How do environmental factors influence life cycles and development? An experimental framework for early‐diverging metazoans

Ecological developmental biology (eco‐devo) explores the mechanistic relationships between the processes of individual development and environmental factors. Recent studies imply that some of these relationships have deep evolutionary origins, and may even pre‐date the divergences of the simplest extant animals, including cnidarians and sponges. Development of these early diverging metazoans is often sensitive to environmental factors, and these interactions occur in the context of conserved signaling pathways and mechanisms of tissue homeostasis whose detailed molecular logic remain elusive. Efficient methods for transgenesis in cnidarians together with the ease of experimental manipulation in cnidarians and sponges make them ideal models for understanding causal relationships between environmental factors and developmental mechanisms. Here, we identify major questions at the interface between animal evolution and development and outline a road map for research aimed at identifying the mechanisms that link environmental factors to developmental mechanisms in early diverging metazoans.

[1]  T. Oliver,et al.  Genomic basis for coral resilience to climate change , 2013, Proceedings of the National Academy of Sciences.

[2]  C. M. Lessells,et al.  The Evolution of Life Histories , 1994 .

[3]  S. Bertrand,et al.  Evolutionary crossroads in developmental biology: amphioxus , 2011, Development.

[4]  R. Wootton The evolution of life histories: Theory and analysis , 1993, Reviews in Fish Biology and Fisheries.

[5]  S. Piraino,et al.  Reverse development in Cnidaria , 2004 .

[6]  Jaap A. Kaandorp,et al.  Morphological analysis of growth forms of branching marine sessile organisms along environmental gradients , 1999 .

[7]  Jr-Kai Yu The evolutionary origin of the vertebrate neural crest and its developmental gene regulatory network--insights from amphioxus. , 2010, Zoology.

[8]  Wesley R. Johnson,et al.  The Montastraea faveolata microbiome: ecological and temporal influences on a Caribbean reef-building coral in decline. , 2013, Environmental microbiology.

[9]  M. Hall,et al.  TOR Signaling in Growth and Metabolism , 2006, Cell.

[10]  S. Palumbi,et al.  Tactics of Acclimation: Morphological Changes of Sponges in an Unpredictable Environment , 1984, Science.

[11]  Thomas C G Bosch,et al.  In an early branching metazoan, bacterial colonization of the embryo is controlled by maternal antimicrobial peptides , 2010, Proceedings of the National Academy of Sciences.

[12]  M. Úriz,et al.  Environmental Flow Regimes for Dysidea avara Sponges , 2008, Marine Biotechnology.

[13]  D. Bellwood,et al.  Confronting the coral reef crisis , 2004, Nature.

[14]  I. Berman‐Frank,et al.  Photosynthetic circadian rhythmicity patterns of Symbiodium, the coral endosymbiotic algae , 2013, Proceedings of the Royal Society B: Biological Sciences.

[15]  T. Cronin,et al.  Spectral sensitivity in a sponge larva , 2002, Journal of Comparative Physiology A.

[16]  P. Falkowski,et al.  Photoreceptors in the cnidarian hosts allow symbiotic corals to sense blue moonlight , 2002 .

[17]  Charles H. Mazel,et al.  Discovery of Symbiotic Nitrogen-Fixing Cyanobacteria in Corals , 2004, Science.

[18]  Q. Wang,et al.  Evidence for Multiple Phototransduction Pathways in a Reef-Building Coral , 2012, PloS one.

[19]  A. Böttger,et al.  Genetic screen for signal peptides in Hydra reveals novel secreted proteins and evidence for non-classical protein secretion. , 2006, European journal of cell biology.

[20]  André F. Rendeiro,et al.  Evolutionary conservation of the eumetazoan gene regulatory landscape , 2014, Genome research.

[21]  T. Bosch What Hydra Has to Say About the Role and Origin of Symbiotic Interactions , 2012, The Biological Bulletin.

