Sponge Behavior and the Chemical Basis of Responses: A Post-Genomic View

Leys, Sally P; Mah, Jasmine L; McGill, Paul R; Hamonic, Laura; De Leo, Fabio C; Kahn, Amanda S

doi:10.1093/icb/icz122

Cited by 46Marine Sponges and Natural ProductsMarine Invertebrate Physiology and EcologyEchinoderm biology and ecology

Sponge Behavior and the Chemical Basis of Responses: A Post-Genomic View

Leys, Sally P, Mah, Jasmine L, McGill, Paul R, Hamonic, Laura, De Leo, Fabio C, Kahn, Amanda S·2019·Integrative and Comparative Biology

DOI 10.1093/icb/icz122

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Abstract

Sponges perceive and respond to a range of stimuli. How they do this is still difficult to pin down despite now having transcriptomes and genomes of an array of species. Here we evaluate the current understanding of sponge behavior and present new observations on sponge activity in situ. We also explore biosynthesis pathways available to sponges from data in genomes/transcriptomes of sponges and other non-bilaterians with a focus on exploring the role of chemical signaling pathways mediating sponge behavior and how such chemical signal pathways may have evolved. Sponge larvae respond to light but opsins are not used, nor is there a common photoreceptor molecule or mechanism used across sponge groups. Other cues are gravity and chemicals. In situ recordings of behavior show that both shallow and deep-water sponges move a lot over minutes and hours, and correlation of behavior with temperature, pressure, oxygen, and water movement suggests that at least one sponge responds to changes in atmospheric pressure. The sensors for these cues as far as we know are individual cells and, except in the case of electrical signaling in Hexactinellida, these most likely act as independent effectors, generating a whole-body reaction by the global reach of the stimulus to all parts of the animal. We found no evidence for use of conventional neurotransmitters such as serotonin and dopamine. Intriguingly, some chemicals synthesized by symbiont microbes could mean other more complex signaling occurs, but how that interplay might happen is not understood. Our review suggests chemical signaling pathways found in sponges do not reflect loss of a more complex set.

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The timescale of sensing and action was slow in pre-Cambrian animals, as it is in extant adult sponges.
“Most importantly, the timescale of sensing and action was slow, as it is in extant adult sponges [31].”
From The social origins of consciousness (2025) · cites this paper as [31]

Broad phylogenomic sampling improves resolution of the animal tree of life
Dunn, C. W., Hejnol, A., Matus, D. Q., Pang, K., Browne, W. E., Smith, S. A., Seaver, E., Rouse, G. W., Obst, M., Edgecombe, G. D., et al. (2008) · Nature · doi:10.1038/nature06614 · Cited by 1,921 · see citing works
Chemical Nature of Synaptic Transmission in Vertebrates
Krnjević, K. (1974) · Physiological Reviews · doi:10.1152/physrev.1974.54.2.418 · Cited by 1,613 · see citing works
Sea Anemone Genome Reveals Ancestral Eumetazoan Gene Repertoire and Genomic Organization
Putnam, N. H., Srivastava, M., Hellsten, U., Dirks, B., Chapman, J., Salamov, A., Terry, A., Shapiro, H., Lindquist, E., Kapitonov, V. V., et al. (2007) · Science · doi:10.1126/science.1139158 · Cited by 1,555 · see citing works
The Amphimedon queenslandica genome and the evolution of animal complexity
Srivastava, M., Simakov, O., Chapman, J., Fahey, B., Gauthier, M. E. A., Mitros, T., Richards, G. S., Conaco, C., Dacre, M., Hellsten, U., et al. (2010) · Nature · doi:10.1038/nature09201 · Cited by 1,049 · see citing works
Self-citation
The Trichoplax genome and the nature of placozoans
