Publications by authors named "Scott F Gilbert"

61 Publications

Systemic racism, systemic sexism, and the embryological enterprise.

Authors:
Scott F Gilbert

Dev Biol 2021 May 17;473:97-104. Epub 2021 Feb 17.

Department of Biology, Swarthmore College, Swarthmore, PA 19081, USA; Institute of Biotechnology, University of Helsinki, Helsinki, Finland. Electronic address:

The core of systemic racism and sexism is not merely an emphasis about human differences and thinking that another group of people is inferior to one's own. Rather, the institutional nature of racism or sexism establishes a permanent group hierarchy that is believed to reflect the laws of nature or the decrees of God. It thus becomes the norm of a culture to think and behave according to these rules. Notions of hierarchy became solidified into the Great Chain of Being during the Middle Ages, as did views concerning hereditary racial and gender superiority. During the Enlightenment, such classifications became established by philosophy and science. Starting in the 1800s, embryology and anthropology were used to provide evidence for the unilinear progression of species and races. The first evolutionary schemes were not "branching trees." In these schemes, women and non-white races were seen as embryonic or juvenile forms of the adult white male, and they were often depicted as intermediaries between the fully human and the animals. Such linear schemes of evolution remain part of popular culture and even some science, promoting the racism and sexism associated with them.
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http://dx.doi.org/10.1016/j.ydbio.2021.02.001DOI Listing
May 2021

Preface.

Authors:
Scott F Gilbert

Curr Top Dev Biol 2021 ;141:xiii-xxiii

Department of Biology, Swarthmore College, Swarthmore, PA, United States; Institute of Biotechnology, University of Helsinki, Helsinki, Finland. Electronic address:

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http://dx.doi.org/10.1016/S0070-2153(21)00011-9DOI Listing
January 2021

Evolutionary developmental biology and sustainability: A biology of resilience.

Authors:
Scott F Gilbert

Evol Dev 2021 Jan 5:e12366. Epub 2021 Jan 5.

Department of Biology, Swarthmore College, Swarthmore, Pennsylvania, USA.

Evolutionary developmental biology, and especially ecological developmental biology, is essential for discussions of sustainability and the responses to global climate change. First, this paper explores examples of animals that have successfully altered their development to accommodate human-made changes to their environments. We next document the ability of global warming to disrupt the development of those organisms with temperature-dependent sex-determination or with phenologies coordinating that organism's development with those of other species. The thermotolerance of Homo sapiens is also related to key developmental factors concerning brain development and maintenance, and the development of corals, the keystone organisms of tropical reefs, is discussed in relation to global warming as well as to other anthropogenic changes. While teratogenic and endocrine-disrupting compounds are not discussed in this essay, the ability of glyphosate herbicides to block insect development is highlighted. Last, the paper discusses the need to creatively integrate developmental biology with ecological, political, religious, and economic perspectives, as the flourishing of contemporary species may require altering the ways that Western science has considered the categories of nature, culture, and self.
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http://dx.doi.org/10.1111/ede.12366DOI Listing
January 2021

Toward a Symbiotic Perspective on Public Health: Recognizing the Ambivalence of Microbes in the Anthropocene.

Microorganisms 2020 May 16;8(5). Epub 2020 May 16.

Department of Biology, Swarthmore College, Swarthmore, PA 19081, USA.

Microbes evolve in complex environments that are often fashioned, in part, by human desires. In a global perspective, public health has played major roles in structuring how microbes are perceived, cultivated, and destroyed. The germ theory of disease cast microbes as enemies of the body and the body politic. Antibiotics have altered microbial development by providing stringent natural selection on bacterial species, and this has led to the formation of antibiotic-resistant bacterial strains. Public health perspectives such as "Precision Public Health" and "One Health" have recently been proposed to further manage microbial populations. However, neither of these take into account the symbiotic relationships that exist between bacterial species and between bacteria, viruses, and their eukaryotic hosts. We propose a perspective on public health that recognizes microbial evolution through symbiotic associations (the hologenome theory) and through lateral gene transfer. This perspective has the advantage of including both the pathogenic and beneficial interactions of humans with bacteria, as well as combining the outlook of the "One Health" model with the genomic methodologies utilized in the "Precision Public Health" model. In the Anthropocene, the conditions for microbial evolution have been altered by human interventions, and public health initiatives must recognize both the beneficial (indeed, necessary) interactions of microbes with their hosts as well as their pathogenic interactions.
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http://dx.doi.org/10.3390/microorganisms8050746DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7285259PMC
May 2020

John Tyler Bonner: Remembering a scientific pioneer.

