic fields to cancer has been re-established [ 38 – 44 ]. Alterations in paracrine factor signaling in both the target and producer cells have been seen to initiate cancer formation, and embryonic processes such as epithelial-mesenchymal transformation are now seen as critical in metastasis. It is without question, though, that developmental biology helped establish oncology and has continued to help mold it. The rightful sovereign returns.

Having generated cell biology, immunology, genetics, neurobiology, and oncology, developmental biology still seems to be budding off new disciplines. Evolutionary developmental biology sees evolution as Huxley did, as changes in development (rather than changes in allele frequency) and focuses on the arrival of the fittest. Ecological developmental biology sees the environment as having instructive as well as permissive agency in normal development. Systems biology, which began with embryologically oriented philosophers such as Woodger and von Bertalanffy [ 45 – 47 ], attempts to fuse developmental biology, ecology, and physiology into an integrative science of becoming.

And other new disciplines are struggling to form an identity separate from their developmental parent discipline. Stem cell biology has its own meetings, its own journals, and its own professional societies, different from those of developmental biology. When Irving Weismann, one of the founders of the International Society for Stem Cell Research, became president of that organization, he threw down the gauntlet to developmental biology, saying [ 48 ],

“We are a field, a discipline, and an entire branch of science that brings new ideas, experiments, concepts, and medical translation. Like anything new, we are a threat to the established order, and at every kind of educational and research institution, to thrive, we must be recognized as entities, not as divisions of old entities.”

But it is not yet a truly independent field, as it has yet to propose anything different from developmental biology. All the articles in Stem Cell Reports are papers that would find a home in journals of developmental biology. At the moment, stem cell biology is a political, rather than an intellectual, bud from developmental biology, and it is performing important services in creating science-based educational accessibility and political guidelines, which the developmental biology societies have not done. Whether it becomes more than a medical aspect of developmental biology remains to be seen.

There are three main messages of this essay. The first is that developmental biology is not a confined, specified discipline—such as genetics, cell biology, immunology, oncology, neurobiology, and so forth. Developmental biology is not confined to any level of organization (in that genes, cells, tissues, organs, organisms, and ecosystems can each be studied developmentally). It can be studied in any species, organ system, or biome. Developmental biology remains pluripotent. The descendants of developmental biology—cell biology, genetics, immunology, neurobiology—are more differentiated and their potency much more restricted. They have boundaries. Surely, developmental biology has its own set of questions, perhaps the best questions of any science—How does the brain form? How do the bones of the arms become different from the bones of the legs, and why can’t we regenerate them like salamanders do? How do testes usually originate in people with a Y chromosome and ovaries in people with two X chromosomes? (And these are only a few of the questions in humans)—and it regenerates itself constantly as new techniques and hypotheses become available. Indeed, developmental biology has been called an “erotetic science,” differing from most other sciences in that it is driven by questions, not theories [ 49 ]. Thus, developmental biology is a stem cell discipline, one that regenerates itself while permitting some of its descendants to develop into their own fields.

The second message is that developmental biology remains a vital generative science. The induced pluripotential stem cells (iPSCs) are derived from the principles and discoveries of developmental biologists, as are the human beta-pancreatic cells now in clinical trials. The neural embryoids derived from such cells are now being used to study the mechanisms by which the Zika virus causes microcephaly. The 3D structure of chromatin and its remodeling during early mammalian development is becoming known, as are the mechanisms of X-chromosome inactivation. Developmental biology is also being expanded by identifying the interactions of the zygote-derived cells with those of symbiotic microbes to form organ gut, capillary, and immune cells. We are discovering how the turtle gets its shell and how the butterfly wing develops structural colors. We are in a new golden age of developmental biology.

The third message of this essay is that in the 21st century, many of the disciplines that had come from developmental biology are returning to a developmental framework, even if they don’t call it “developmental biology.” This is probably because developmental biology has always been a science about relationships in which context is critical [ 50 ], and the biology of the 21st century is focusing on relations, process, and context, rather than on entities. Thus, modern biology has come to the place where developmental biology has always been residing, a place of context-dependent interactions. Being relatively undifferentiated does not mean that developmental biology is immature [ 47 , 49 – 51 ]. Indeed, it is a science that was initiated with Aristotle and is now at the forefront of contemporary theories and methods. We can expect that even if developmental biology is not mentioned by name, the principles of developmental biology are becoming a framework integrating disciplines across biology.