[22]  L. Holland Genomics, evolution and development of amphioxus and tunicates: The Goldilocks principle. , 2015, Journal of experimental zoology. Part B, Molecular and developmental evolution.

[23]  M. Sarras,et al.  Response to insulin and the expression pattern of a gene encoding an insulin receptor homologue suggest a role for an insulin-like molecule in regulating growth and patterning in Hydra , 1996, Development Genes and Evolution.

[24]  Todd H. Oakley,et al.  Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin , 2012, Journal of Experimental Biology.

[25]  David J. Miller,et al.  Maintenance of ancestral complexity and non-metazoan genes in two basal cnidarians. , 2005, Trends in genetics : TIG.

[26]  C. Voolstra,et al.  Bacterial profiling of White Plague Disease across corals and oceans indicates a conserved and distinct disease microbiome , 2014, Molecular ecology.

[27]  Richard A. Hoover,et al.  Interannual variation of strobilation by the scyphozoan Aurelia labiata in relation to polyp density, temperature, salinity, and light conditions in situ , 2009 .

[28]  S. Stearns Life history evolution: successes, limitations, and prospects , 2000, Naturwissenschaften.

[29]  L. Hyman MISCELLANEOUS OBSERVATIONS ON HYDRA, WITH SPECIAL REFERENCE TO REPRODUCTION , 1928 .

[30]  Sandie M. Degnan,et al.  Genomic insights into the marine sponge microbiome , 2012, Nature Reviews Microbiology.

[31]  L. Dini,et al.  Morphological and ultrastructural analysis of Turritopsis nutricula during life cycle reversal. , 2003, Tissue & cell.

[32]  O. Levy,et al.  Influence of the Quantity and Quality of Light on Photosynthetic Periodicity in Coral Endosymbiotic Algae , 2012, PloS one.

[33]  Peter W. Glynn,et al.  Coral reefs: Corals' adaptive response to climate change , 2004, Nature.

[34]  B. Degnan,et al.  Transcriptome profiling of the demosponge Amphimedon queenslandica reveals genome-wide events that accompany major life cycle transitions , 2012, BMC Genomics.

[35]  N. Webster,et al.  Crustose Coralline Algae and a Cnidarian Neuropeptide Trigger Larval Settlement in Two Coral Reef Sponges , 2012, PloS one.

[36]  B. Willis,et al.  Spatial and temporal genetic structure of Symbiodinium populations within a common reef‐building coral on the Great Barrier Reef , 2013, Molecular ecology.

[37]  D. Roff,et al.  The evolution of trade‐offs: where are we? , 2007, Journal of evolutionary biology.

[38]  M. Maldonado,et al.  The cellular basis of photobehavior in the tufted parenchymella larva of demosponges , 2003 .

[39]  T. Bosch,et al.  Why bacteria matter in animal development and evolution , 2010, BioEssays : news and reviews in molecular, cellular and developmental biology.

[40]  D. Erwin,et al.  The Cambrian Explosion: The Construction of Animal Biodiversity. , 2013 .

[41]  N. Sonenberg,et al.  Upstream and downstream of mTOR. , 2004, Genes & development.

[42]  T. Leitz,et al.  Metamorphosis in the Cnidaria , 2002 .

[43]  T. Bosch,et al.  Embryo protection in contemporary immunology: Why bacteria matter. , 2011, Communicative & integrative biology.

[44]  A. Heyward,et al.  Turbulence, Cleavage, and the Naked Embryo: A Case for Coral Clones , 2012, Science.

[45]  T. Urich,et al.  Metatranscriptomics of the marine sponge Geodia barretti: tackling phylogeny and function of its microbial community. , 2012, Environmental microbiology.

[46]  U. Technau,et al.  Induction of gametogenesis in the basal cnidarian Nematostella vectensis (Anthozoa) , 2002, Development Genes and Evolution.

[47]  K. Sharp,et al.  Multi-Partner Interactions in Corals in the Face of Climate Change , 2012, The Biological Bulletin.

