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Minor changes in olfactory sensory pathways can lead to the evolution of new species

Asmita Sengupta

Female apple maggot, Rhagoletis Pomonella
Female apple maggot, Rhagoletis Pomonella   (Photo: By Joseph Berger, Bugwood.org - http://www.insectimages.org/browse/detail.cfm?imgnum=5402797, CC BY 3.0, https://commons.wikimedia.org/w/index.php?curid=11649117)

In his On the Origin of Species’, Charles Darwin had suggested that natural selection is a principal driver of speciation — the formation of new and distinct species. Five years after the publication of Darwin’s work, Benjamin Walsh observed that certain plant-feeding insects could speciate simply through shifts and adaptations to new host plants. The case in point was that of the fly Rhagoletis pomonella which had downy hawthorn (Crataegus spp.) as its native host plant in North America. Since these insects usually show high host-specificity, it was indeed remarkable to discover populations of this species infesting domesticated, introduced apple (Malus pumila) in the mid-1800s in the Hudson Valley region of New York. Subsequently, the populations infesting apples (apple flies) were conferred the status of host race’ to distinguish them from those feeding on hawthorn (hawthorn flies). Speciation occurs when a population of a species becomes so different from other populations of the same species that they cannot interbreed. A host race’ denotes speciation in progress. For the apple and hawthorn flies, the reproductive isolation has been attributed to variations in their olfactory preferences for fruit volatiles found in the host plants. The apple and hawthorn fruit blends differ significantly in terms of volatile compounds that the host racesrespond to. More importantly, the main volatile attractant for apple flies in apple blends is an antagonist for hawthorn flies. Similarly, the major attractant for hawthorn flies found in hawthorn blends is an antagonist for apple flies.

What are the neurophysiological underpinnings for such olfactory discriminations between the host races? Cheyenne Tait, a PhD student at the University of Notre Dame (UND), USA, has addressed this important question for her doctoral dissertation under the co-supervision of Jeff Feder from UND and Shannon Olsson from the National Centre for Biological Sciences (NCBS), Bangalore. With the research team at NCBS, Tait characterised the sensitivity, specificity, and organisation of Olfactory Sensory Neurons (OSN) present on the sensilla (hair-like cuticular structures present on the antennae) of the Rhagoletis,which responded to host and non-host volatiles, to examine the patterns of sensory organisations which contributed to host shifts. 

Scanning electron microscopy was used to observe the antennae of the flies to understand the kind of sensilla present. Following this, single sensillum recording was conducted on adult flies to record the responses to a panel of 76 volatiles. The chief findings, summarised in their recent paper, were as follows: (i) very few OSNs responded to behaviourally active volatiles in the apple and hawthorn fruit blends, (ii) there was no overlap between the OSNs which responded to the active volatiles in the apple blend and those which responded to the active volatiles in the hawthorn blend, and (iii) of the 28OSN classes identified, only two colocalised OSN pairs responded to the major attractant and antagonist volatiles for each of the host races. 

On being asked about the importance of this work with respect to ecology and evolutionary biology, Olsson explained Our work is significant in its implication that even for such complex behaviours as host choice, tiny changes in the nervous system can have dramatic effects on a species, even on an evolutionary timescale. This finding thus has implications beyond evolution for our understanding of the relationships between the brain, behaviour, and animal ecology.” She added that “…we have proposed that such a switch in neural coding could underlie this change in preference for fruit but we have not shown where and how it is happening. Currently, Cheyenne and others in our lab are pursuing a number of experiments to try and track these fruit odours as they are processed in the brain”.