Acknowledgments

I wish to thank Ron Amundson, Robert Auerbach, James Briscoe, Blanche Capel, David Epel, John Gearhart, Steve Klein, Alan Love, John Opitz, Larry Ruben, Sherrie Lyons, and Ken Zaret for their careful reading of this manuscript and for their insightful comments and criticisms.

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Developmental Biology

An article about Dr. Mayssa Mokalled’s research has been published by the Washington University School of Medicine

Congratulations to Mayssa Mokalled, PhD., Associate Professor in the Department of Developmental Biology and her lab on their research .

From the article publish by the Washington University School of Medicine: “A new study from Washington University School of Medicine in St. Louis maps out a detailed atlas of all the cells involved — and how they work together — in regenerating the zebrafish spinal cord. In an unexpected finding, the researchers showed that survival and adaptability of the severed neurons themselves is required for full spinal cord regeneration. Surprisingly, the study showed that stem cells capable of forming new neurons — and typically thought of as central to regeneration — play a complementary role but don’t lead the process.”

Read the full article at: Zebrafish use surprising strategy to regrow spinal cord

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Dynamics of duplicated gene regulatory networks governing cotton fiber development following polyploidy

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Cotton fiber development entails complex genome-wide gene regulatory networks (GRN) that remain mostly unexplored. Here we present integrative analyses of fiber GRNs using public RNA-seq datasets, integrated with multi-omics genomic, transcriptomic, and cistromic data. We detail the fiber co-expression dynamics and regulatory connections, validating findings with external datasets and transcription factor (TF) binding site data. We elucidate previously uncharacterized TFs that regulate genes involved in fiber-related functions and cellulose synthesis, and identify the regulatory role of two homoeologous G2-like transcription factors on fiber length. Analysis of duplicated gene expression and network relationships in allopolyploid cotton, which has two co-resident genomes (A, D), revealed novel aspects of asymmetric subgenomic developmental contributions. Whereas D-based homoeolog pairs drive higher overall gene expression from the D subgenome, TFs from the A subgenome play a preferential regulatory role in the fiber gene regulatory network. Following allopolyploid formation, it appears that the trans-regulatory roles of TFs diversified more rapidly between homoeologs than did the cis-regulatory elements of their target genes. Our approach underscores the utility of network analysis for detection of master regulators and provides fresh perspectives on fiber development and polyploid functional genomics, through the lens of co-expression and GRN dynamics.

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Science students embrace research opportunities through annual ASSURE program

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August 20, 2024 : By Ryan Klinker - Office of Communications & Public Engagement

Taking six weeks out of their summer break, students and faculty from Liberty University’s Department of Biology & Chemistry engaged in research as part of the department’s ASSURE program, an annual summer intensive that introduces many students to the practices and skills of research.

ASSURE stands for Acquiring Skills for Students Underrepresented in Research Experience and includes students from historically underrepresented demographic groups in the sciences (such as women, some ethnic groups, and first-generation college students). Groups of two to three undergraduate students are assigned to a professor for six weeks to conduct new or existing studies and receive valuable mentoring.

“The ASSURE program is intentionally designed to enrich our students’ education experience, and for many in the program, this is their first venture into research,” said Dr. Heidi DiFrancesca, dean of the School of Health Sciences . “Throughout this experience, students are reinforcing their understanding of the content they’ve been learning in the classroom while also developing an indispensable skill set — critical thinking, problem solving, collaboration, and communication — that will help them to be successful both during their time here at LU and in their chosen professions.”

This summer marked the fourth year of the program, consisting of 24 students (21 undergraduate and three graduate) with 10 faculty members. The groups conducted research across a wide variety of disciplines, including biology, ecology, organic chemistry, forensics, anatomy, and more.

Nathaniel Williams, a junior biomedical sciences student, worked under Professor of Chemistry Dr. Alan Fulp to explore the body’s endocannabinoid system, a cell-signaling system that regulates and balances many bodily functions. His group’s research focused on developing a molecular compound that can combat inhibitors in the system and reduce inflammation and pain.

“We wanted to see how far we could take things and how much we could help people by activating these receptors,” Williams said. “There are natural chemicals in the eyes that are constantly being broken down by inhibitors, so we wanted to see if we could stop the inhibitors and let the chemicals do what they need to do and activate the receptors.”

“I’d love to have published research before I go, and I love chemistry, and the ASSURE program allowed me to work toward that. I know the professors here very well, and they’re very friendly, and I wanted to take advantage of this unique opportunity that I otherwise wouldn’t have had. It was a great six weeks.”