J Exp Zool B Mol Dev Evol 2019 12 19;332(8):365-370. Epub 2019 Nov 19.

Smithsonian Tropical Research Institute at the Escuela de Biologia, Universidad de Costa Rica, San Pedro, Costa Rica.

Throughout his life, John Tyler Bonner contributed to major transformations in the fields of developmental and evolutionary biology. He pondered the evolution of complexity and the significance of randomness in evolution, and was instrumental in the formation of evolutionary developmental biology. His contributions were vast, ranging from highly technical scientific articles to numerous books written for a broad audience. This historical vignette gathers reflections by several prominent researchers on the greatness of John Bonner and the implications of his work.
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http://dx.doi.org/10.1002/jez.b.22920DOI Listing
December 2019

Evolutionary transitions revisited: Holobiont evo-devo.

Authors:
Scott F Gilbert

J Exp Zool B Mol Dev Evol 2019 12 29;332(8):307-314. Epub 2019 Sep 29.

Department of Biology, Swarthmore College, Swarthmore, Pennsylvania.

John T. Bonner lists four essential transformations in the evolution of life: the emergence of the eukaryotic cell, meiosis, multicellularity, and the nervous system. This paper analyses the mechanisms for those transitions in light of three of Dr. Bonner's earlier hypotheses: (a) that the organism is its life cycle, (b) that evolution consists of alterations of the life cycle, and (c) that development extends beyond the body and into interactions with other organisms. Using the notion of the holobiont life cycle, this paper attempts to show that these evolutionary transitions can be accomplished through various means of symbiosis. Perceiving the organism both as an interspecies consortium and as a life cycle supports a twofold redefinition of the organism as a holobiont constructed by integrating together the life cycles of several species. These findings highlight the importance of symbiosis and the holobiont development in analyses of evolution.
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http://dx.doi.org/10.1002/jez.b.22903DOI Listing
December 2019

Developmental symbiosis facilitates the multiple origins of herbivory.

Authors:
Scott F Gilbert

Evol Dev 2020 01 22;22(1-2):154-164. Epub 2019 Jul 22.

Department of Biology, Swarthmore College, Swarthmore, Pennsylvania.

Developmental bias toward particular evolutionary trajectories can be facilitated through symbiosis. Organisms are holobionts, consisting of zygote-derived cells and a consortia of microbes, and the development, physiology, and immunity of animals are properties of complex interactions between the zygote-derived cells and microbial symbionts. Such symbionts can be agents of developmental plasticity, allowing an organism to develop in particular directions. This plasticity can lead to genetic assimilation either through the incorporation of microbial genes into host genomes or through the direct maternal transmission of the microbes. Such plasticity can lead to niche construction, enabling the microbes to remodel host anatomy and/or physiology. In this article, I will focus on the ability of symbionts to bias development toward the evolution of herbivory. I will posit that the behavioral and morphological manifestations of herbivorous phenotypes must be preceded by the successful establishment of a community of symbiotic microbes that can digest cell walls and detoxify plant poisons. The ability of holobionts to digest plant materials can range from being a plastic trait, dependent on the transient incorporation of environmental microbes, to becoming a heritable trait of the holobiont organism, transmitted through the maternal propagation of symbionts or their genes.
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http://dx.doi.org/10.1111/ede.12291DOI Listing
January 2020

The combined impact of IgLON family proteins Lsamp and Neurotrimin on developing neurons and behavioral profiles in mouse.

Brain Res Bull 2018 06 29;140:5-18. Epub 2018 Mar 29.

Department of Physiology, Institute of Biomedicine and Translational Medicine, University of Tartu, 19 Ravila Street, 50411, Tartu, Estonia; Centre of Excellence in Genomics and Translational Medicine, University of Tartu, 19 Ravila Street, 50411, Tartu, Estonia. Electronic address:

