Larval Defense against Attack from Parasitoid Wasps Requires Nociceptive Neurons

Parasitoid wasps are a fierce predator of Drosophila larvae. Female Leptopilina boulardi (LB) wasps use a sharp ovipositor to inject eggs into the bodies of Drosophila melanogaster larvae. The wasp then eats the Drosophila larva alive from the inside, and an adult wasp ecloses from the Drosophila pupal case instead of a fly. However, the Drosophila larvae are not defenseless as they may resist the attack of the wasps through somatosensory-triggered behavioral responses. Here we describe the full range of behaviors performed by the larval prey in immediate response to attacks by the wasps. Our results suggest that Drosophila larvae primarily sense the wasps using their mechanosensory systems. The range of behavioral responses included both “gentle touch” like responses as well as nociceptive responses. We found that the precise larval response depended on both the somatotopic location of the attack, and whether or not the larval cuticle was successfully penetrated during the course of the attack. Interestingly, nociceptive responses are more likely to be triggered by attacks in which the cuticle had been successfully penetrated by the wasp. Finally, we found that the class IV neurons, which are necessary for mechanical nociception, were also necessary for a nociceptive response to wasp attacks. Thus, the class IV neurons allow for a nociceptive behavioral response to a naturally occurring predator of Drosophila.

[1]  M. Galko,et al.  Cytokine Signaling Mediates UV-Induced Nociceptive Sensitization in Drosophila Larvae , 2009, Current Biology.

[2]  T. Schlenke,et al.  Alcohol Consumption as Self-Medication against Blood-Borne Parasites in the Fruit Fly , 2012, Current Biology.

[3]  Richard Y. Hwang,et al.  Thermosensory and nonthermosensory isoforms of Drosophila melanogaster TRPA1 reveal heat-sensor domains of a thermoTRP Channel. , 2012, Cell reports.

[4]  Seol Hee Im,et al.  Pokes, sunburn, and hot sauce: Drosophila as an emerging model for the biology of nociception , 2012, Developmental dynamics : an official publication of the American Association of Anatomists.

[5]  Darren W. Williams,et al.  Cellular mechanisms of dendrite pruning in Drosophila: insights from in vivo time-lapse of remodeling dendritic arborizing sensory neurons , 2005, Development.

[6]  F. Frey,et al.  Immune suppressive virus-like particles in a Drosophila parasitoid: significance of their intraspecific morphological variations , 1996, Parasitology.

[7]  W. A. Johnson,et al.  Enhanced Locomotion Caused by Loss of the Drosophila DEG/ENaC Protein Pickpocket1 , 2003, Current Biology.

[8]  K. Broadie,et al.  Targeted expression of tetanus toxin light chain in Drosophila specifically eliminates synaptic transmission and causes behavioral defects , 1995, Neuron.

[9]  Nathan T. Mortimer,et al.  Integrative Approach Reveals Composition of Endoparasitoid Wasp Venoms , 2013, PloS one.

[10]  Stefan R. Pulver,et al.  An internal thermal sensor controlling temperature preference in Drosophila , 2008, Nature.

[11]  H. L. Carson,et al.  The Genetics and Biology of Drosophila , 1976, Heredity.

[12]  M. Sokolowski,et al.  Drosophila parasitoid-host interactions: vibrotaxis and ovipositor searching from the host's perspective , 1987 .

[13]  Richard Y. Hwang,et al.  Pickpocket Is a DEG/ENaC Protein Required for Mechanical Nociception in Drosophila Larvae , 2010, Current Biology.

[14]  P. Haccou,et al.  INFORMATION PROCESSING BY FORAGERS: EFFECTS OF INTRA-PATCH EXPERIENCE ON THE LEAVING TENDENCY OF LEPTOPILINA HETEROTOMA , 1991 .

[15]  A. Tsubouchi,et al.  Dendritic Filopodia, Ripped Pocket, NOMPC, and NMDARs Contribute to the Sense of Touch in Drosophila Larvae , 2012, Current Biology.

[16]  Y. Jan,et al.  hamlet, a Binary Genetic Switch Between Single- and Multiple- Dendrite Neuron Morphology , 2002, Science.

[17]  Y. Jan,et al.  Integrins Regulate Repulsion-Mediated Dendritic Patterning of Drosophila Sensory Neurons by Restricting Dendrites in a 2D Space , 2012, Neuron.

[18]  Stefan R. Pulver,et al.  Temporal dynamics of neuronal activation by Channelrhodopsin-2 and TRPA1 determine behavioral output in Drosophila larvae. , 2009, Journal of neurophysiology.

[19]  Andrew G Clark,et al.  Contrasting Infection Strategies in Generalist and Specialist Wasp Parasitoids of Drosophila melanogaster , 2007, PLoS pathogens.