[48]  P. D. Vize,et al.  Transcriptome Analysis of the Circadian Regulatory Network in the Coral Acropora millepora , 2009, The Biological Bulletin.

[49]  B. Willis,et al.  Flexibility in Algal Endosymbioses Shapes Growth in Reef Corals , 2004, Science.

[50]  T. Hughes,et al.  Competitive dominance by tabular corals: an experimental analysis of recruitment and survival of understorey assemblages. , 2000, Journal of experimental marine biology and ecology.

[51]  T. Bosch Cnidarian-microbe interactions and the origin of innate immunity in metazoans. , 2013, Annual review of microbiology.

[52]  H. Nijhout Control Mechanisms of Polyphenic Development in Insects , 1999 .

[53]  The Invertebrates: Protozoa Through Ctenophora , 1940 .

[54]  T. Oliver,et al.  Many corals host thermally resistant symbionts in high-temperature habitat , 2011, Coral Reefs.

[55]  T. Harder,et al.  Induction of Larval Metamorphosis of the Coral Acropora millepora by Tetrabromopyrrole Isolated from a Pseudoalteromonas Bacterium , 2011, PloS one.

[56]  D. Arendt,et al.  Methods for Generating Year-Round Access to Amphioxus in the Laboratory , 2013, PloS one.

[57]  A. Eijkelenboom,et al.  FOXOs: signalling integrators for homeostasis maintenance , 2013, Nature reviews. Molecular cell biology.

[58]  S. Loomis,et al.  The Effects of Elevated Osmotic Concentration on Control of Germination in the Gemmules of Freshwater Sponges Eunapius fragilis and Anheteromeyania ryderi , 2008, Physiological and Biochemical Zoology.

[59]  Ulrich C. Klostermeier,et al.  Molecular signatures of the three stem cell lineages in hydra and the emergence of stem cell function at the base of multicellularity. , 2012, Molecular biology and evolution.

[60]  J. Wiedenmann,et al.  Corals from the Persian/Arabian Gulf as models for thermotolerant reef-builders: prevalence of clade C3 Symbiodinium, host fluorescence and ex situ temperature tolerance. , 2013, Marine pollution bulletin.

[61]  O. Levy,et al.  The effect of temperature compensation on the circadian rhythmicity of photosynthesis in Symbiodinium, coral-symbiotic alga , 2012, Scientific Reports.

[62]  D. Morse,et al.  Morphogen-Based Chemical Flypaper for Agaricia humilis Coral Larvae. , 1994, The Biological bulletin.

[63]  D. Epel,et al.  Beakers versus breakers: how fertilisation in the laboratory differs from fertilisation in nature , 1995, Zygote.

[64]  D. Hayward,et al.  Light-Responsive Cryptochromes from a Simple Multicellular Animal, the Coral Acropora millepora , 2007, Science.

[65]  A. Tarrant,et al.  Light Entrained Rhythmic Gene Expression in the Sea Anemone Nematostella vectensis: The Evolution of the Animal Circadian Clock , 2010, PloS one.

[66]  Nicholas H. Putnam,et al.  Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization , 2007, Science.

[67]  J. V. van Leeuwen,et al.  Re-plumbing in a Mediterranean sponge , 2007, Biology Letters.

[68]  J. E. N. Veron,et al.  Corals in space and time : biogeography and evolution of the Scleractinia , 1995 .

[69]  P. Rosenstiel,et al.  Stem cells and aging from a quasi‐immortal point of view , 2013, BioEssays : news and reviews in molecular, cellular and developmental biology.

[70]  N. Price Habitat selection, facilitation, and biotic settlement cues affect distribution and performance of coral recruits in French Polynesia , 2010, Oecologia.

[71]  L. Muscatine,et al.  Symbiosis: On the Role of Algae Symbiotic with Hydra , 1963, Science.