Senior forensic science student Alyssa Spillar had spent part of the spring semester working under Director of Forensic Science Dr. J. Thomas McClintock and Instructor of Biology Kristin Mossé but said the summer research she did through ASSURE was a new, exciting experience. Spillar was able to continue with DNA research from the historical Hillsman House in Rice, Va., where McClintock and students have been studying blood samples since 2018 to corroborate that the building served as a Union field hospital during the last major Civil War battle fought in Virginia. A table once used in the house was recently acquired, presenting the group with more samples to study.

“The goal of the project was to generate DNA profiles from the presumably 160-year-old bloodstains on the table using typical DNA lab procedure,” Spillar said.

She said being involved in the project through the summer brought additional experiences she didn’t have in the spring.

“I applied to the ASSURE program because I love research and the more research experience I can get, the better. I really loved being in a lab or doing research for eight hours a day. It was such an immersive experience.”

ASSURE is funded by a grant from Liberty’s  Office of Sponsored Programs & Research and supported by the Office of the Provost.

“The Office of Sponsored Programs & Research is passionate about supporting student research at Liberty University,” grants administrator Emily Stevens said. “As a Christian university, we want to empower students to grow into credible investigators and experts in their fields by supporting the pursuit of knowledge.”

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Developmental Biology , 6th edition

Scott F Gilbert .

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Developmental biology is a great field for scientists who want to integrate different levels of biology. We can take a problem and study it on the molecular and chemical levels (e.g., How are globin genes transcribed, and how do the factors activating their transcription interact with one another on the DNA?), on the cellular and tissue levels (Which cells are able to make globin, and how does globin mRNA leave the nucleus?), on the organ and organ system levels (How do the capillaries form in each tissue, and how are they instructed to branch and connect?), and even at the ecological and evolutionary levels (How do differences in globin gene activation enable oxygen to flow from mother to fetus, and how do environmental factors trigger the differentiation of more red blood cells?).

Developmental biology is one of the fastest growing and most exciting fields in biology, creating a framework that integrates molecular biology, physiology, cell biology, anatomy, cancer research, neurobiology, immunology, ecology, and evolutionary biology. The study of development has become essential for understanding any other area of biology.