Cell surface neural adhesion proteins are critical components in the complex orchestration of cell proliferation, apoptosis, and neuritogenesis essential for proper brain construction and behavior. We focused on the impact of two plasticity-associated IgLON family neural adhesion molecules, Neurotrimin (Ntm) and Limbic system associated membrane protein (Lsamp), on mouse behavior and its underlying neural development. Phenotyping neurons derived from the hippocampi of Lsamp, Ntm and LsampNtm mice was performed in parallel with behavioral testing. While the anatomy of mutant brains revealed no gross changes, the Ntm hippocampal neurons exhibited premature sprouting of neurites and manifested accelerated neurite elongation and branching. We propose that Ntm exerts an inhibitory impact on neurite outgrowth, whereas Lsamp appears to be an enhancer of the said process as premature neuritogenesis in Ntm neurons is apparent only in the presence of Lsamp. We also show interplay between Lsamp and Ntm in regulating tissue homeostasis: the impact of Ntm on cellular proliferation was dependent on Lsamp, and Lsamp appeared to be a positive regulator of apoptosis in the presence of Ntm. Behavioral phenotyping indicated test-specific interactions between Lsamp and Ntm. The phenotypes of single mutant lines, such as reduced swimming speed in Morris water maze and increased activity in the elevated plus maze, were magnified in LsampNtm mice. Altogether, evidence both from behavioral experiments and cultured hippocampal cells show combined and differential interactions between Ntm and Lsamp in the formation of hippocampal circuits and behavioral profiles. We demonstrate that mutual interactions between IgLON molecules regulate the initiation of neurite sprouting at very early ages, and even cell-autonomously, independent of their regulation of cell-cell adhesion.
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http://dx.doi.org/10.1016/j.brainresbull.2018.03.013DOI Listing
June 2018

Achilles and the tortoise: Some caveats to mathematical modeling in biology.

Authors:
Scott F Gilbert

Prog Biophys Mol Biol 2018 09 31;137:37-45. Epub 2018 Jan 31.

Department of Biology, Swarthmore College, Swarthmore, PA, 19081, USA. Electronic address:

Mathematical modeling has recently become a much-lauded enterprise, and many funding agencies seek to prioritize this endeavor. However, there are certain dangers associated with mathematical modeling, and knowledge of these pitfalls should also be part of a biologist's training in this set of techniques. (1) Mathematical models are limited by known science; (2) Mathematical models can tell what can happen, but not what did happen; (3) A model does not have to conform to reality, even if it is logically consistent; (4) Models abstract from reality, and sometimes what they eliminate is critically important; (5) Mathematics can present a Platonic ideal to which biologically organized matter strives, rather than a trial-and-error bumbling through evolutionary processes. This "Unity of Science" approach, which sees biology as the lowest physical science and mathematics as the highest science, is part of a Western belief system, often called the Great Chain of Being (or Scala Natura), that sees knowledge emerge as one passes from biology to chemistry to physics to mathematics, in an ascending progression of reason being purification from matter. This is also an informal model for the emergence of new life. There are now other informal models for integrating development and evolution, but each has its limitations.
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http://dx.doi.org/10.1016/j.pbiomolbio.2018.01.005DOI Listing
September 2018

Developmental biology, the stem cell of biological disciplines.

Authors:
Scott F Gilbert

PLoS Biol 2017 12 28;15(12):e2003691. Epub 2017 Dec 28.

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

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.
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http://dx.doi.org/10.1371/journal.pbio.2003691DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5761959PMC
December 2017

Melanoblast development coincides with the late emerging cells from the dorsal neural tube in turtle Trachemys scripta.

Sci Rep 2017 09 21;7(1):12063. Epub 2017 Sep 21.

Developmental Biology, Institute of Biotechnology, University of Helsinki, Helsinki, Finland.

Ectothermal reptiles have internal pigmentation, which is not seen in endothermal birds and mammals. Here we show that the development of the dorsal neural tube-derived melanoblasts in turtle Trachemys scripta is regulated by similar mechanisms as in other amniotes, but significantly later in development, during the second phase of turtle trunk neural crest emigration. The development of melanoblasts coincided with a morphological change in the dorsal neural tube between stages mature G15 and G16. The melanoblasts delaminated and gathered in the carapacial staging area above the neural tube at G16, and differentiated into pigment-forming melanocytes during in vitro culture. The Mitf-positive melanoblasts were not restricted to the dorsolateral pathway as in birds and mammals but were also present medially through the somites similarly to ectothermal anamniotes. This matched a lack of environmental barrier dorsal and lateral to neural tube and the somites that is normally formed by PNA-binding proteins that block entry to medial pathways. PNA-binding proteins may also participate in the patterning of the carapacial pigmentation as both the migratory neural crest cells and pigment localized only to PNA-free areas.
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http://dx.doi.org/10.1038/s41598-017-12352-0DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5608706PMC
September 2017

Patterning of the turtle shell.

Curr Opin Genet Dev 2017 Aug 29;45:124-131. Epub 2017 May 29.

Biology Department, Swarthmore College, USA.