[72]  R. Hill,et al.  Metamorphosis of broadcast spawning corals in response to bacteria isolated from crustose algae , 2001 .

[73]  First record of photosynthetic cyanobacterial symbionts from mesophotic temperate sponges , 2012 .

[74]  S. Leys,et al.  The analysis of eight transcriptomes from all poriferan classes reveals surprising genetic complexity in sponges. , 2014, Molecular biology and evolution.

[75]  M. Treviño,et al.  Noradrenergic ‘Tone’ Determines Dichotomous Control of Cortical Spike-Timing-Dependent Plasticity , 2012, Scientific Reports.

[76]  K. McGuinness,et al.  Influence of re-orientation on alignment to flow and tissue production in a Spongia sp. (Porifera:Demospongiae:Dictyoceratida) , 2003 .

[77]  T. Bosch Rethinking the role of immunity: lessons from Hydra. , 2014, Trends in immunology.

[78]  M. Berumen,et al.  Trade-offs associated with dietary specialization in corallivorous butterflyfishes (Chaetodontidae: Chaetodon) , 2008, Behavioral Ecology and Sociobiology.

[79]  M. Berumen,et al.  Habitat associations of juvenile versus adult butterflyfishes , 2008, Coral Reefs.

[80]  Todd H. Oakley,et al.  The Amphimedon queenslandica genome and the evolution of animal complexity , 2010, Nature.

[81]  J. Hagadorn,et al.  The fossil record of cnidarian medusae , 2010 .

[82]  R. Steneck,et al.  Running the Gauntlet: Inhibitory Effects of Algal Turfs on the Processes of Coral Recruitment , 2010 .

[83]  Chaolun Allen Chen,et al.  Symbiont communities and host genetic structure of the brain coral Platygyra verweyi, at the outlet of a nuclear power plant and adjacent areas , 2012, Molecular ecology.

[84]  R. Steneck,et al.  Larval settlement preferences and post-settlement survival of the threatened Caribbean corals Acropora palmata and A. cervicornis , 2010, Coral Reefs.

[85]  B. Degnan,et al.  Cytological Basis of Photoresponsive Behavior in a Sponge Larva , 2001, The Biological Bulletin.

[86]  J. Haldane Organisers and Genes , 1940, Nature.

[87]  Y. Loya,et al.  Antimicrobial activity of Red Sea corals , 2006 .

[88]  S. Sunagawa,et al.  Symbiodinium Transcriptomes: Genome Insights into the Dinoflagellate Symbionts of Reef-Building Corals , 2012, PloS one.

[89]  Ulrich C. Klostermeier,et al.  Regulation of Polyp-to-Jellyfish Transition in Aurelia aurita , 2014, Current Biology.

[90]  E. Snell‐Rood,et al.  Mechanisms of Life History Evolution : The Genetics and Physiology of Life History , 2012 .

[91]  T. Fujisawa,et al.  Cnidarians and the evolutionary origin of the nervous system , 2009, Development, growth & differentiation.

[92]  M. Hadfield,et al.  Are G-protein-Coupled Receptors Involved in Mediating Larval Settlement and Metamorphosis of Coral Planulae? , 2012, The Biological Bulletin.

[93]  S. Gilbert Ecological developmental biology: environmental signals for normal animal development , 2012, Evolution & development.

[94]  T. Flatt,et al.  Mechanisms of Life History Evolution: The Genetics and Physiology of Life History Traits and Trade-Offs , 2011 .

[95]  L. Blackall,et al.  Metamorphosis of a Scleractinian Coral in Response to Microbial Biofilms , 2004, Applied and Environmental Microbiology.

[96]  Philip Rosenstiel,et al.  Uncovering the evolutionary history of innate immunity: the simple metazoan Hydra uses epithelial cells for host defence. , 2009, Developmental and comparative immunology.

[97]  S. Gilbert Ecological developmental biology: developmental biology meets the real world. , 2001, Developmental biology.