Srivastava, M., Begovic, E., Chapman, J., Putnam, N. H., Hellsten, U., Kawashima, T., Kuo, A., Mitros, T., Salamov, A., Carpenter, M. L., et al. (2008) · Nature · doi:10.1038/nature07191 · Cited by 889 · see citing works
The ctenophore genome and the evolutionary origins of neural systems
Moroz, L. L., Kocot, K. M., Citarella, M. R., Dosung, S., Norekian, T. P., Povolotskaya, I. S., Grigorenko, A. P., Dailey, C., Berezikov, E., Buckley, K. M., et al. (2014) · Nature · doi:10.1038/nature13400 · Cited by 716 · see citing works
The Genome of the Ctenophore Mnemiopsis leidyi and Its Implications for Cell Type Evolution
Ryan, J. F., Pang, K., Schnitzler, C. E., Nguyen, A.-D., Moreland, R. T., Simmons, D. K., Koch, B. J., Francis, W. R., Havlak, P., Program, N. C. S., et al. (2013) · Science · doi:10.1126/science.1242592 · Cited by 702 · see citing works
Phylogenomics Revives Traditional Views on Deep Animal Relationships
Philippe, H., Derelle, R., Lopez, P., Pick, K., Borchiellini, C., Boury-Esnault, N., Vacelet, J., Renard, E., Houliston, E., Quéinnec, E., et al. (2009) · Current Biology · doi:10.1016/j.cub.2009.02.052 · Cited by 695 · see citing works
Self-citation
The origin and evolution of synapses
Ryan, T. J., & Grant, S. G. N. (2009) · Nature reviews. Neuroscience · doi:10.1038/nrn2717 · Cited by 527 · see citing works
A Prokaryotic Voltage-Gated Sodium Channel
Ren, D., Navarro, B., Xu, H., Yue, L., Shi, Q., & Clapham, D. E. (2001) · Science · doi:10.1126/science.1065635 · Cited by 508 · see citing works
In situ pumping activities of tropical Demospongiae
Reiswig, H. M. (1971) · Marine Biology · doi:10.1007/bf00348816 · Cited by 319 · see citing works
Atlas of Marine Invertebrate Larvae
Young, C. M., Sewell, M. A., & Rice, M. E. (2003) · Aquaculture Research · doi:10.1046/j.1365-2109.2003.00819.x · Cited by 312 · see citing works
Structure and Function of Human Tyrosinase and Tyrosinase‐Related Proteins
Lai, X., Wichers, H. J., Soler‐López, M., & Dijkstra, B. W. (2017) · Chemistry - A European Journal · doi:10.1002/chem.201704410 · Cited by 300 · see citing works
Early metazoan cell type diversity and the evolution of multicellular gene regulation
Sebé-Pedrós, A., Chomsky, E., Pang, K., Lara‐Astiaso, D., Gaiti, F., Mukamel, Z., Amit, I., Hejnol, A., Degnan, B. M., & Tanay, A. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0575-6 · Cited by 292 · see citing works
A Post-Synaptic Scaffold at the Origin of the Animal Kingdom
Sakarya, O., Armstrong, K. A., Adamska, M., Adamski, M., Wang, I.-F., Tidor, B., Degnan, B. M., Oakley, T. H., & Kosik, K. S. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000506 · Cited by 291 · see citing works
Improved Modeling of Compositional Heterogeneity Supports Sponges as Sister to All Other Animals
Feuda, R., Dohrmann, M., Pett, W., Philippe, H., Rota-Stabelli, O., Lartillot, N., Wörheide, G., & Pisani, D. (2017) · Current Biology · doi:10.1016/j.cub.2017.11.008 · Cited by 291 · see citing works
The ecology of the sponge larva
Maldonado, M. (2006) · Canadian Journal of Zoology · doi:10.1139/z05-177 · Cited by 282 · see citing works
Structure and Evolution of Invertebrate Nervous Systems
Schmidt‐Rhaesa, A., Harzsch, S., & Purschke, G. (2015) · doi:10.1093/acprof:oso/9780199682201.001.0001 · Cited by 267 · see citing works
The Analysis of Eight Transcriptomes from All Poriferan Classes Reveals Surprising Genetic Complexity in Sponges
Riesgo, A., Farrar, N., Windsor, P. J., Giribet, G., & Leys, S. P. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu057 · Cited by 266 · see citing works
Self-citation
Anatomy and development of the nervous system of Nematostella vectensis , an anthozoan cnidarian
Marlow, H. Q., Srivastava, M., Matus, D. Q., Rokhsar, D., & Martindale, M. Q. (2009) · Developmental Neurobiology · doi:10.1002/dneu.20698 · Cited by 247 · see citing works
Non-model model organisms
