Exploring brain diversity in crustaceans: sensory systems of deep vent shrimps

Julia Machon 1 , Jakob Krieger 2 , Magali Zbinden 1 , Juliette Ravaux 1 , and Steffen Harzschhttp://orcid.org/https://orcid.org/0000-0002-8645-3320 2
  • 1 UMR CNRS MNHN 7208 Biologie des Organismes et Écosystèmes Aquatiques (BOREA), Equipe Adaptation aux Milieux Extrêmes, Sorbonne Université, Paris, France
  • 2 Department of Cytology and Evolutionary Biology, Zoological Institute and Museum, University of Greifswald, Greifswald, Germany
Julia Machon
  • UMR CNRS MNHN 7208 Biologie des Organismes et Écosystèmes Aquatiques (BOREA), Equipe Adaptation aux Milieux Extrêmes, Sorbonne Université, Paris, France
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  • Julia Machon studied Biology at the Sorbonne University (Paris, France). She obtained her Ph.D. degree in 2018 in the team “Adaptation to Extreme Environments”, under the supervision of Dr. Magali Zbinden and Dr. Juliette Ravaux. Her research focused on sensory adaptations -mainly chemoreception- in shrimp from deep-sea hydrothermal vents, using various approaches such as morphology, behavior experiments and electrophysiology. She later worked with the team of Pr. Steffen Harzsch, at the University of Greifswald (Germany) for a collaborative research project to investigate the brain architecture in these rare deep-sea invertebrates.
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, Jakob Krieger
  • Department of Cytology and Evolutionary Biology, Zoological Institute and Museum, University of Greifswald, Greifswald, Germany
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  • Jakob Krieger is a scientific assistant and post doc in Steffen Harzsch’s Lab at the Zoological Institute and Museum of the University of Greifswald. He studied Marine Biology in Rostock and received his Diploma in Biology and his PhD from the University of Greifswald. He worked on crustacean neuroanatomy with emphasis on the olfactory system as well as on behavioral aspects in different malacostracan crustaceans such as coconut crabs, brachyurans, or cleaner shrimps. He is currently analysing the neuroethology of terrestrial hermit crabs related to shell-choice behavior.
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, Magali Zbinden
  • UMR CNRS MNHN 7208 Biologie des Organismes et Écosystèmes Aquatiques (BOREA), Equipe Adaptation aux Milieux Extrêmes, Sorbonne Université, Paris, France
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  • Magali Zbinden studied Biology at the University Pierre and Marie Curie (Paris, France) and obtained her Ph.D degree in Physiology in 2001. Since 2004: Associate professor at Sorbonne University, doing her research on deep-sea biology, and her teaching at the Zoology Department. 2017: French Scientific Habilitation in Life and Health Sciences. She carried out her postdoctoral research at the University of Liège, Belgium (European Ventox and FNRS grant). M. Zbinden works on the biology and physiology of animals associated with chemosynthetic ecosystems, in particular deep hydrothermal vents. Her main research field are: i) study of symbiosis with chemoautotrophic bacteria, ii) sensory perception in hydrothermal shrimp, using morphological, molecular and behavioral approaches andin vivoexperiments in prototype pressurized aquarium developed by our lab (B. Shillito) dedicated to the study and maintenance of deep marine organisms.
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, Juliette Ravaux
  • UMR CNRS MNHN 7208 Biologie des Organismes et Écosystèmes Aquatiques (BOREA), Equipe Adaptation aux Milieux Extrêmes, Sorbonne Université, Paris, France
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  • Juliette Ravaux studied Biology at the University Pierre and Marie Curie (Paris, France) and obtained her Ph.D degree in Invertebrate Physiology in 1999. Since 2000: Associate professor at Sorbonne University, doing her research on deep-sea biology, and her teaching at the Zoology Department. 2014: French Scientific Habilitation in Life and Health Sciences. Her main research topics focus on understanding the adaptations to deep-sea vent environments, and more specifically the strategies to cope with highly variable thermal environments, the adaptation to high hydrostatic pressure, and more recently the sensory functions (as part of the european project Managing Impacts of Deep-sea resource exploitation, Work program ENV.2013.6.2-8 Sustainable management of Europe’s deep sea and sub-sea floor resources, P.I. Pr. Philip Weaver, Southampton, UK).
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and Steffen HarzschORCID iD: https://orcid.org/0000-0002-8645-3320
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  • Department of Cytology and Evolutionary Biology, Zoological Institute and Museum, University of Greifswald, Greifswald, Germany
  • orcid.org/0000-0002-8645-3320
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  • Steffen Harzsch obtained his PhD in 1995 from the University of Bielefeld/Germany with a thesis on the development of crustaceans and continued to work on crustacean neurogenesis as a PostDoc at Wellesley College/Massachusetts. He then moved to the University of Ulm/Germany for comparative analyses of arthropod brains and promoted the discipline “neurophylogeny”, a synthesis of neurobiological studies and phylogenetic aspects. He obtained his habilitation in 2001 and continued to work in Ulm on a Heisenberg stipend funded by the Deutsche Forschungsgemeinschaft. In 2006, Steffen Harzsch moved to Bill Hansson’s group “Evolutionary Neuroethology” at the Max Planck Institute for Chemical Ecology in Jena/Germany as group leader in neuroanatomy focussing on the evolution of arthropod olfactory systems. In 2008, Steffen Harzsch obtained tenure as professor in Cytology and Evolutionary Biology at the Zoological Institute of the University of Greifswald/Germany
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Abstract