[98]  O. Hoegh-Guldberg,et al.  Complex Diel Cycles of Gene Expression in Coral-Algal Symbiosis , 2011, Science.

[99]  Jun Wang,et al.  Distinct antimicrobial peptide expression determines host species-specific bacterial associations , 2013, Proceedings of the National Academy of Sciences.

[100]  Koutarou D. Kimura,et al.  daf-2, an insulin receptor-like gene that regulates longevity and diapause in Caenorhabditis elegans. , 1997, Science.

[101]  T. Bosch,et al.  Embryo protection in contemporary immunology , 2011 .

[102]  T. Leitz,et al.  The marine bacterium Alteromonas espejiana induces metamorphosis of the hydroid Hydractinia echinata , 1993 .

[103]  R. Saint,et al.  EST Analysis of the Cnidarian Acropora millepora Reveals Extensive Gene Loss and Rapid Sequence Divergence in the Model Invertebrates , 2003, Current Biology.

[104]  A. Fujiyama,et al.  Using the Acropora digitifera genome to understand coral responses to environmental change , 2011, Nature.

[105]  Oren Levy,et al.  Circadian clocks in symbiotic corals: the duet between Symbiodinium algae and their coral host. , 2014, Marine genomics.

[106]  S. Akira,et al.  Pathogen Recognition and Innate Immunity , 2006, Cell.

[107]  M. Hadfield Biofilms and marine invertebrate larvae: what bacteria produce that larvae use to choose settlement sites. , 2011, Annual review of marine science.

[108]  Joshua S Madin,et al.  Calcification, Storm Damage and Population Resilience of Tabular Corals under Climate Change , 2012, PloS one.

[109]  M. W. Taylor,et al.  Marine sponges and their microbial symbionts: love and other relationships. , 2012, Environmental microbiology.

[110]  Benjamin M. Wheeler,et al.  The dynamic genome of Hydra , 2010, Nature.

[111]  V. Weis,et al.  Study of Cnidarian-Algal Symbiosis in the “Omics” Age , 2012, The Biological Bulletin.

[112]  A. Knoll,et al.  Animals in a bacterial world, a new imperative for the life sciences , 2013, Proceedings of the National Academy of Sciences.

[113]  I. Berman‐Frank,et al.  Photosynthetic circadian rhythmicity patterns of Symbiodium, the coral endosymbiotic algae , 2013, Proceedings of the Royal Society B: Biological Sciences.

[114]  S. Leys,et al.  Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges , 2014, BMC Evolutionary Biology.

[115]  Ulrich C. Klostermeier,et al.  FoxO is a critical regulator of stem cell maintenance in immortal Hydra , 2012, Proceedings of the National Academy of Sciences.

[116]  C. Kenyon A pathway that links reproductive status to lifespan in Caenorhabditis elegans , 2010, Annals of the New York Academy of Sciences.

[117]  N. Funayama The stem cell system in demosponges: suggested involvement of two types of cells: archeocytes (active stem cells) and choanocytes (food-entrapping flagellated cells) , 2012, Development Genes and Evolution.

[118]  Peter W. Glynn,et al.  Corals' adaptive response to climate change: Shifting to new algal symbionts may safeguard devastated reefs from extinction , 2004 .

[119]  S. Künzel,et al.  MyD88-deficient Hydra reveal an ancient function of TLR signaling in sensing bacterial colonizers , 2012, Proceedings of the National Academy of Sciences.

[120]  T. Simpson,et al.  Dormancy among the Porifera: Gemmule Formation and Germination in Fresh-Water and Marine Sponges , 1974 .

[121]  W. Buzgariu,et al.  Autophagy in Hydra: a response to starvation and stress in early animal evolution. , 2009, Biochimica et biophysica acta.

[122]  S. Sugano,et al.  Draft Assembly of the Symbiodinium minutum Nuclear Genome Reveals Dinoflagellate Gene Structure , 2013, Current Biology.