• Collapse All
• Acknowledgments
• The Questions of Developmental Biology
• Anatomical Approaches to Developmental Biology
• Epigenesis and preformation
• Naming the parts: The primary germ layers and early organs
• The four principles of Karl Ernst von Baer
• Fate mapping the embryo
• Cell migration
• Embryonic homologies
• Medical Embryology and Teratology
• The mathematics of organismal growth
• The mathematics of patterning
• Principles of Development: Developmental Anatomy
• The Circle of Life: The Stages of Animal Development
• The Frog Life Cycle
• Control of developmental morphogenesis: The role of the nucleus
• Unicellular protists and the origins of sexual reproduction
• The Volvocaceans
• Differentiation and Morphogenesis in Dictyostelium: Cell Adhesion
• Diploblasts
• Protostomes and deuterostomes
• Principles of Development: Life Cycles and Developmental Patterns
• Environmental sex determination
• Adaptation of embryos and larvae to their environments
• Autonomous Specification
• Conditional specification
• Syncytial specification
• Differential cell affinity
• The thermodynamic model of cell interactions
• Cadherins and cell adhesion
• Principles of Development: Experimental Embryology
• Nucleus or cytoplasm: Which controls heredity?
• The split between embryology and genetics
• Early attempts at developmental genetics
• Amphibian cloning: The restriction of nuclear potency
• Amphibian cloning: The pluripotency of somatic cells
• Cloning mammals
• Differential Gene Expression
• Northern blotting
• In situ hybridization
• The polymerase chain reaction
• Transgenic cells and organisms
• Determining the function of a message: Antisense RNA
• Identifying the Genes for Human Developmental Anomalies
• Principles of Development: Genes and Development
• Anatomy of the gene: Exons and introns
• Anatomy of the gene: Promoters and enhancers
• Transcription factors
• Locus control regions in globin genes
• DNA methylation and gene activity
• Possible mechanisms by which methylation represses gene transcription
• Transcriptional Regulation of an Entire Chromosome: Dosage Compensation
• Control of early development by nuclear RNA selection
• Creating families of proteins through differential nRNA splicing
• Differential mRNA longevity
• Selective inhibition of mRNA translation
• Control of RNA expression by cytoplasmic localization
• Epilogue: Posttranslational Gene Regulation
• Principles of Development: Developmental Genetics
• Cascades of induction: Reciprocal and sequential inductive events
• Instructive and permissive interactions
• Epithelial-mesenchymal interactions
• The fibroblast growth factors
• The Hedgehog family
• The Wnt family
• The TGF-β superfamily
• Other paracrine factors
• The RTK pathway
• The Smad pathway
• The JAK-STAT pathway
• The Wnt pathway
• The Hedgehog pathway
• The Cell Death Pathways
• The Notch pathway: Juxtaposed ligands and receptors
• The extracellular matrix as a source of critical developmental signals
• Direct transmission of signals through gap junctions
• Cross-Talk between Pathways
• Principles of Development:Cell-Cell Communication
• Sperm attraction: Action at a distance
• The acrosomal reaction in sea urchins
• Species-specific recognition in sea urchins
• Gamete binding and recognition in mammals
• Fusion of the egg and sperm plasma membranes
• The prevention of polyspermy
• Early responses
• Late responses
• Fusion of genetic material in sea urchins
• Fusion of genetic material in mammals
• Preparation for cleavage
• Snapshot Summary: Fertilization
• Gastrulation
• Axis Formation
• Cleavage in Sea Urchins
• Sea Urchin Gastrulation
• Cleavage in Snail Eggs
• Gastrulation in Snails
• Tunicate Cleavage
• Gastrulation in Tunicates
• Why C. elegans?
• Cleavage and Axis Formation in C. elegans
• Gastrulation in C. elegans
• Snapshot Summary: Early Invertebrate Development
• The Maternal Effect Genes
• The Segmentation Genes
• The Homeotic Selector Genes
• The Morphogenetic Agent for Dorsal-Ventral Polarity
• The Translocation of Dorsal Protein
• Axes and Organ Primordia: The Cartesian Coordinate Model
• Snapshot Summary: Drosophila Development and Axis Specification
• Cleavage in Amphibians
• Amphibian Gastrulation
• The Progressive Determination of the Amphibian Axes
• Hans Spemann and Hilde Mangold: Primary Embryonic Induction
• The Mechanisms of Axis Formation in Amphibians
• The Functions of the Organizer
• The Regional Specificity of Induction
• Snapshot Summary: Early Development and Axis Formation in Amphibians
• Cleavage in Fish Eggs
• Gastrulation in Fish Embryos
• Axis Formation in Fish Embryos
• Cleavage in Bird Eggs
• Gastrulation of the Avian Embryo
• Axis Formation in the Chick Embryo
• Cleavage in Mammals
• Escape from the Zona Pellucida
• Gastrulation in Mammals
• Mammalian Anterior-Posterior Axis Formation
• The Dorsal-Ventral and Left-Right Axes in Mammals
• Snapshot Summary: The Early Development of Vertebrates
• Primary neurulation
• Secondary neurulation
• The anterior-posterior axis
• The dorsal-ventral axis
• Spinal chord and medulla organization
• Cerebellar organization
• Cerebral organization
• Adult neural stem cells
• Neuronal Types
• The dynamics of optic development
• Neural retina differentiation
• Lens and cornea differentiation
• The origin of epidermal cells
• Cutaneous appendages
• Patterning of cutaneous appendages
• Snapshot Summary: Central Nervous System and Epidermis
• The Trunk Neural Crest
• The Cranial Neural Crest
• The Cardiac Neural Crest
• The Generation of Neuronal Diversity
• Pattern Generation in the Nervous System
• The Development of Behaviors: Constancy and Plasticity
• Snapshot Summary: Neural Crest Cells and Axonal Specificity
• The initiation of somite formation
• Specification and commitment of somitic cell types
• Determining somitic cell fates
• Specification and differentiation by the myogenic bHLH proteins
• Muscle cell fusion
• Intramembranous ossification
• Endochondral ossification
• Osteoclasts
• Progression of kidney types
• Reciprocal interaction of kidney tissues
• The mechanisms of reciprocal induction
• Snapshot Summary: Paraxial and Intermediate Mesoderm
• Formation of Blood Vessels
• The Development of Blood Cells
• The Pharynx
• The Digestive Tube and Its Derivatives
• The Respiratory Tube
• The Extraembryonic Membranes
• Snapshot Summary: Lateral Mesoderm and Endoderm
• Specification of the limb fields: Hox genes and retinoic acid
• Induction of the early limb bud: Fibroblast growth factors
• Specification of forelimb or hindlimb: Tbx4 and Tbx5
• Induction of the apical ectodermal ridge
• The apical ectodermal ridge: The ectodermal component
• The progress zone: The mesodermal component
• Hox genes and the specification of the proximal-distal axis
• The zone of polarizing activity
• Sonic hedgehog defines the ZPA
• The Generation of the Dorsal-Ventral Axis
• Coordination among the Three Axes
• Sculpting the autopod
• Forming the joints
• Snapshot Summary: The Tetrapod Limb
• Primary and secondary sex determination
• The developing gonads
• The mechanisms of mammalian primary sex determination
• Secondary sex determination: Hormonal regulation of the sexual phenotype
• The sexual development pathway
• The sex-lethal gene as the pivot for sex determination
• The transformer genes
• Doublesex: The switch gene of sex determination
• Temperature-dependent sex determination in reptiles
• Location-dependent sex determination in Bonellia and Crepidula
• Snapshot Summary: Sex Determination
• Amphibian Metamorphosis
• Metamorphosis in Insects
• Epimorphic Regeneration of Salamander Limbs
• Compensatory Regeneration in the Mammalian Liver
• Morphallactic Regeneration in Hydras
• Maximum Life Span and Life Expectancy
• Causes of Aging
• Snapshot Summary: Metamorphosis, Regeneration, and Aging
• Germ cell determination in nematodes
• Germ cell determination in insects
• Germ cell determination in amphibians
• Germ cell migration in amphibians
• Germ cell migration in mammals
• Germ cell migration in birds and reptiles
• Germ cell migration in Drosophila
• Spermiogenesis
• Oogenic meiosis
• Maturation of the oocyte in amphibians
• Completion of amphibian meiosis: Progesterone and fertilization
• Gene transcription in oocytes
• Meroistic oogenesis in insects
• Oogenesis in mammals
• Snapshot Summary: The Germ Line
• Plant Life Cycles
• Pollination
• Fertilization
• Experimental studies
• Embryogenesis
• Germination
• Root development
• Shoot development
• Leaf development
• The Vegetative-to-Reproductive Transition
• Snapshot Summary: Plant Development
• Environmental Cues and Normal Development
• Predictable Environmental Differences as Cues for Development
• Phenotypic Plasticity: Polyphenism and Reaction Norms
• Predator-Induced Defenses
• Mammalian Immunity as a Predator-Induced Response
• Learning: An Environmentally Adaptive Nervous System
• Teratogenic Agents
• Genetic-Environmental Interactions
• Snapshot Summary: The Environmental Regulation of Development
• Charles Darwin's synthesis
• E. B. Wilson and F. R. Lillie
• “Life's splendid drama”
• The search for the Urbilaterian ancestor
• Changes in Hox-responsive elements of downstream genes
• Changes in Hox gene transcription patterns within a body portion
• Changes in Hox gene expression between body segments
• Changes in Hox gene number
• Instructions for forming the central nervous system
• Limb formation
• Dissociation: Heterochrony and allometry
• Duplication and divergence
• Correlated progression
• Coevolution of ligand and receptor
• Physical constraints
• Morphogenetic constraints
• Phyletic constraints
• A New Evolutionary Synthesis
• Snapshot Summary: Evolutionary Developmental Biology