Russell, J. J., Theriot, J. A., Sood, P., Marshall, W. F., Landweber, L. F., Fritz‐Laylin, L. K., Polka, J., Oliferenko, S., Gerbich, T. M., Gladfelter, A. S., et al. (2017) · BMC Biology · doi:10.1186/s12915-017-0391-5 · Cited by 224 · see citing works
Cytological Basis of Photoresponsive Behavior in a Sponge Larva
Leys, S. P., & Degnan, B. M. (2001) · The Biological Bulletin · doi:10.2307/1543611 · Cited by 212 · see citing works
Self-citation
The Non-neuronal Cholinergic System
Wessler, I. K., Kilbinger, H. J., Bittinger, F., et al. (2001) · The Japanese Journal of Pharmacology · doi:10.1254/jjp.85.2 · Cited by 193 · see citing works
Coordinated contractions effectively expel water from the aquiferous system of a freshwater sponge
Elliott, G. R. D., & Leys, S. P. (2007) · Journal of Experimental Biology · doi:10.1242/jeb.003392 · Cited by 189 · see citing works
Self-citation
A Potassium Channel Protein Encoded by Chlorella Virus PBCV-1
Plugge, B., Gazzarrini, S., Nelson, M. B., et al. (2000) · Science · doi:10.1126/science.287.5458.1641 · Cited by 184 · see citing works
The neuropeptide complement of the marine annelid Platynereis dumerilii
Conzelmann, M., Williams, E. A., Krug, K., Franz-Wachtel, M., Macek, B., & Jékely, G. (2013) · BMC Genomics · doi:10.1186/1471-2164-14-906 · Cited by 165 · see citing works
Impulse conduction in a sponge
Leys, S. P., Mackie, G. O., & Meech, R. W. (1999) · Journal of Experimental Biology · doi:10.1242/jeb.202.9.1139 · Cited by 156 · see citing works
Self-citation
Large-Scale Combinatorial Deorphanization of Platynereis Neuropeptide GPCRs
Bauknecht, P., & Jékely, G. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.06.052 · Cited by 154 · see citing works
Cnidarian chemical neurotransmission, an updated overview
Kass-Simon, G., & Pierobon, P. (2007) · Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology · doi:10.1016/j.cbpa.2006.09.008 · Cited by 150 · see citing works
Evolution of sodium channels predates the origin of nervous systems in animals
Liebeskind, B. J., Hillis, D. M., & Zakon, H. H. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1106363108 · Cited by 149 · see citing works
Back to the Basics: Cnidarians Start to Fire
Bosch, T. C. G., Klimovich, A., Domazet-Lošo, T., Gründer, S., Holstein, T. W., Jékely, G., Miller, D. J., Murillo-Rincon, A. P., Rentzsch, F., Richards, G. S., et al. (2017) · Trends in Neurosciences · doi:10.1016/j.tins.2016.11.005 · Cited by 144 · see citing works
Chemical transmission in the sea anemone Nematostella vectensis: a genomic perspective
Anctil, M. (2009) · Comparative Biochemistry and Physiology Part D Genomics and Proteomics · doi:10.1016/j.cbd.2009.07.001 · Cited by 139 · see citing works
Elements of a ‘nervous system’ in sponges
Leys, S. P. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110817 · Cited by 138 · see citing works
Self-citation
Developmental gene expression provides clues to relationships between sponge and eumetazoan body plans
Leininger, S., Adamski, M., Bergum, B., Guder, C., Liu, J., Laplante, M., Bråte, J., Hoffmann, F., Fortunato, S., Jordal, S., et al. (2014) · Nature Communications · doi:10.1038/ncomms4905 · Cited by 136 · see citing works
Reconstruction of the ancestral metazoan genome reveals an increase in genomic novelty
Paps, J., & Holland, P. W. H. (2018) · Nature Communications · doi:10.1038/s41467-018-04136-5 · Cited by 135 · see citing works
Convergent evolution of neural systems in ctenophores
Moroz, L. L. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110692 · Cited by 134 · see citing works
Genomic organization, evolution, and expression of photoprotein and opsin genes in Mnemiopsis leidyi: a new view of ctenophore photocytes