Interest in the origin and evolution of the turtle shell has resulted in a most unlikely clade becoming an important research group for investigating morphological diversity in developmental biology. Many turtles generate a two-component shell that nearly surrounds the body in a bony exoskeleton. The ectoderm covering the shell produces epidermal scutes that form a phylogenetically stable pattern. In some lineages, the bones of the shell and their ectodermal covering become reduced or lost, and this is generally associated with different ecological habits. The similarity and diversity of turtles allows research into how changes in development create evolutionary novelty, interacting modules, and adaptive physiology and anatomy.
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http://dx.doi.org/10.1016/j.gde.2017.03.016DOI Listing
August 2017

Wfs1 is expressed in dopaminoceptive regions of the amniote brain and modulates levels of D1-like receptors.

PLoS One 2017 7;12(3):e0172825. Epub 2017 Mar 7.

Department of Physiology, Institute of Biomedicine and Translational Medicine, University of Tartu, Tartu, Estonia.

During amniote evolution, the construction of the forebrain has diverged across different lineages, and accompanying the structural changes, functional diversification of the homologous brain regions has occurred. This can be assessed by studying the expression patterns of marker genes that are relevant in particular functional circuits. In all vertebrates, the dopaminergic system is responsible for the behavioral responses to environmental stimuli. Here we show that the brain regions that receive dopaminergic input through dopamine receptor D1 are relatively conserved, but with some important variations between three evolutionarily distant vertebrate lines-house mouse (Mus musculus), domestic chick (Gallus gallus domesticus) / common quail (Coturnix coturnix) and red-eared slider turtle (Trachemys scripta). Moreover, we find that in almost all instances, those brain regions expressing D1-like dopamine receptor genes also express Wfs1. Wfs1 has been studied primarily in the pancreas, where it regulates the endoplasmic reticulum (ER) stress response, cellular Ca2+ homeostasis, and insulin production and secretion. Using radioligand binding assays in wild type and Wfs1-/- mouse brains, we show that the number of binding sites of D1-like dopamine receptors is increased in the hippocampus of the mutant mice. We propose that the functional link between Wfs1 and D1-like dopamine receptors is evolutionarily conserved and plays an important role in adjusting behavioral reactions to environmental stimuli.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0172825PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5436468PMC
September 2017

Neuroembryology.

Wiley Interdiscip Rev Dev Biol 2017 01 1;6(1). Epub 2016 Dec 1.

Swarthmore College, Swarthmore, PA, USA.

How is it that some cells become neurons? And how is it that neurons become organized in the spinal cord and brain to allow us to walk and talk, to see, recall events in our lives, feel pain, keep our balance, and think? The cells that are specified to form the brain and spinal cord are originally located on the outside surface of the embryo. They loop inward to form the neural tube in a process called neurulation. Structures that are nearby send signals to the posterior neural tube to form and pattern the spinal cord so that the dorsal side receives sensory input and the ventral side sends motor signals from neurons to muscles. In the brain, stem cells near the center of the neural tube migrate out to form a mantel zone, and a set of dividing cells from the mantle zone migrate further to produce a second set of neurons at the outer surface of the brain. These neurons will form the cerebral cortex, which contains six discrete layers. Each layer has different connections and different functions. WIREs Dev Biol 2017, 6:e215. doi: 10.1002/wdev.215 For further resources related to this article, please visit the WIREs website.
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http://dx.doi.org/10.1002/wdev.215DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5193482PMC
January 2017

Getting the Hologenome Concept Right: an Eco-Evolutionary Framework for Hosts and Their Microbiomes.

mSystems 2016 Mar-Apr;1(2). Epub 2016 Mar 29.

Departments of Biological Sciences and Pathology, Microbiology and Immunology, Vanderbilt University, Nashville, Tennessee, USA.

Given the complexity of host-microbiota symbioses, scientists and philosophers are asking questions at new biological levels of hierarchical organization-what is a holobiont and hologenome? When should this vocabulary be applied? Are these concepts a null hypothesis for host-microbe systems or limited to a certain spectrum of symbiotic interactions such as host-microbial coevolution? Critical discourse is necessary in this nascent area, but productive discourse requires that skeptics and proponents use the same lexicon. For instance, critiquing the hologenome concept is not synonymous with critiquing coevolution, and arguing that an entity is not a primary unit of selection dismisses the fact that the hologenome concept has always embraced multilevel selection. Holobionts and hologenomes are incontrovertible, multipartite entities that result from ecological, evolutionary, and genetic processes at various levels. They are not restricted to one special process but constitute a wider vocabulary and framework for host biology in light of the microbiome.
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http://dx.doi.org/10.1128/mSystems.00028-16DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5069740PMC
March 2016

Development of the turtle plastron, the order-defining skeletal structure.