The current report focuses on shrimps from deep hydrothermal vents of the Mid-Atlantic Ridge that live in an environment characterized by high hydrostatic pressure, lack of sunlight, and with hot and potentially toxic emissions of black smoker vents. Malacostracan crustaceans display a large diversity of lifestyles and life histories and a rich repertoire of complex behavioral patterns including sophisticated social interactions. These aspects promote this taxon as an interesting group of organisms for those neurobiologists interested in evolutionary transformation of brain structures and evolutionary diversification of neuronal circuits. Here, we explore how analyzing the nervous system of crustacean species from extreme habitats can provide deeper insights into the functional adaptations that drive the diversification of crustacean brain structure.

  • Becker, J.H., Curtis, L.M., and Grutter, A.S. (2005). Cleaner shrimp use a rocking dance to advertise cleaning service to clients. Curr. Biol. 15, 760–764.

    • Crossref
    • PubMed
    • Export Citation
  • Breithaupt, T. and Thiel, M. (2011). Chemical Communication in Crustaceans (New York: Springer).

  • Chamberlain, S.C. (2000). Vision in hydrothermal vent shrimp. Philos. Trans. R. Soc. London B 355, 1151–1154.

    • Crossref
    • Export Citation
  • Charlou, J.L., Donval, J.P., Douville, E., Jean-Baptiste, P., Radford-Knoery, J., Fouquet, Y., Dapoigny, A., Stievenard, M., 2000. Compared geochemical signatures and the evolution of Menez Gwen (37°50′N) and Lucky Strike (37°17′N) hydrothermal fluids, south of the Azores Triple Junction on the Mid-Atlantic Ridge. Chem. Geol. 171, 49–75.

    • Crossref
    • Export Citation
  • Charlou, J.L., Donval, J.P., Fouquet, Y., Jean-Baptiste, P., Holm, N., 2002. Geochemistry of high H2 and CH4 vent fluids issuing from ultramafic rocks at the Rainbow hydrothermal field (36°14′N, MAR). Chem. Geol. 191, 345–359.

    • Crossref
    • Export Citation
  • Charlou, J.L., Donval, J.P., Konn, C., Ondréas, H., Fouquet, Y., Jean‐Baptiste, P., and Fourré, E. (2010). High production and fluxes of H2 and CH4 and evidence of abiotic hydrocarbon synthesis by serpentinization in ultramafic-hosted hydrothermal systems on the Mid-Atlantic Ridge. Geophys. Monogr. Ser. 188, 265–296.

  • Charmantier-Daures, M. and Segonzac, M. (1998). Organ of Bellonci and sinus gland in three decapods from Atlantic hydrothermal vents: Rimicaris exoculata, Chorocaris chacei, and Segonzacia mesatlantica. J. Crustac. Biol. 18, 213–223.

    • Crossref
    • Export Citation
  • Derby, C. and Thiel, M. (2014). Nervous Systems and Control of Behavior (New York: Oxford University Press).

  • Derby, C. and Weissburg, M.J. (2014). The Chemical Senses and Chemosensory Ecology of Crustaceans. Nervous Systems and Control of Behavior. C. Derby and M. Thiel, eds. (New York: Oxford University Press), pp. 263–292.

  • Duffy, J.E. and Thiel, M. (2007). Evolutionary Ecology of Social and Sexual Systems: Crustaceans as Model Organisms (New York: Oxford University Press).

  • Gebruk, A.V., Southward, E.C., Kennedy, H., and Southward, A.J. (2000). Food sources, behaviour, and distribution of hydrothermal vent shrimps at the Mid-Atlantic Ridge. J. Mar. Biol. Assoc. UK 80, 485–499.