Schnitzler, C. E., Pang, K., Powers, M. L., Reitzel, A. M., Ryan, J. F., Simmons, D., Tada, T., Park, M., Gupta, J., Brooks, S. Y., et al. (2012) · BMC Biology · doi:10.1186/1741-7007-10-107 · Cited by 132 · see citing works
Cilia and the life of ctenophores
Tamm, S. L. (2014) · Invertebrate Biology · doi:10.1111/ivb.12042 · Cited by 129 · see citing works
Evolutionary origins of sensation in metazoans: functional evidence for a new sensory organ in sponges
Ludeman, D. A., Farrar, N. R., Riesgo, A., Paps, J., & Leys, S. P. (2014) · BMC Evolutionary Biology · doi:10.1186/1471-2148-14-3 · Cited by 129 · see citing works
Self-citation
The nervous system of ctenophores III. Ultrastructure of synapses
Hernandez-Nicaise, M.-L. (1973) · Journal of Neurocytology · doi:10.1007/bf01104029 · Cited by 121 · see citing works
Kinetics and rhythm of body contractions in the spongeTethya wilhelma(Porifera: Demospongiae)
Nickel, M. (2004) · Journal of Experimental Biology · doi:10.1242/jeb.01289 · Cited by 120 · see citing works
High Cell Diversity and Complex Peptidergic Signaling Underlie Placozoan Behavior
Varoqueaux, F., Williams, E. A., Grandemange, S., Truscello, L., Kamm, K., Schierwater, B., Jékely, G., & Fasshauer, D. (2018) · Current Biology · doi:10.1016/j.cub.2018.08.067 · Cited by 118 · see citing works
Neuropeptidergic integration of behavior in Trichoplax adhaerens, an animal without synapses
Senatore, A., Reese, T. S., & Smith, C. L. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.162396 · Cited by 113 · see citing works
Intracellular Fate Mapping in a Basal Metazoan, the Ctenophore Mnemiopsis leidyi, Reveals the Origins of Mesoderm and the Existence of Indeterminate Cell Lineages
Martindale, M. Q., & Henry, J. Q. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9427 · Cited by 112 · see citing works
Blue-light-receptive cryptochrome is expressed in a sponge eye lacking neurons and opsin
Rivera, A. S., Öztürk, N., Fahey, B., Plachetzki, D. C., Degnan, B. M., Sancar, A., & Oakley, T. H. (2012) · Journal of Experimental Biology · doi:10.1242/jeb.067140 · Cited by 112 · see citing works
Electrical recording from a glass sponge
Leys, S. P., & Mackie, G. O. (1997) · Nature · doi:10.1038/387029b0 · Cited by 107 · see citing works
Self-citation
Evidence for glutamate, GABA and NO in coordinating behaviour in the sponge, Ephydatia muelleri (Demospongiae, Spongillidae)
Elliott, G. R. D., & Leys, S. P. (2010) · Journal of Experimental Biology · doi:10.1242/jeb.039859 · Cited by 106 · see citing works
Self-citation
Ecological regulation of development: induction of marine invertebrate metamorphosis
Jackson, D. J., Leys, S. P., Hinman, V. F., Woods, R. G., Lavin, M. F., & Degnan, B. M. (2002) · The International Journal of Developmental Biology · doi:10.1387/ijdb.12141457 · Cited by 103 · see citing works
Self-citation
Deep developmental transcriptome sequencing uncovers numerous new genes and enhances gene annotation in the sponge Amphimedon queenslandica
Fernández-Valverde, S. L., Calcino, A., & Degnan, B. M. (2015) · BMC Genomics · doi:10.1186/s12864-015-1588-z · Cited by 101 · see citing works
Embryogenesis and larval differentiation in sponges
Leys, S. P., & Ereskovsky, A. V. (2006) · Canadian Journal of Zoology · doi:10.1139/z05-170 · Cited by 100 · see citing works
Self-citation
Spectral sensitivity in a sponge larva
Leys, S. P., Cronin, T., Degnan, B. M., & Marshall, N. J. (2002) · Journal of Comparative Physiology A · doi:10.1007/s00359-002-0293-y · Cited by 99 · see citing works
Self-citation
5-Hydroxytryptamine-Derived Alkaloids from Two Marine Sponges of the Genus Hyrtios
Salmoun, M., Devijver, C., Daloze, D., Braekman, J. C., & van Soest, R. W. M. (2002) · Journal of Natural Products · doi:10.1021/np020009+ · Cited by 98 · see citing works
Evolutionary emergence of synaptic nervous systems: what can we learn from the non‐synaptic, nerveless Porifera?