With a chapter on Plant Development by Susan R Singer, Carleton College

• Cite this Page Gilbert SF. Developmental Biology. 6th edition. Sunderland (MA): Sinauer Associates; 2000.

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Embracing Gen AI at Work

• H. James Wilson
• Paul R. Daugherty

The skills you need to succeed in the era of large language models

Today artificial intelligence can be harnessed by nearly anyone, using commands in everyday language instead of code. Soon it will transform more than 40% of all work activity, according to the authors’ research. In this new era of collaboration between humans and machines, the ability to leverage AI effectively will be critical to your professional success.

This article describes the three kinds of “fusion skills” you need to get the best results from gen AI. Intelligent interrogation involves instructing large language models to perform in ways that generate better outcomes—by, say, breaking processes down into steps or visualizing multiple potential paths to a solution. Judgment integration is about incorporating expert and ethical human discernment to make AI’s output more trustworthy, reliable, and accurate. It entails augmenting a model’s training sources with authoritative knowledge bases when necessary, keeping biases out of prompts, ensuring the privacy of any data used by the models, and scrutinizing suspect output. With reciprocal apprenticing, you tailor gen AI to your company’s specific business context by including rich organizational data and know-how into the commands you give it. As you become better at doing that, you yourself learn how to train the AI to tackle more-sophisticated challenges.

The AI revolution is already here. Learning these three skills will prepare you to thrive in it.