    • Crossref
    • Export Citation
  • Hansson, B.S., Harzsch, S., Knaden, M., and Stensmyr, M. (2011). The Neural and Behavioral Basis of Chemical Communication in Terrestrial Crustaceans. Chemical Communication in Crustaceans. T. Breithaupt and M. Thiel, eds. (New York: Springer), pp. 149–173.

  • Harzsch, S. and Hansson, B.S. (2008). Brain architecture in the terrestrial hermit crab Coenobita clypeatus (Anomura, Coenobitidae), a crustacean with a good aerial sense of smell. BMC Neurosci. 9, 58.

    • Crossref
    • PubMed
    • Export Citation
  • Harzsch, S. and Krieger, J. (2018). Crustacean olfactory systems: A comparative review and a crustacean perspective on olfaction in insects. Prog. Neurobiol. 161, 23–60.

    • Crossref
    • Export Citation
  • Hempel, G. (1987). The krill-dominated pelagic system of the Southern Ocean. Environ. Int. 13, 33–36.

    • Crossref
    • Export Citation
  • Herring, P.J., Gaten, E., and Shelton, P.M. (1999). Are vent shrimps blinded by science? Nature 398, 116–116.

  • Jinks, R.N., Battelle, B.-A., Herzog, E.D., Kass, L., Renninger, G.H., and Chamberlain, S.C. (1998). Sensory adaptations in hydrothermal vent shrimps from the Mid-Atlantic Ridge. Cah. Biol. Mar. 39, 309–312.

  • Klaus, S., Mendoza, J.C., Liew, J.H., Plath, M., Meier, R., and Yeo, D.C. (2013). Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs. Biol. Lett. 9, 20121098.

    • PubMed
    • Export Citation
  • Krieger, J., Hörnig, M.K., Sandeman, R.E., Sandeman, D.C., Harzsch, S., 2019. Masters of communication: The brain of the banded cleaner shrimp Stenopus hispidus (Olivier, 1811) with an emphasis on sensory processing areas. J. Comp. Neurol. https://doi.org/10.1002/cne.24831.

    • PubMed
    • Export Citation
  • Krieger, J., Sandeman, R.E., Sandeman, D.C., Hansson, B.S., and Harzsch, S. (2010). Brain architecture of the largest living land arthropod, the Giant Robber Crab Birgus latro (Crustacea, Anomura, Coenobitidae): Evidence for a prominent central olfactory pathway? Front. Zool. 7, 25.

    • Crossref
    • PubMed
    • Export Citation
  • Machon, J., Lucas, P., Ravaux, J., and Zbinden, M. (2018). Comparison of chemoreceptive abilities of the hydrothermal shrimp Mirocaris fortunata and the coastal shrimp Palaemon elegans. Chem. Senses 43, 489–501.

    • Crossref
    • PubMed
    • Export Citation
  • Machon, J., Krieger, J., Meth, R., Zbinden, M., Ravaux, J., Montagne, N., Chertemps, T., and Harzsch, S. (2019). Neuroanatomy of a hydrothermal vent shrimp provides insights into the evolution of crustacean integrative brain centers. ELife 8.

    • PubMed
    • Export Citation
  • Matabos, M., Cuvelier, D., Brouard, J., Shillito, B., Ravaux, J., Zbinden, M., Barthelemy, D., Sarradin, P.M., and Sarrazin, J. (2015). Behavioural study of two hydrothermal crustacean decapods: Mirocaris fortunata and Segonzacia mesatlantica, from the Lucky Strike vent field (Mid-Atlantic Ridge). Deep Sea Res. II 121, 146–158.

    • Crossref
    • Export Citation
  • Maza, F.J., Sztarker, J., Shkedy, A., Peszano, V.N., Locatelli, F.F., and Delorenzi, A. (2016). Context-dependent memory traces in the crab’s mushroom bodies: Functional support for a common origin of high-order memory centers. Proc. Natl. Acad. Sci. 113, E7957–E7965.

    • Crossref
    • Export Citation
  • Moran, D., Softley, R., and Warrant, E.J. (2015). The energetic cost of vision and the evolution of eyeless Mexican cavefish. Sci. Adv. 1, e1500363.

    • PubMed
    • Export Citation
  • Niven, J.E. and Laughlin, S.B. (2008). Energy limitation as a selective pressure on the evolution of sensory systems. J. Exp. Biol. 211, 1792–1804.