Nickel, M. (2010) · Invertebrate Biology · doi:10.1111/j.1744-7410.2010.00193.x · Cited by 93 · see citing works
The reactions of sponges, with a consideration of the origin of the nervous system
Parker, G. H. (1910) · Journal of Experimental Zoology · doi:10.1002/jez.1400080102 · Cited by 91 · see citing works
The contractile sponge epitheliumsensu lato– body contraction of the demospongeTethya wilhelmais mediated by the pinacoderm
Nickel, M., Scheer, C., Hammel, J. U., Herzen, J., & Beckmann, F. (2011) · Journal of Experimental Biology · doi:10.1242/jeb.049148 · Cited by 89 · see citing works
Origin of neuronal-like receptors in Metazoa: cloning of a metabotropic glutamate/GABA-like receptor from the marine sponge Geodia cydonium
Perovic, S., Krasko, A., Prokic, I., Müller, I. M., & Müller, W. E. G. (1999) · Cell and Tissue Research · doi:10.1007/s004410051299 · Cited by 88 · see citing works
Settlement induction of Acropora palmata planulae by a GLW-amide neuropeptide
Erwin, P. M., & Szmant, A. M. (2010) · Coral Reefs · doi:10.1007/s00338-010-0634-1 · Cited by 82 · see citing works
GABA and glutamate specifically induce contractions in the sponge Tethya wilhelma
Ellwanger, K., Eich, A., & Nickel, M. (2006) · Journal of Comparative Physiology A · doi:10.1007/s00359-006-0165-y · Cited by 81 · see citing works
The role of G protein-coupled receptors in the early evolution of neurotransmission and the nervous system
Krishnan, A., & Schiöth, H. B. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110312 · Cited by 81 · see citing works
Atlas of Marine Invertebrate Larvae
Havenhand, J. (2002) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/s0022-0981(02)00277-0 · Cited by 80 · see citing works
Neuroactive substances specifically modulate rhythmic body contractions in the nerveless metazoon Tethya wilhelma (Demospongiae, Porifera)
Ellwanger, K., & Nickel, M. (2006) · Frontiers in Zoology · doi:10.1186/1742-9994-3-7 · Cited by 79 · see citing works
The backbone of the post-synaptic density originated in a unicellular ancestor of choanoflagellates and metazoans
Alié, A., & Manuel, M. (2010) · BMC Evolutionary Biology · doi:10.1186/1471-2148-10-34 · Cited by 79 · see citing works
Convergence of ion channel genome content in early animal evolution
Liebeskind, B. J., Hillis, D. M., & Zakon, H. H. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1501195112 · Cited by 76 · see citing works
Comparative feeding behavior of planktonic ctenophores
Haddock, S. H. D. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm088 · Cited by 75 · see citing works
Genome-wide analysis of the sox family in the calcareous sponge Sycon ciliatum: multiple genes with unique expression patterns
Fortunato, S., Adamski, M., Bergum, B., Guder, C., Jordal, S., Leininger, S., Zwafink, C., Rapp, H. T., & Adamska, M. (2012) · EvoDevo · doi:10.1186/2041-9139-3-14 · Cited by 75 · see citing works
The cellular basis of photobehavior in the tufted parenchymella larva of demosponges
Maldonado, M., Durfort, M., McCarthy, D. A., & Young, C. M. (2003) · Marine Biology · doi:10.1007/s00227-003-1100-1 · Cited by 74 · see citing works
An ancient role for nitric oxide in regulating the animal pelagobenthic life cycle: evidence from a marine sponge
Ueda, N., Richards, G. S., Degnan, B. M., Kranz, A. M., Adamska, M., Croll, R. P., & Degnan, B. M. (2016) · Scientific Reports · doi:10.1038/srep37546 · Cited by 69 · see citing works
The morphology and behaviour of larvae of some intertidal sponges
Bergquist, P. R., & Sinclair, M. E. (1968) · New Zealand Journal of Marine and Freshwater Research · doi:10.1080/00288330.1968.9515247 · Cited by 66 · see citing works
Invertebrate serotonin receptors: a molecular perspective on classification and pharmacology
Tierney, A. J. (2018) · Journal of Experimental Biology · doi:10.1242/jeb.184838 · Cited by 66 · see citing works
Histochemical localization of neurohumors in a sponge
Lentz, T. L. (1966) · Journal of Experimental Zoology · doi:10.1002/jez.1401620204 · Cited by 63 · see citing works
The reactions of sponges, with a consideration of the origin of the nervous system
(1910) · Development Genes and Evolution · doi:10.1007/bf02161768 · Cited by 61 · see citing works
Functionalization of a protosynaptic gene expression network
Conaco, C., Bassett, D. S., Zhou, H., Arcila, M. L., Degnan, B. M., Degnan, B. M., & Kosik, K. S. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1201890109 · Cited by 61 · see citing works
Rethinking the Role of the Nervous System: Lessons From the Hydra Holobiont
Klimovich, A. V., & Bosch, T. C. G. (2018) · BioEssays · doi:10.1002/bies.201800060 · Cited by 61 · see citing works
The origin and evolution of synaptic proteins – choanoflagellates lead the way
