Neuroethology and chemical ecology of arthropod vector of diseases
Zainulabeuddin (Zain) Syed
Signals & Senses: What do insects smell and how?
All living organisms -- from bacteria to humans -- detect and respond to chemicals in their environment. Insects are the most diverse and adaptable organisms on earth, representing more than half of all the known living organisms. They destroy or eat almost one third of our domesticated crops and produce. Others can transmit various life threatening diseases. Malaria, one of the many diseases transmitted by mosquitoes, takes a human life every 30 seconds in Africa alone.
The remarkable success of insects on earth has largely been due to their ability to adapt to new environments and utilize new food resources. To accomplish this, they display amazing diversity in their sensory structures and function. Among these, olfaction is especially pronounced. In some cases, half of the insect brain is dedicated to smell. A male moth can track a ‘calling’ female from miles. Females, when ready to mate, emit tiny amounts of chemicals that are detected by elaborate and exquisite olfactory organs, antennae, in male moths. Just fifty years ago, the chemical identity of these signaling molecules was determined and the term ‘pheromone’ was coined. Subsequent neuroethological observations were exciting: a single molecule of this newly discovered pheromone chemical from the silk moth, bombykol, was sufficient to elicit an action potential and only a handful of bombykol molecules could induce complete stereotypic female-search behavior in males.
The past two decades have witnessed exciting developments in molecular aspects of insect olfaction. Insect Olfactory Receptor (ORs) have been identified and functionally characterized. Bombykol (above) ORs have been expressed into a surrogate fly (Syed et al, PNAS 2006) and a further functional analysis of those receptors in different settings has shown how a receptor’s function is further modulated by additional proteins, viz. odorant binding proteins (OBP) and odor degrading enzymes (ODE) (Syed et al PNAS 2010).
These seminal discoveries have helped us ask similar question in blood-feeding insects (Guerin et al 2000, Pickett et al 2010). We are trying to understand the conserved signals (http://news.sciencemag.org/sciencenow/2009/10/27-01.html) and receptors amongst blood feeding insects, and how these common principles can help us understand the origin and development of hematophagy.
What are we interested in?
What molecular and cellular elements are involved in detection of olfactory landscape that insects are surrounded with, and how these transduced signals are turned into some meaningful behavior? Our overall objective can be broadly summed up as: what and how insect smell?
The WHAT part deals with identifying the chemicals of biogenic or conspecific origin that act as ligands. The HOW part deals with studies spanning from molecular and cellular elements contributing leading to the detection of these chemical. We extend our studies to organismal response under different behavioral paradigms to the identified stimuli that ultimately form the percept. The overall aim is to exploit this basic understanding of insect olfaction to develop safer and better insect management practices.
How do we study this?
We use a combination of techniques to identify the chemical landscape insects live in. Chemicals from and around the host/attractive substrate (headspace odors) are trapped onto a suitable adsorbent/Solid Phase Micro-Extraction that is injected onto a Gas Chromatogram (GC). Eluted components are split into two after they are resolved at the end of a high resolution capillary column. A major fraction is diverted onto a clean, humidified air flow bathing a live restrained insect and the smaller fraction goes to the chemical detector, FID. Chemical (effluent) induced physiological (olfactory) responses are measured by the electroantennogram (EAG) or Single Unit/Sensillum Recording (SSR) method that measures changes in electrical properties. Thus, constituent chemicals of headspace odors are simultaneously monitored via response from a biological detector (insect) and FID. Therefore GC-EAG and GC-SSR offer a unique platform to use animals as biological sensing elements to identify chemostimuli. Compounds that elicit excitatory and/or inhibitory responses are further screened for their dose-response function to establish their potency. Chemical identity is established by GC-Mass Spectrometry (GC-MS) and further verified by injecting its synthetic standard and measuring the electrophysiological response. These methods have led to identification of unique attractants for tsetse flies (Glossina spp) (Syed and Guerin, J Insect Phyiol 2004) and mosquitoes (Culex quinquefasciatus) (Syed and Leal, PNAS 2009).
From an evolutionary perspective, we are interested in understanding how selective forces shape the repertoire and function of olfactory genes. We employ transgenic methods to express and deorphanize receptors of interest (Syed et al, PNAS 2006; Pelz et al, J Neurobiol; 2006).
And finally, we are very interested in understanding how repulsion is mediated in insects (Syed et al 2011, Syed and Leal 2008). Since insect repellents offer the first line of defense against insect bites -- thus saving us from diseases – we aim to explore this area further.
Syed, Z. and Leal, W. S. 2011. Electrophysiological measurements from a moth olfactory system. Journal of Visual Experimentation (JoVE). DOI: 10.3791/2489.
Syed, Z., Pelletier, J., Flounders, E. and Leal, W. S. 2011. Generic insect repellent detectors from the fruit fly, Drosophila melanogaster. PLoS One. 0.1371/journal.pone.0017705.
Pickett, J.A., Birkett, M.A., Dewhirst, S.Y., Logan, J.G., Omollo, M.O., Torto, B., Pelletier, J., Syed, Z. and Leal, W.S. 2010. Chemical Ecology of Animal and Human Pathogen Vectors in a Changing Global Climate. Journal of Chemical Ecology. 36: 113-121.
Syed, Z., Kopp, A., Kimbrell, D, A. and Leal, W, S. 2010. Bombykol receptors in the silkworm moth and the fruit fly. Proceedings of the National Academy of Science USA. 107: 9436–9439.
Syed, Z. and Leal, W. S. 2009. Acute olfactory response of Culex mosquitoes to a human- and bird-derived attractant. Proceedings of the National Academy of Science USA. 106: 18803–18808 (Recommended by the “Faculty of 1000”). Highlighted “In this issue of the PNAS”. Commentary in Science.
Syed, Z. and Leal, W.S. 2008. Mosquitoes smell and avoid the insect repellent DEET. Proceedings of the National Academy of Science USA. 105: 13598 – 603 (Recommended by the "Faculty of 1000"). From the cover and commentary in PNAS.
Syed, Z. and Leal, W,S. 2007. Maxillary palps in Culex quinquefasciatus Say (Diptera: Culicidae): broad spectrum detectors for host and habitat related chemostimuli. Chemical Senses. 32: 727-738.
Pelz, D., Roeske, T., Syed, Z., Bruyne, M. and Galizia, C, G. 2006. The molecular receptive range of an olfactory receptor in vivo (Drosophila melanogaster Or22a). Journal of Neurobiology. 66: 1544-63.
Syed, Z., Ishida, Y., Taylor, K., Kimbrell, D, A. and Leal, W, S. 2006. Pheromone reception in fruit flies expressing a moth's odorant receptor. Proceedings of the National Academy of Science USA. 103: 16538-43. (Recommended by the “Faculty of 1000”).
Syed, Z., and Guerin. P.M. 2004. Tsetse flies are attracted to the invasive plant Lantana camara. Journal of Insect Physiology. 50: 43-50
Guerin, P.M., Kröber, T., McMahon, C., Guerenstein, P., Grenacher, S., Vlimant M., Diehl, P.A., Steullet, P. and Syed, Z. 2000. Chemosensory and behavioral adaptations of ectoparasitic arthropods. 2000. Novo Acta Leopoldina 83: 197-213.