    • Crossref
    • PubMed
    • Export Citation
  • Nuckley, D.J., Jinks, R.N., Battelle, B.A., Herzog, E.D., Kass, L., Renninger, G.H., and Chamberlain, S.C. (1996). Retinal anatomy of a new species of bresiliid shrimp from a hydrothermal vent field on the Mid-Atlantic Ridge. Biol. Bull. 190, 98–110.

    • Crossref
    • PubMed
    • Export Citation
  • O’Neill, P.J., Jinks, R.N., Herzog, E.D., Battelle, B.-A., Kass, L., Renninger, G.H., and Chamberlain, S.C. (1995). The morphology of the dorsal eye of the hydrothermal vent shrimp, Rimicaris exoculata. Vis. Neurosci. 12, 861–875.

    • Crossref
    • PubMed
    • Export Citation
  • Patria, M.P. and Wiese, K. (2004). Swimming in formation in krill (Euphausiacea), a hypothesis: Dynamics of the flow field, properties of antennular sensor systems and a sensory-motor link. J. Plankton Res. 26, 1315–1325.

    • Crossref
    • Export Citation
  • Pelli, D.G. and Chamberlain, S.C. (1989). The visibility of 350 °C black-body radiation by the shrimp Rimicaris exoculata and man. Nature 337, 460–461.

    • Crossref
    • PubMed
    • Export Citation
  • Ramm, T. and Scholtz, G. (2017). No sight, no smell? – Brain anatomy of two amphipod crustaceans with different lifestyles. Arthropod Struct. Dev. 46, 537–551.

    • Crossref
    • PubMed
    • Export Citation
  • Renninger, G.H., Kass, L., Gleeson, R.A., Van Dover, C.L., Battelle, B.-A., Jinks, R.N., Herzog, E.D., and Chamberlain, S.C. (1995). Sulfide as a chemical stimulus for deep-sea hydrothermal vent shrimp. Biol. Bull. 189, 69–76.

    • Crossref
    • PubMed
    • Export Citation
  • Richter, S. and Scholtz, G. (2001). Phylogenetic analysis of the Malacostraca (Crustacea). J. Zool. Syst. Evol. Res. 39, 113–136.

    • Crossref
    • Export Citation
  • Sandeman, D., Kenning, M., and Harzsch, S. (2014a). Adaptive trends in malacostracan brain form and function related to behavior. Crustacean Nervous System and their Control of Behavior, Vol. 3. C. Derby and M. Thiel, eds. (New York: Oxford University Press), pp. 11–48.

  • Sandeman, D., Kenning, M., and Harzsch, S. (2014b). Adaptive Trends in Malacostracan Brain form and Function related to Behavior. Crustacean Nervous System and their Control of Behaviour. C. Derby and M. Thiel, eds. (New York: Oxford University Press), pp. 11–48.

  • Sarrazin, J., Juniper, S.K., Massoth, G., and Legendre, P. (1999). Physical and chemical factors influencing species distributions on hydrothermal sulfide edifices of the Juan de Fuca Ridge, northeast Pacific. Mar. Ecol. Prog. Ser. 190, 89–112.

    • Crossref
    • Export Citation
  • Sayre, M.E. and Strausfeld, N.J. (2019). Mushroom bodies in crustaceans: insect-like organization in the caridid shrimp Lebbeus groenlandicus. J. Comp. Neurol. 527, 2371–2387.

    • Crossref
    • PubMed
    • Export Citation
  • Schmidt, M. (2016). Malacostraca. Structure and Evolution of Invertebrate Nervous Systems. A. Schmidt-Rhaesa, S. Harzsch, and G. Purschke, eds. (Oxford: Oxford University Press), pp. 529–582.

  • Schram, F.R. (2013). Comments on crustacean biodiversity and disparity of body plans. Natural History of the Crustacea, Volume 1: Functional morphology and diversity. M. Thiel and G.A. Wellborn, eds. Natural History of Crustacea (New York: Oxford University Press), pp. 1–33.

  • Segonzac, M., De Saint Laurent, M., and Casanova, B. (1993). L’énigme du comportement trophique des crevettes Alvinocarididae des sites hydrothermaux de la dorsale médio-atlantique. Cah. Biol. Mar. 34, 535–571.

  • Stegner, M.E., Stemme, T., Iliffe, T.M., Richter, S., and Wirkner, C.S. (2015). The brain in three crustaceans from cavernous darkness. BMC Neurosci. 16, 19.