Burkhardt, P. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110247 · Cited by 59 · see citing works
The Role of Homology and Orthology in the Phylogenomic Analysis of Metazoan Gene Content
Pett, W., Adamski, M., Adamska, M., Francis, W. R., Eitel, M., Pisani, D., & Wörheide, G. (2019) · Molecular Biology and Evolution · doi:10.1093/molbev/msz013 · Cited by 57 · see citing works
Evolutionary insights into premetazoan functions of the neuronal protein homer
Burkhardt, P., Grønborg, M., McDonald, K., Sulur, T., Wang, Q., & King, N. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu178 · Cited by 56 · see citing works
The GPCR repertoire in the demosponge Amphimedon queenslandica: insights into the GPCR system at the early divergence of animals
Krishnan, A., Dnyansagar, R., Almén, M. S., Williams, M. J., Fredriksson, R., Manoj, N., & Schiöth, H. B. (2014) · BMC Evolutionary Biology · doi:10.1186/s12862-014-0270-4 · Cited by 54 · see citing works
The genome of the contractile demosponge Tethya wilhelma and the evolution of metazoan neural signalling pathwaysPreprint
Francis, W. R., Eitel, M., Vargas, S., Adamski, M., Haddock, S. H. D., Krebs, S., Blum, H., Erpenbeck, D., & Wörheide, G. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/120998 · Cited by 54 · see citing works
New Insights into the Evolution of Metazoan Tyrosinase Gene Family
Esposito, R., D’Aniello, S., Squarzoni, P., Pezzotti, M. R., Ristoratore, F., & Spagnuolo, A. (2012) · PLoS ONE · doi:10.1371/journal.pone.0035731 · Cited by 52 · see citing works
The energetic cost of filtration by demosponges and their behavioural response to ambient currents
Ludeman, D. A., Reidenbach, M. A., & Leys, S. P. (2016) · Journal of Experimental Biology · doi:10.1242/jeb.146076 · Cited by 52 · see citing works
Self-citation
The Presence of a Functionally Tripartite Through-Gut in Ctenophora Has Implications for Metazoan Character Trait Evolution
Presnell, J. S., Vandepas, L. E., Warren, K. J., Swalla, B. J., Amemiya, C. T., & Browne, W. E. (2016) · Current Biology · doi:10.1016/j.cub.2016.08.019 · Cited by 51 · see citing works
Osculum dynamics and filtration activity in small single-osculum explants of the demosponge Halichondria panicea
Kumala, L., Riisgård, H. U., & Canfield, D. E. (2017) · Marine Ecology Progress Series · doi:10.3354/meps12155 · Cited by 51 · see citing works
Origin of the neuro‐sensory system: new and expected insights from sponges
Renard, E., Vacelet, J., Gazave, E., Lapébie, P., Borchiellini, C., & Ereskovsky, A. V. (2009) · Integrative Zoology · doi:10.1111/j.1749-4877.2009.00167.x · Cited by 50 · see citing works
The Behavior of Sponge Larvae
Warburton, F. E. (1966) · Ecology · doi:10.2307/1933952 · Cited by 50 · see citing works
Trichoplax adhaerens (Phylum Placozoa) has Cells that React with Antibodies Against the Neuropeptide RFamide
Schuchert, P. (1993) · Acta Zoologica · doi:10.1111/j.1463-6395.1993.tb01227.x · Cited by 49 · see citing works
Sensory Flask Cells in Sponge Larvae Regulate Metamorphosis via Calcium Signaling
Nakanishi, N., Stoupin, D., Degnan, B. M., & Degnan, B. M. (2015) · Integrative and Comparative Biology · doi:10.1093/icb/icv014 · Cited by 48 · see citing works
Immunocytochemical evidence for biogenic amines and immunogold labeling of serotonergic synapses in tentacles of Aiptasia pallida (Cnidaria, Anthozoa)
Westfall, J. A., Elliott, S. R., MohanKumar, P. S., & Carlin, R. W. (2000) · Invertebrate Biology · doi:10.1111/j.1744-7410.2000.tb00105.x · Cited by 48 · see citing works
Oxygen and the Energetic Requirements of the First Multicellular Animals
Leys, S. P., & KAHN, A. S. (2018) · Integrative and Comparative Biology · doi:10.1093/icb/icy051 · Cited by 46 · see citing works
Self-citation
Think like a sponge: The genetic signal of sensory cells in sponges
Mah, J. L., & Leys, S. P. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.06.012 · Cited by 44 · see citing works
Self-citation
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Müller, W. E. G., Thakur, N. L., Ushijima, H., et al. (2004) · Journal of Cell Science · doi:10.1242/jcs.01083 · Cited by 42 · see citing works
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Wahab, M. A. A., de Nys, R., Webster, N. S., & Whalan, S. (2014) · PLoS ONE · doi:10.1371/journal.pone.0098181 · Cited by 41 · see citing works
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Tiselius, P. T., & Møller, L. F. (2016) · Journal of Plankton Research · doi:10.1093/plankt/fbw096 · Cited by 41 · see citing works
Understanding Animal Evolution: The Added Value of Sponge Transcriptomics and Genomics
Renard, E., Leys, S. P., Wörheide, G., & Borchiellini, C. (2018) · BioEssays · doi:10.1002/bies.201700237 · Cited by 41 · see citing works
Self-citation
Sediment tolerance mechanisms identified in sponges using advanced imaging techniques.