Proc Natl Acad Sci U S A 2016 May 25;113(19):5317-22. Epub 2016 Apr 25.

Developmental Biology, Institute of Biotechnology, University of Helsinki, Helsinki 00014, Finland; Department of Biology, Swarthmore College, Swarthmore, PA 19081;

The dorsal and ventral aspects of the turtle shell, the carapace and the plastron, are developmentally different entities. The carapace contains axial endochondral skeletal elements and exoskeletal dermal bones. The exoskeletal plastron is found in all extant and extinct species of crown turtles found to date and is synaptomorphic of the order Testudines. However, paleontological reconstructed transition forms lack a fully developed carapace and show a progression of bony elements ancestral to the plastron. To understand the evolutionary development of the plastron, it is essential to know how it has formed. Here we studied the molecular development and patterning of plastron bones in a cryptodire turtle Trachemys scripta We show that plastron development begins at developmental stage 15 when osteochondrogenic mesenchyme forms condensates for each plastron bone at the lateral edges of the ventral mesenchyme. These condensations commit to an osteogenic identity and suppress chondrogenesis. Their development overlaps with that of sternal cartilage development in chicks and mice. Thus, we suggest that in turtles, the sternal morphogenesis is prevented in the ventral mesenchyme by the concomitant induction of osteogenesis and the suppression of chondrogenesis. The osteogenic subroutines later direct the growth and patterning of plastron bones in an autonomous manner. The initiation of plastron bone development coincides with that of carapacial ridge formation, suggesting that the development of dorsal and ventral shells are coordinated from the start and that adopting an osteogenesis-inducing and chondrogenesis-suppressing cell fate in the ventral mesenchyme has permitted turtles to develop their order-specific ventral morphology.
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http://dx.doi.org/10.1073/pnas.1600958113DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4868452PMC
May 2016

Developmental Plasticity and Developmental Symbiosis: The Return of Eco-Devo.

Authors:
Scott F Gilbert

Curr Top Dev Biol 2016 1;116:415-33. Epub 2016 Feb 1.

Swarthmore College, Swarthmore, Pennsylvania, USA. Electronic address:

Ecological developmental biology is the study of the interactions between developing organisms and their environments. Organisms have evolved to use the environment as a source of important cues that can alter the trajectory of their development. First, developmental plasticity enables the genome to generate a repertoire of possible phenotypes, and environmental cues are often used to select the phenotype that appears most adaptive at that time. This facilitates evolutionary strategies such as phenotypic accommodation, genetic assimilation, and niche construction. Second, developmental symbiosis, wherein the developing animal utilizes cues from other organisms for normal cell differentiation and morphogenesis, has been found to be ubiquitous. The coevolution of symbiotic microbes and animal cells has often led to the dependency of an animal's development on particular microbial signals, making these cues essential and expected components of normal development.
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http://dx.doi.org/10.1016/bs.ctdb.2015.12.006DOI Listing
December 2016

Eco-Evo-Devo: developmental symbiosis and developmental plasticity as evolutionary agents.

Nat Rev Genet 2015 Oct 15;16(10):611-22. Epub 2015 Sep 15.

Department of Biology, Indiana University, Bloomington, Indiana 47405, USA.

The integration of research from developmental biology and ecology into evolutionary theory has given rise to a relatively new field, ecological evolutionary developmental biology (Eco-Evo-Devo). This field integrates and organizes concepts such as developmental symbiosis, developmental plasticity, genetic accommodation, extragenic inheritance and niche construction. This Review highlights the roles that developmental symbiosis and developmental plasticity have in evolution. Developmental symbiosis can generate particular organs, can produce selectable genetic variation for the entire animal, can provide mechanisms for reproductive isolation, and may have facilitated evolutionary transitions. Developmental plasticity is crucial for generating novel phenotypes, facilitating evolutionary transitions and altered ecosystem dynamics, and promoting adaptive variation through genetic accommodation and niche construction. In emphasizing such non-genomic mechanisms of selectable and heritable variation, Eco-Evo-Devo presents a new layer of evolutionary synthesis.
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http://dx.doi.org/10.1038/nrg3982DOI Listing
October 2015

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

Evol Dev 2015 May-Jun;17(3):198-219

Department of Organismic and Evolutionary Biology, Department of Molecular and Cellular Biology, Harvard University, 16 Divinity Avenue, BioLabs 4103, Cambridge, MA, 02138, USA.

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.
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http://dx.doi.org/10.1111/ede.12125DOI Listing
August 2015

Emerging from the rib: resolving the turtle controversies.