    • Crossref
    • PubMed
    • Export Citation
  • Strausfeld, N.J. (2012). Arthropod Brains: Evolution, Functional Elegance, and Historical Significance (Cambridge: Belknap Press).

  • Strausfeld, N.J., Wolff, G.H., and Sayre, M.E. (2020). Mushroom body evolution demonstrates homology and divergence across Pancrustacea. eLIFE 9, e52411.

    • Crossref
    • PubMed
    • Export Citation
  • Sullivan, J.M. and Beltz, B.S. (2001). Neural pathways connecting the deutocerebrum and lateral protocerebrum in the brains of decapod crustaceans. J. Comp. Neurol. 441, 9–22.

    • Crossref
    • PubMed
    • Export Citation
  • Sullivan, J.M. and Beltz, B.S. (2004). Evolutionary changes in the olfactory projection neuron pathways of eumalacostracan crustaceans. J. Comp. Neurol. 470, 25–38.

    • Crossref
    • PubMed
    • Export Citation
  • Thiel, M. and Walting, L. (2015). Lifestyles and Feeding Biology, the Natural History of Crustacea, Vol. 2 (New York: Oxford University Press).

  • Tomsic, D. (2016). Visual motion processing subserving behavior in crabs. Curr. Opin. Neurobiol. 41, 113–121.

    • Crossref
    • PubMed
    • Export Citation
  • Van Dover, C.L. and Fry, B. (1994). Microorganisms as food resources at deep-sea hydrothermal vents. Limnol. Oceanogr. 39, 51–57.

    • Crossref
    • Export Citation
  • Van Dover, C.L., Fry, B., Grassle, J.F., Humphris, S., and Rona, P.A. (1988). Feeding biology of the shrimp Rimicaris exoculata at hydrothermal vents on the Mid-Atlantic Ridge. Mar. Biol. 98, 209–216.

    • Crossref
    • Export Citation
  • Van Dover, C.L., Szuts, E.Z., Chamberlain, S.C., and Cann, J.R. (1989). A novel eye in “eyeless” shrimp from hydrothermal vents of the Mid-Atlantic Ridge. Nature 337, 458–460.

    • Crossref
    • PubMed
    • Export Citation
  • Van Dover, C.L., Reynolds, G.T., Chave, A.D., and Tyson, J.A. (1996). Light at deep-sea hydrothermal vents. Geophys. Res. Lett. 23, 2049–2052.

    • Crossref
    • Export Citation
  • Wirkner, C.S. and Richter, S. (2010). Evolutionary morphology of the circulatory system in Peracarida (Malacostraca; Crustacea). Cladistics 26, 143–167.

    • Crossref
    • Export Citation
  • Wittfoth, C., Harzsch, S., Wolff, C., and Sombke, A. (2010). The “amphi”-brains of amphipods: new insights from the neuroanatomy of Parhyale hawaiensis (Dana, 1853). Front. Zool. 16, 30.

  • Wolff, G.H. and Strausfeld, N.J. (2015). Genealogical correspondence of mushroom bodies across invertebrate phyla. Curr. Biol. 25, 38–44.

    • Crossref
    • PubMed
    • Export Citation
  • Wolff, G., Harzsch, S., Hansson, B.S., Brown, S., and Strausfeld, N. (2012). Neuronal organization of the hemiellipsoid body of the land hermit crab, Coenobita clypeatus: Correspondence with the mushroom body ground pattern. J. Comp. Neurol. 520, 2824–2846.

    • Crossref
    • PubMed
    • Export Citation
  • Wolff, G.H., Thoen, H.H., Marshall, J., Sayre, M.E., and Strausfeld, N.J. (2017). An insect-like mushroom body in a crustacean brain. ELife 6.

  • Zbinden, M., Berthod, C., Montagné, N., Machon, J., Léger, N., Chertemps, T., Rabet, N., Shillito, B., and Ravaux, J. (2017). Comparative study of chemosensory organs of shrimp from hydrothermal vent and coastal environments. Chem. Sens. 42, 319–331.

    • Crossref
    • Export Citation
  • Zbinden, M., Gallet, A., Szafranski, K.M., Machon, J., Ravaux, J., Léger, N., and Duperron, S. (2018). Blow your nose, shrimp! Unexpectedly dense bacterial communities occur on the antennae and antennules of hydrothermal vent Shrimp. Front. Mar. Sci. 5, 357.

    • Crossref
    • Export Citation
  • Zeil, J. and Hemmi, J.M. (2006). The visual ecology of fiddler crabs. J. Comp. Physiol. A 192, 1–25.

    • Crossref
    • Export Citation
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