Strehlow, B. W., Pineda, M. C., Duckworth, A. R., et al. (2017) · PubMed · doi:10.7717/peerj.3904 · Cited by 40 · see citing works
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Liu, H., Mishima, Y., Fujiwara, T., et al. (2004) · Marine Drugs · doi:10.3390/md204154 · Cited by 39 · see citing works
A New Flow-Regulating Cell Type in the Demosponge Tethya wilhelma – Functional Cellular Anatomy of a Leuconoid Canal System
Hammel, J. U., & Nickel, M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0113153 · Cited by 34 · see citing works
Comparative transcriptome analysis reveals insights into the streamlined genomes of haplosclerid demosponges
Guzman, C., & Conaco, C. (2016) · Scientific Reports · doi:10.1038/srep18774 · Cited by 34 · see citing works
Evolution of the Pax-Six-Eya-Dach network: the calcisponge case study
Fortunato, S., Leininger, S., & Adamska, M. (2014) · EvoDevo · doi:10.1186/2041-9139-5-23 · Cited by 32 · see citing works
Nitric oxide modulates peristaltic muscle activity associated with fluid circulation in the sea pansyRenilla koellikeri
Anctil, M., Poulain, I., & Pelletier, C. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01607 · Cited by 32 · see citing works
MOTOR REACTIONS OF THE FRESH-WATER SPONGE,EPHYDATIA FLUVIATILIS
McNAIR, G. T. (1923) · Biological Bulletin · doi:10.2307/1536773 · Cited by 32 · see citing works
Phototactic responses of larvae from the marine sponges Neopetrosia proxima and Xestospongia bocatorensis (Haplosclerida: Petrosiidae)
Collin, R., Mobley, A. S., Busutil, L., Leys, S. P., Díaz, M. C., & THACKER, R. W. (2010) · Invertebrate Biology · doi:10.1111/j.1744-7410.2010.00196.x · Cited by 29 · see citing works
Self-citation
Community cascades in a marine pelagic food web controlled by the non-visual apex predator Mnemiopsis leidyi
Tiselius, P., & Møller, L. F. (2017) · Technical University of Denmark, DTU Orbit (Technical University of Denmark, DTU) · Cited by 29 · see citing works
Origin of the Animal Circadian Clock: Diurnal and Light-Entrained Gene Expression in the Sponge Amphimedon queenslandica
Jindrich, K., Roper, K. E., Lemon, S., Degnan, B. M., Reitzel, A. M., & Degnan, B. M. (2017) · Frontiers in Marine Science · doi:10.3389/fmars.2017.00327 · Cited by 28 · see citing works
Mechanical adaptability of a sponge extracellular matrix: evidence for cellular control of mesohyl stiffness inChondrosia reniformisNardo
Wilkie, I. C., Parma, L., Bonasoro, F., et al. (2006) · Journal of Experimental Biology · doi:10.1242/jeb.02527 · Cited by 27 · see citing works
SPONGE LARVAL PHOTOTAXIS: A COMPARATIVE STUDY
Elliott, G. R., & Leys, S. P. (2004) · Cited by 26 · see citing works
Self-citation
Evolutionary conservation of complexins: from choanoflagellates to mice
Yang, X., Pei, J., Kaeser‐Woo, Y. J., Bacaj, T., Grishin, N. V., & Südhof, T. C. (2015) · EMBO Reports · doi:10.15252/embr.201540305 · Cited by 25 · see citing works
Enzymatic 5-hydroxylation of l-dopa by a tyrosinase isolated from the sea anemone Metridium senile
Carlberg, M., Jergil, B., Lindbladh, C., & Rosengren, E. (1984) · General Pharmacology The Vascular System · doi:10.1016/0306-3623(84)90005-3 · Cited by 19 · see citing works
The GABAergic‐like system in the marine demosponge Chondrilla nucula
Ramoino, P., Gallus, L., Paluzzi, S., et al. (2007) · Microscopy Research and Technique · doi:10.1002/jemt.20499 · Cited by 18 · see citing works
The perfection of sponges.