J Exp Zool B Mol Dev Evol 2015 May 11;324(3):208-20. Epub 2015 Feb 11.

Institute of Biotechnology, University of Helsinki, Helsinki, Finland.

Two of the major controversies in the present study of turtle shell development involve the mechanism by which the carapacial ridge initiates shell formation and the mechanism by which each rib forms the costal bones adjacent to it. This paper claims that both sides of each debate might be correct-but within the species examined. Mechanism is more properly "mechanisms," and there is more than one single way to initiate carapace formation and to form the costal bones. In the initiation of the shell, the rib precursors may be kept dorsal by either "axial displacement" (in the hard-shell turtles) or "axial arrest" (in the soft-shell turtle Pelodiscus), or by a combination of these. The former process would deflect the rib into the dorsal dermis and allow it to continue its growth there, while the latter process would truncate rib growth. In both instances, though, the result is to keep the ribs from extending into the ventral body wall. Our recent work has shown that the properties of the carapacial ridge, a key evolutionary innovation of turtles, differ greatly between these two groups. Similarly, the mechanism of costal bone formation may differ between soft-shell and hard-shell turtles, in that the hard-shell species may have both periosteal flattening as well as dermal bone induction, while the soft-shelled turtles may have only the first of these processes.
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http://dx.doi.org/10.1002/jez.b.22600DOI Listing
May 2015

A holobiont birth narrative: the epigenetic transmission of the human microbiome.

Authors:
Scott F Gilbert

Front Genet 2014 19;5:282. Epub 2014 Aug 19.

Department of Biology, Swarthmore College Swarthmore, PA, USA ; Biotechnology Institute, University of Helsinki Helsinki, Finland.

This essay plans to explore, expand, and re-tell the human birth narrative. Usually, human birth narratives focus on the origins of a new individual, focusing on the mother and fetus. This essay discusses birth as the origin of a new community. For not only is the eukaryotic body being reproduced, but so also are the bodies of its symbiotic microbes and so is the set of relationships between these organic components. Several parts of the new narrative are surprising: (1) bacterial symbionts might cause some of the characteristics of pregnancy and prepare a symbiotic community for transfer; (2) the first bacterial colonizers of the mammalian organism my enter the fetus prior to the lysing of the amniotic membrane and birth; (3) the same signals that often cause immunological attack against a microbe may serve under these conditions to signal homeostatic stability between symbiont and host; and (4) the mother may actively provide substances that promote the growth and settlement of helpful bacteria. The birth of the holobiont exemplifies principles of co-evolution, co-development, niche construction, and scaffolding. Birth is nothing less than the passage from one set of symbiotic relationships to another.
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http://dx.doi.org/10.3389/fgene.2014.00282DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4137224PMC
September 2014

The origin and loss of periodic patterning in the turtle shell.

Development 2014 Aug;141(15):3033-9

Developmental Biology Program, Institute of Biotechnology, University of Helsinki, P.O. Box 56, Helsinki FIN-00014, Finland Biology Department, Swarthmore College, 500 College Avenue, Swarthmore, PA 19081, USA

The origin of the turtle shell over 200 million years ago greatly modified the amniote body plan, and the morphological plasticity of the shell has promoted the adaptive radiation of turtles. The shell, comprising a dorsal carapace and a ventral plastron, is a layered structure formed by basal endochondral axial skeletal elements (ribs, vertebrae) and plates of bone, which are overlain by keratinous ectodermal scutes. Studies of turtle development have mostly focused on the bones of the shell; however, the genetic regulation of the epidermal scutes has not been investigated. Here, we show that scutes develop from an array of patterned placodes and that these placodes are absent from a soft-shelled turtle in which scutes were lost secondarily. Experimentally inhibiting Shh, Bmp or Fgf signaling results in the disruption of the placodal pattern. Finally, a computational model is used to show how two coupled reaction-diffusion systems reproduce both natural and abnormal variation in turtle scutes. Taken together, these placodal signaling centers are likely to represent developmental modules that are responsible for the evolution of scutes in turtles, and the regulation of these centers has allowed for the diversification of the turtle shell.
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http://dx.doi.org/10.1242/dev.109041DOI Listing
August 2014

Symbiosis as the way of eukaryotic life: the dependent co-origination of the body.