[20]  Charles C. Kim,et al.  The microRNA bantam Functions in Epithelial Cells to Regulate Scaling Growth of Dendrite Arbors in Drosophila Sensory Neurons , 2009, Neuron.

[21]  S. Govind,et al.  Virulence factors and strategies of Leptopilina spp.: selective responses in Drosophila hosts. , 2009, Advances in parasitology.

[22]  Y. Carton,et al.  Ecological and genetic interactions in Drosophila-parasitoids communities: a case study with D. melanogaster, D. simulans and their common Leptopilina parasitoids in south-eastern France. , 2004 .

[23]  N. Isidoro,et al.  Functional anatomy of the ovipositor clip in the parasitoid leptopilina heterotoma (Thompson) (Hymenoptera : Eucoilidae), a structure to grip escaping host larvae , 1998 .

[24]  P. Garrity,et al.  Distinct TRP channels are required for warm and cool avoidance in Drosophila melanogaster , 2008, Proceedings of the National Academy of Sciences.

[25]  J. Brenman,et al.  Calcium/Calmodulin-Dependent Protein Kinase II Alters Structural Plasticity and Cytoskeletal Dynamics in Drosophila , 2005, The Journal of Neuroscience.

[26]  Gilles Laurent,et al.  painless, a Drosophila Gene Essential for Nociception , 2003, Cell.

[27]  Yuh Nung Jan,et al.  Tiling of the Drosophila epidermis by multidendritic sensory neurons. , 2002, Development.

[28]  S. Asgari,et al.  Virus or not? Phylogenetics of polydnaviruses and their wasp carriers. , 2003, Journal of insect physiology.

[29]  A. Grafen,et al.  Inferring life history from ovipositor morphology in parasitoid wasps using phylogenetic regression and discriminant analysis , 2003 .

[30]  L. Kaiser,et al.  Differentiation of innate but not learnt responses to host‐habitat odours contributes to rapid host finding in a parasitoid genotype , 2008 .

[31]  Kristin Scott,et al.  Motor Control in a Drosophila Taste Circuit , 2009, Neuron.

[32]  L. Kaiser,et al.  Dynamic use of fruit odours to locate host larvae: individual learning, physiological state and genetic variability as adaptive mechanisms. , 2009, Advances in parasitology.

[33]  Lily Yeh Jan,et al.  Branching out: mechanisms of dendritic arborization , 2010, Nature Reviews Neuroscience.

[34]  A. Nappi,et al.  IN VITRO STUDY OF PHYSIOLOGICAL SUPPRESSION OF SUPERNUMERARY PARASITES BY THE ENDOPARASITIC WASP LEPTOPILINA HETEROTOMA , 1986 .

[35]  Feng Zhang,et al.  Nociceptive Neurons Protect Drosophila Larvae from Parasitoid Wasps , 2007, Current Biology.

[36]  E. Wajnberg,et al.  Time allocation strategies in insect parasitoids: from ultimate predictions to proximate behavioral mechanisms , 2006, Behavioral Ecology and Sociobiology.

[37]  M. Krasnow,et al.  Cellular and Genetic Analysis of Wound Healing in Drosophila Larvae , 2004, PLoS biology.

[38]  C. Lo,et al.  Restrictions in gap junctional communication in the Drosophila larval epidermis , 1992, Developmental dynamics : an official publication of the American Association of Anatomists.

[39]  P. Garrity,et al.  The Drosophila ortholog of vertebrate TRPA1 regulates thermotaxis. , 2005, Genes & development.

[40]  S. Sweeney,et al.  A novel thermosensitive escape behavior in Drosophila larvae , 2011, Fly.

[41]  Y. Jan,et al.  Morphological differentiation of the embryonic peripheral neurons in Drosophila , 1987, Roux's archives of developmental biology.

[42]  A. Patapoutian,et al.  The role of Drosophila Piezo in mechanical nociception , 2011, Nature.

[43]  M. Buffington The occurrence and phylogenetic implications of the ovipositor clip within the Figitidae (Insecta: Hymenoptera: Cynipoidea) , 2007 .

[44]  Yasuyuki Shima,et al.  Opposing roles in neurite growth control by two seven-pass transmembrane cadherins , 2007, Nature Neuroscience.

[45]  C. Zuker,et al.  Genetic dissection of mechanosensory transduction: Mechanoreception-defective mutations of drosophila , 1994, Neuron.

[46]  Michelle E. Kim,et al.  Integrins Establish Dendrite-Substrate Relationships that Promote Dendritic Self-Avoidance and Patterning in Drosophila Sensory Neurons , 2012, Neuron.

[47]  D. Shepherd,et al.  Persistent larval sensory neurons in adult Drosophila melanogaster. , 1999, Journal of neurobiology.