Ecological developmental biology: environmental signals for normal animal development

Gilbert, Scott F.

doi:10.1111/j.1525-142x.2011.00519.x

Cited by 91 publications

(39 citation statements)

References 98 publications

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“…In many animal species, neuroendocrine signals involving hormones and neuropeptides regulate life cycle transitions (1-3). Environmental cues are often important instructors of the timing of life cycle transitions (4), and can affect behavioral, physiological, or morphological change via neuroendocrine signaling (5).…”

mentioning

confidence: 99%

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

Conzelmann

Williams

Tunaru

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

134

216

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Life-cycle transitions connecting larval and juvenile stages in metazoans are orchestrated by neuroendocrine signals including neuropeptides and hormones. In marine invertebrate life cycles, which often consist of planktonic larval and benthic adult stages, settlement of the free-swimming larva to the sea floor in response to environmental cues is a key life cycle transition. Settlement is regulated by a specialized sensory-neurosecretory system, the larval apical organ. The neuroendocrine mechanisms through which the apical organ transduces environmental cues into behavioral responses during settlement are not yet understood. Here we show that myoinhibitory peptide (MIP)/allatostatin-B, a pleiotropic neuropeptide widespread among protostomes, regulates larval settlement in the marine annelid Platynereis dumerilii. MIP is expressed in chemosensory-neurosecretory cells in the annelid larval apical organ and signals to its receptor, an orthologue of the Drosophila sex peptide receptor, expressed in neighboring apical organ cells. We demonstrate by morpholino-mediated knockdown that MIP signals via this receptor to trigger settlement. These results reveal a role for a conserved MIP receptor-ligand pair in regulating marine annelid settlement.M etazoan life cycles show great diversity in larval, juvenile, and adult forms, as well as in the timing and ecological context of the transitions between these forms. In many animal species, neuroendocrine signals involving hormones and neuropeptides regulate life cycle transitions (1-3). Environmental cues are often important instructors of the timing of life cycle transitions (4), and can affect behavioral, physiological, or morphological change via neuroendocrine signaling (5).Marine invertebrate larval settlement is a prime example of the strong link between environmental cues and the timing of life-cycle transitions. Marine invertebrate life cycles often consist of a free-swimming (i.e., pelagic) larval stage that settles to the ocean floor and metamorphoses into a bottom-dwelling (i.e., benthic) juvenile (6-8). In many invertebrate larvae, a pelagicbenthic transition is induced by chemical cues from the environment (9, 10). Larval settlement commonly includes the cessation of swimming and the appearance of substrate exploratory behavior, including crawling on or attachment to the substrate (11-14). In diverse ciliated marine larvae (15), the apical organ, an anterior cluster of larval sensory neurons (16) with a strong neurosecretory character (17-20), has been implicated in the detection of cues for the initiation of larval settlement (21). Although molecular markers of the apical organ have been described (22-24), our knowledge of the neuroendocrine mechanisms with which apical organ cells transmit signals to initiate larval settlement behavior is incomplete.Here, we identify a conserved myoinhibitory peptide (MIP)/ allatostatin-B receptor-ligand pair as a regulator of larval settlement behavior in the marine polychaete annelid Platynereis dumerilii. MIPs are pleiotro...

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mentioning

confidence: 99%

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

Conzelmann

Williams

Tunaru

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

134

216

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“…Half a century later, however, developmental biologists are reawakening to the significance of the environment, and the need to incorporate developmental context (from physical parameters to interspecific interactions) in attempts to understand the genesis of phenotypes (Gilbert, 2001, 2012; Gilbert and Bolker, ; Gilbert and Epel, ). Establishing experimental, analytical embryology was accomplished in part by isolating the embryo from its surroundings; we can now apply developmental insights and techniques honed in the laboratory in a broader context.…”

Section: Resultsmentioning

confidence: 99%

From experimental zoology to big data: Observation and integration in the study of animal development