Authors:
Scott F Gilbert

J Biosci 2014 Apr;39(2):201-9

Department of Biology, Swarthmore College, Swarthmore, Pennsylvania 19081, USA and Biotechnology Institute, University of Helsinki, 00014 Helsinki, Finland,

Molecular analyses of symbiotic relationships are challenging our biological definitions of individuality and supplanting them with a new notion of normal part-whole relationships. This new notion is that of a 'holobiont', a consortium of organisms that becomes a functionally integrated 'whole'. This holobiont includes the zoological organism (the 'animal') as well as its persistent microbial symbionts. This new individuality is seen on anatomical and physiological levels, where a diversity of symbionts form a new 'organ system' within the zoological organism and become integrated into its metabolism and development. Moreover, as in normal development, there are reciprocal interactions between the 'host' organism and its symbionts that alter gene expression in both sets of cells. The immune system, instead of being seen as functioning solely to keep microbes out of the body, is also found to develop, in part, in dialogue with symbionts. Moreover, the immune system is actively involved in the colonization of the zoological organism, functioning as a mechanism for integrating microbes into the animal-cell community. Symbionts have also been found to constitute a second mode of genetic inheritance, providing selectable genetic variation for natural selection. We develop, grow and evolve as multi-genomic consortia/teams/ecosystems.
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http://dx.doi.org/10.1007/s12038-013-9343-6DOI Listing
April 2014

Late-emigrating trunk neural crest cells in turtle embryos generate an osteogenic ectomesenchyme in the plastron.

Dev Dyn 2013 Nov 6;242(11):1223-35. Epub 2013 Sep 6.

Biology Department, Millersville University, Millersville, Pennsylvania.

Background: The turtle plastron is composed of a keratinized epidermis overlying nine dermal bones. Its developmental origin has been controversial; recent evidence suggests that the plastral bones derive from trunk neural crest cells (NCCs).

Results: This study extends the observations that there is a turtle-specific, second wave of trunk NCC delamination and migration, after the original NCCs have reached their destination and differentiated. This second wave was confirmed by immunohistochemistry in whole-mounts and serial sections, by injecting DiI (1,1', di-octadecyl-3,3,3',3',-tetramethylindo-carbocyanine perchlorate) into the lumen of the neural tube and tracing labeled cells into the plastron, and by isolating neural tubes from older turtle embryos and observing delaminating NCCs. This later migration gives rise to a plastral ectomesenchyme that expresses NCC markers and can be induced to initiate bone formation.

Conclusions: The NCCs of this second migration have properties similar to those of the earlier NCCs, but also express markers characteristic of cranial NCCs. The majority of the cells of the plastron mesenchyme express neural crest markers, and have osteogenic differentiation capabilities that are similar or identical to craniofacial ectomesenchyme. Our evidence supports the contention that turtle plastron bones are derived from a late emigrating population of cells derived from the trunk neural crest.
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http://dx.doi.org/10.1002/dvdy.24018DOI Listing
November 2013

The Embryonic Transcriptome of the Red-Eared Slider Turtle (Trachemys scripta).

PLoS One 2013 19;8(6):e66357. Epub 2013 Jun 19.

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

The bony shell of the turtle is an evolutionary novelty not found in any other group of animals, however, research into its formation has suggested that it has evolved through modification of conserved developmental mechanisms. Although these mechanisms have been extensively characterized in model organisms, the tools for characterizing them in non-model organisms such as turtles have been limited by a lack of genomic resources. We have used a next generation sequencing approach to generate and assemble a transcriptome from stage 14 and 17 Trachemys scripta embryos, stages during which important events in shell development are known to take place. The transcriptome consists of 231,876 sequences with an N50 of 1,166 bp. GO terms and EC codes were assigned to the 61,643 unique predicted proteins identified in the transcriptome sequences. All major GO categories and metabolic pathways are represented in the transcriptome. Transcriptome sequences were used to amplify several cDNA fragments designed for use as RNA in situ probes. One of these, BMP5, was hybridized to a T. scripta embryo and exhibits both conserved and novel expression patterns. The transcriptome sequences should be of broad use for understanding the evolution and development of the turtle shell and for annotating any future T. scripta genome sequences.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0066357PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3686863PMC
October 2017

Turtle origins: picking up speed.

Dev Cell 2013 May;25(4):326-8

Institute of Biotechnology, University of Helsinki, 00014 Helsinki, Finland.

Genomes for three species of turtles were recently reported in Nature Genetics and Genome Biology. The findings of Wang et al. (2013) and Abramyan et al. (2013) place the turtles as a sister group to birds and crocodiles and offer clues to the origins of this group's remarkable physiological traits.
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http://dx.doi.org/10.1016/j.devcel.2013.05.011DOI Listing
May 2013

A symbiotic view of life: we have never been individuals.

Q Rev Biol 2012 Dec;87(4):325-41

Department of Biology, Swarthmore College Swarthmore, Pennsylvania 19081, USA.