Bidder, G. P. (1937) · Proceedings of the Linnean Society of London · doi:10.1111/j.1095-8312.1937.tb00131.x · Cited by 16 · see citing works
Serotonin in Porifera? Evidence from developing Tedania ignis, the Caribbean fire sponge (Demospongiae)
Weyrer, S., Rützler, K., & Rieger, R. (1999) · Biodiversity Heritage Library (Smithsonian Institution) · Cited by 15 · see citing works
Metabotropic γ‐aminobutyric acid (GABAB) receptors modulate feeding behavior in the calcisponge Leucandra aspera
Ramoino, P., Ledda, F. D., Ferrando, S., Gallus, L., Bianchini, P., Diaspro, A., Fato, M., Tagliafierro, G., & Manconi, R. (2010) · Journal of Experimental Zoology Part A Ecological Genetics and Physiology · doi:10.1002/jez.657 · Cited by 13 · see citing works
Cnidarian neurobiology: what does the future hold?
Anderson, P. A. V. (2007) · Springer eBooks · doi:10.1007/978-1-4020-2762-8_13 · Cited by 12 · see citing works
海洋イチリンソウ属Nematostella vectensisにおける化学的伝達ゲノム展望
Michel, A. (2009) · Cited by 9 · see citing works
Cnidarian neurobiology: what does the future hold?
Anderson, P. A. V. (2004) · Hydrobiologia · doi:10.1007/s10750-004-2660-x · Cited by 9 · see citing works
Catecholic Compounds in Ctenophore Colloblast and Nerve Net Proteins Suggest a Structural Role for DOPA-Like Molecules in an Early-Diverging Animal Lineage
Townsend, J. P., & Sweeney, A. (2018) · Biological Bulletin · doi:10.1086/700695 · Cited by 8 · see citing works

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Authors: Leys, S. P., Mah, J. L., McGill, P. R., Hamonic, L., De Leo, F. C., & Kahn, A. S.
Affiliations: University of Alberta (CA)
Monterey Bay Aquarium Research Institute (US)
Ocean Networks Canada, University of Victoria, Queenswood Campus 100-2474 Arbutus Road, Victoria, British Columbia, Canada V8N 1V8
Corresponding author: Leys, Sally P
ORCID: Leys, Sally P
Mah, Jasmine L
McGill, Paul R
Kahn, Amanda S
Venue: Integrative and Comparative Biology
Publisher: Oxford University Press (OUP)
Published: 2019-07-03
Volume: 59
Issue: 4
Pages: 751-764
ISSN: 1540-7063 (ISSN-L)
1557-7023
DOI: 10.1093/icb/icz122
OpenAlex: W2953817598
Cited by: 46
References: 115
Citations by year: 2026: 3 · 2025: 5 · 2024: 8 · 2023: 3 · 2022: 7 · 2021: 17 · 2020: 3
FWCI: 3.72
Type: journal article
Language: en
Open access: closed
Licence: academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model (vor)
Locations: Integrative and Comparative Biology (publishedVersion)
PubMed (publishedVersion)
Funders: NSERC
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Biotechnology › Marine Sponges and Natural Products
Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Echinoderm biology and ecology
Keywords: sponges, chemical communication, sponge larvae, light response, gravity sensing, atmospheric pressure sensing, sponge genome, biosynthetic pathway, Hexactinellida, evolution of signaling pathways
MeSH terms: Animals, Movement, Porifera, Signal Transduction, Genome, Transcriptome

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Sponge Behavior and the Chemical Basis of Responses: A Post-Genomic View

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