Generative artificial intelligence is expected to radically transform all kinds of jobs over the next few years. No longer the exclusive purview of technologists, AI can now be put to work by nearly anyone, using commands in everyday language instead of code. According to our research, most business functions and more than 40% of all U.S. work activity can be augmented, automated, or reinvented with gen AI. The changes are expected to have the largest impact on the legal, banking, insurance, and capital-market sectors—followed by retail, travel, health, and energy.

• H. James Wilson is the global managing director of technology research and thought leadership at Accenture Research. He is the coauthor, with Paul R. Daugherty, of Human + Machine: Reimagining Work in the Age of AI, New and Expanded Edition (HBR Press, 2024). hjameswilson
• Paul R. Daugherty is Accenture’s chief technology and innovation officer. He is the coauthor, with H. James Wilson, of Human + Machine: Reimagining Work in the Age of AI, New and Expanded Edition (HBR Press, 2024). pauldaugh

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Lincoln Laboratory and National Strategic Research Institute launch student research program to tackle biothreats to national security

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The following announcement was released jointly by MIT Lincoln Laboratory and the National Strategic Research Institute.

MIT Lincoln Laboratory and the National Strategic Research Institute (NSRI) at the University of Nebraska (NU), a university-affiliated research center designated by the U.S. Department of Defense (DoD), have established a joint student research program.

The goal is to bring together the scientific expertise, cutting-edge capabilities, and student capacity of NU and MIT for critical issues within global health and agricultural security, aiming to foster solutions to detect and neutralize emerging biological threats.

"We are excited to combine forces with NSRI to develop critical biotechnologies that will enhance national security," says Catherine Cabrera, who leads Lincoln Laboratory's Biological and Chemical Technologies Group. "This partnership underscores our shared commitment to safeguarding America through scientific leadership."

"In an era of rapidly evolving dangers, we must stay ahead of the curve through continuous innovation," says  David Roberts , the NSRI research director for special programs. "This partnership harnesses a unique combination of strengths from two leading academic institutions and two research institutes to create new paradigms in biological defense."

With funding from a DoD agency, the collaborators conducted a pilot of the program embedded within the MIT Engineering Systems Design and Development II course . The students’ challenge was to develop methods to rapidly screen for novel biosynthetic capabilities. Currently, such methods are limited by the lack of standardized, high-throughput devices that can support the culture of traditionally “uncultivable” microorganisms, which severely limits the cell diversity that could be probed for bioprospecting or biomanufacturing applications.

Led by  Todd Thorsen , a technical staff member in the  Biological and Chemical Technologies Group at Lincoln Laboratory, MIT students created the project, "Bioprospecting Experimentation Apparatus with Variable Environmental Regulation," which focused on developing simple high-throughput tools with integrated environmental control systems to expand the environmental testing envelope.

"This program, which emphasizes both engineering design and prototyping, challenges students to take what they learned in the classroom in their past undergraduate and graduate studies, and apply it to a real-world problem," Thorsen says. "For many students, the hands-on nature of this course is an exciting opportunity to test their abilities to prioritize what is important in developing products that are both functional and easy to use. What I found most impressive was the students’ ability to apply their collective knowledge to the design and prototyping of the biomedical devices, emphasizing their diverse backgrounds in areas like fluid mechanicals, controls, and solid mechanics."

In total, 12 mechanical engineering students contributed to the program, producing and validating a gas gradient manifold prototype and a droplet-dispensing manifold that has the potential to generate arbitrary pH gradients in industry-standard 96-well plates used for biomedical research. These devices will greatly simplify and accelerate the microculture of complex mixtures of organisms, like bacteria populations, where the growth conditions are unknown, allowing the end user to use the manifolds to dial in the optimal environmental parameters without the need for expensive, bulky hardware like the anaerobic chambers typically used for microbiology research.

"This class was my first experience with microfluidics and biotech, and thanks to our sponsors, I gained the confidence to pursue a career path in biotech," says Rachael Rosco, an MIT mechanical engineering graduate student. "The project itself was meaningful, and I know that our work will hopefully one day make an impact. Who knows, maybe one day it will lead to cultivating extremophile bacteria on a foreign planet!"

The collaboration will continue to seek DoD research funding to create workforce development opportunities for top scientific talent and introduce students to long-standing DoD challenges. Projects will take place nationwide at several NSRI, NU, Lincoln Laboratory, and MIT facilities.

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• Mechanical engineering
• Bioengineering and biotechnology
• Security studies and military
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• Synthetic biology
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