The notion of the "biological individual" is crucial to studies of genetics, immunology, evolution, development, anatomy, and physiology. Each of these biological subdisciplines has a specific conception of individuality, which has historically provided conceptual contexts for integrating newly acquired data. During the past decade, nucleic acid analysis, especially genomic sequencing and high-throughput RNA techniques, has challenged each of these disciplinary definitions by finding significant interactions of animals and plants with symbiotic microorganisms that disrupt the boundaries that heretofore had characterized the biological individual. Animals cannot be considered individuals by anatomical or physiological criteria because a diversity of symbionts are both present and functional in completing metabolic pathways and serving other physiological functions. Similarly, these new studies have shown that animal development is incomplete without symbionts. Symbionts also constitute a second mode of genetic inheritance, providing selectable genetic variation for natural selection. The immune system also develops, in part, in dialogue with symbionts and thereby functions as a mechanism for integrating microbes into the animal-cell community. Recognizing the "holobiont"--the multicellular eukaryote plus its colonies of persistent symbionts--as a critically important unit of anatomy, development, physiology, immunology, and evolution opens up new investigative avenues and conceptually challenges the ways in which the biological subdisciplines have heretofore characterized living entities.
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http://dx.doi.org/10.1086/668166DOI Listing
December 2012

Animals in a bacterial world, a new imperative for the life sciences.

Proc Natl Acad Sci U S A 2013 Feb 7;110(9):3229-36. Epub 2013 Feb 7.

Department of Medical Microbiology and Immunology, University of Wisconsin, Madison, WI 53706, USA.

In the last two decades, the widespread application of genetic and genomic approaches has revealed a bacterial world astonishing in its ubiquity and diversity. This review examines how a growing knowledge of the vast range of animal-bacterial interactions, whether in shared ecosystems or intimate symbioses, is fundamentally altering our understanding of animal biology. Specifically, we highlight recent technological and intellectual advances that have changed our thinking about five questions: how have bacteria facilitated the origin and evolution of animals; how do animals and bacteria affect each other's genomes; how does normal animal development depend on bacterial partners; how is homeostasis maintained between animals and their symbionts; and how can ecological approaches deepen our understanding of the multiple levels of animal-bacterial interaction. As answers to these fundamental questions emerge, all biologists will be challenged to broaden their appreciation of these interactions and to include investigations of the relationships between and among bacteria and their animal partners as we seek a better understanding of the natural world.
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http://dx.doi.org/10.1073/pnas.1218525110DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3587249PMC
February 2013

Ecological developmental biology: environmental signals for normal animal development.

Authors:
Scott F Gilbert

Evol Dev 2012 Jan-Feb;14(1):20-8

Swarthmore College, Swarthmore, PA 19081, USA.

The environment plays instructive roles in development and selective roles in evolution. This essay reviews several of the instructive roles whereby the organism has evolved to receive cues from the environment in order to modulate its developmental trajectory. The environmental cues can be abiotic (such as temperature or photoperiod) or biotic (such as those emanating from predators, conspecifics, or food), and the "alteration" produces a normal, not a pathological, phenotype, that is appropriate for the environment. In addition, symbiotic organisms can produce important signals during normal development. Environmental cues can be obligatory, such that the organism cannot develop without the environmental cue. These cues often permit and instruct the organism to proceed from one developmental stage to another, as when larvae receive cues to settle and undergo metamorphosis from substrates. Such obligatory cues can also be given by symbionts, as when Wolbachia bacteria prevent apoptosis in developing ovaries of some wasps. Other environmental cues can be used facultatively, allowing organisms to follow different developmental trajectories depending on whether the cue is present or not. This can be seen in the temperature-dependent determination of sex in many reptiles and in the determination of thermotolerance in aphids by their symbiotic bacteria. Signaling from the environment is essential in development, and co-development appears to be normative between symbionts and their hosts. Here, one sees the reciprocal induction of gene expression, just as within the embryonic organism. The ability of organisms to respond to environmental cues by producing different phenotypes may be critically important in evolution, and it may be an essential feature that can facilitate or limit evolution.
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http://dx.doi.org/10.1111/j.1525-142X.2011.00519.xDOI Listing
July 2013

Commentary: 'The epigenotype' by C.H. Waddington.

Authors:
Scott F Gilbert

Int J Epidemiol 2012 Feb 20;41(1):20-3. Epub 2011 Dec 20.

Department of Biology, Swarthmore College, Swarthmore, PA 19081, USA.

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http://dx.doi.org/10.1093/ije/dyr186DOI Listing
February 2012