Bolker

Brauckmann

2015

J. Exp. Zool.

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Our goal in this paper is to explore the nexus of experiment, observation, and environment in developmental biology, weaving together history and epistemology. We will not attempt a comprehensive treatment of each of these areas. Instead, we use the development of the Journal of Experimental Zoology (JEZ)-which marked its 110th anniversary this past year-as a lens through which to examine how issues of experiment and environment were articulated by some of its founders, and how central questions about how and where to study development continue to resonate a century later.The journal came into being in a tavern in Philadelphia on November 21, 1903. There E.B. Wilson, T.H. Morgan, and E.G. Conklin met to discuss the "the composition of the editorial board, the managing editor, the name, scope and policies of the new publication" (Harrison, '45, xiv). R.G. Harrison was shortly persuaded to serve as the managing editor-a position he held for more than 40 years. ABSTRACTThe founding of the Journal of Experimental Zoology in 1904 was inspired by a widespread turn toward experimental biology in the 19th century. The founding editors sought to promote experimental, laboratory-based approaches, particularly in developmental biology. This agenda raised key practical and epistemological questions about how and where to study development: Does the environment matter? How do we know that a cell or embryo isolated to facilitate observation reveals normal developmental processes? How can we integrate descriptive and experimental data? R.G. Harrison, the journal's first editor, grappled with these questions in justifying his use of cell culture to study neural patterning. Others confronted them in different contexts: for example, F.B. Sumner insisted on the primacy of fieldwork in his studies on adaptation, but also performed breeding experiments using wild-collected animals. The work of Harrison, Sumner, and other early contributors exemplified both the power of new techniques, and the meticulous explanation of practice and epistemology that was marshaled to promote experimental approaches. A century later, experimentation is widely viewed as the standard way to study development; yet at the same time, cutting-edge "big data" projects are essentially descriptive, closer to natural history than to the approaches championed by Harrison et al. Thus, the original questions about how and where we can best learn about development are still with us. Examining their history can inform current efforts to incorporate data from experiment and description, lab and field, and a broad range of organisms and disciplines, into an integrated understanding of animal development.

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“…The digestive system marker genes were identified through domain conservation, reciprocal BLAST and phylogenetic analyses as: extracellular digestive enzymes, peptidases subtilisin-1 and subtilisin-2 (Peptidase_S8; Pfam domain: PF00082), the protease enteropeptidase, responsible for the activation of proteolytic enzymes [49], the polysaccharidedigesting enzyme alpha-amylase, and the intracellular digestive enzyme legumain protease precursor (Figure 1D, I; Additional files 6,7,8). Alpha-amylase and subtilisin-1 expression was restricted to the midgut at 6 dpf, but expanded to mid-and hindgut at 14 dpf and 1 mpf.…”

Section: Resultsmentioning

confidence: 99%

“…Genes were named according to their common conserved domains, reciprocal BLAST to the Homo sapiens peptidome, and neighbor-joining and maximum likelihood phylogenetic analyses (Additional files 7,8). Genes were analyzed for the presence of a signal peptide assigned using the SignalP 4.1 server (http://www.cbs.dtu.dk/services/ SignalP/) and conserved domains assigned by searches in the Pfam database with an e-value cutoff 1e-06 (http:// pfam.xfam.org/search).…”

Section: Platynereis Culturementioning

confidence: 99%

“…These behavioral, physiological and morphological changes have to be tightly coordinated for the successful transition to a benthic life style. Knowledge of how this transition is regulated is important for understanding population structure in the ocean, life-history evolution, and how the environment influences animal life cycles [3][4][5][6][7][8].…”

Section: Introductionmentioning

confidence: 99%

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Myoinhibitory peptide regulates feeding in the marine annelidPlatynereis

Williams

Conzelmann

Jékely

2014

Preprint

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Background: During larval settlement and metamorphosis, marine invertebrates undergo changes in habitat, morphology, behavior and physiology. This change between life-cycle stages is often associated with a change in diet or a transition between a non-feeding and a feeding form. How larvae regulate changes in feeding during this life-cycle transition is not well understood. Neuropeptides are known to regulate several aspects of feeding, such as food search, ingestion and digestion. The marine annelid Platynereis dumerilii has a complex life cycle with a pelagic non-feeding larval stage and a benthic feeding postlarval stage, linked by the process of settlement. The conserved neuropeptide myoinhibitory peptide (MIP) is a key regulator of larval settlement behavior in Platynereis. Whether MIP also regulates the initiation of feeding, another aspect of the pelagic-to-benthic transition in Platynereis, is currently unknown.

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Ecological developmental biology: environmental signals for normal animal development

Cited by 91 publications

References 98 publications

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

Conserved MIP receptor–ligand pair regulates Platynereis larval settlement

From experimental zoology to big data: Observation and integration in the study of animal development

Myoinhibitory peptide regulates feeding in the marine annelidPlatynereis

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