Too many, too few, or empty: The number of passengers determines whether nematodes will hitchhike on a vehicle

This blog post is provided by Satyajeet Gupta and Renee M Borges from the Centre for Ecological Sciences, Indian Institute of Science, Bangalore and tells the #StoryBehindThePaper for the article “Hopping on: Conspecific traveller density within a vehicle regulates parasitic hitchhiking between ephemeral microcosms, which was recently published in the Journal of Animal Ecology.

Tiny organisms that are unable to move far by themselves or assisted by water or wind may hitch rides on other animals to disperse out of habitat patches that become unsuitable due to diminishing food resources, overcrowding or unavailability of mates. The phenomenon of using other animals to disperse is referred to as phoresy and such organisms are called phoretic organisms. Although phoresy is one of the most understudied modes of dispersal, its prevalence has been observed across highly diverse taxa. Among the classic examples of phoresy are ostracods travelling on tree frogs, pseudoscorpions hitching rides on beetles and flower mites using hummingbirds as vehicles. Similar vehicle–passenger interactions have also been observed in the 75+ million-year-old fig–fig wasp brood-site pollination mutualism.

The fig tree Ficus racemosa is a common tropical keystone plant species which shares a mutualistic association with its pollinator fig wasp Ceratosolen fusciceps. Each fig inflorescence acts as a developmental microcosm for pollinator wasps as well as three hitchhiking genera of nematodes, i.e., the herbivorous Schistonchus, the carnivorous Teratodiplogaster and the omnivorous Pristionchus. These nematodes have an obligate vehicle–passenger relationship with the pollinator wasps wherein they enter the abdomen of wasps and use them as vehicles to disperse from one fig inflorescence to another. This hitchhiking relationship is estimated to be 15–45 million years old. The pollinator wasps carry juvenile nematodes to other figs where the nematodes will mature and mate, and their offspring in turn will use the wasps to disperse out of their fig nurseries.

Pollinator fig wasp on the fig syconium surface. Photo credit: Nikhil More

In a previously published study, we showed by experimentally loading different numbers of nematodes onto wasp vehicles that the hitchhiking nematodes behave as harmless commensals at lower numbers while at higher numbers they act as parasites; such parasites negatively affect the survival and reproduction of both their fig wasp vehicles as well as of the host fig trees. These experimental results together with the natural low abundance of nematodes on wasp vehicles that successfully reach their destination suggested that the nematodes might be able to differentiate between wasp vehicles loaded with lower or higher numbers of co-passenger nematodes. We therefore asked the following questions. Do the nematodes estimate the numbers of co-travellers on vehicles before embarking on them? If yes, what are the cues involved? Do they differentiate between co-passengers of the same species (i.e., conspecifics) from co-passengers belonging to different species (i.e., heterospecifics)? Does this discrimination ability differ between carnivorous and herbivorous nematodes?

Adult diplogasterid nematodes under the microscope. Photo credit: Satyajeet Gupta

To answer these intriguing questions, we offered individual nematodes a choice between live fig wasps loaded with varying numbers of conspecific nematodes. As expected, both Schistonchus and Teratodiplogaster avoided overcrowded vehicles and chose to embark onto vehicles with lower numbers of conspecific nematodes. Since vehicles contain potential mates, therefore the presence of conspecifics as co-passengers is vital for reproduction at their destination. Surprisingly, the herbivorous nematodes preferred an empty vehicle while the carnivorous ones did not. The choice of an empty vehicle might sound absurd at first, but when we observed Schistonchus nematodes boarding the empty vehicle “in pairs”, unlike Teratodiplogaster, then we were assured that the choice is correct indeed! Hitchhiking as a pair ensured that the juvenile phoretic nematodes always had a partner to mate with at their final destination. So far, we have found nematodes of both sexes, and no hermaphrodites, but we do not know how the pre-boarding pairing occurs.
Both nematode types were unable to discriminate between live fig wasps loaded with varying numbers of heterospecific nematodes. It appears that the nematodes fail to recognize the presence of heterospecific co-passengers and treat them as empty vehicles.

Well then, how do the nematodes discriminate between vehicles carrying different numbers of conspecifics? Nematodes are known to use a combination of different types of host- specific cues such as chemical and vibrational cues that might play a role in directing them towards their carriers. Since vibrational cues potentially emitted by wasps loaded with different numbers of passengers were hard to mimic, we tested if chemical cues were responsible for the discrimination. Nematodes gather host-specific chemical information by standing on their “tails” and waving their front ends that are laden with sensory structures. This behavior is referred to as nictation. By offering individual nematodes a choice between volatiles emitted by wasps carrying a low or high number of conspecific passengers, we showed that both types of nematodes chose volatiles emitted by wasps carrying fewer passengers. This suggests that hitchhiking nematodes use olfactory cues from their vehicles and co-passengers to choose their vehicles.

The study system – fig plant, fig wasp and nematode parasites. Nematodes prefer to hitchhike on wasps with fewer conspecifics. Photo credit: Satyajeet Gupta

Picking a wasp vehicle with a large number of conspecifics on it might seem lucrative due to the promise of obtaining multiple partners to mate with later, upon reaching the destination site. However, overloaded vehicles have a lower probability of reaching their destination as we have shown before. Therefore, it is essential to choose fig wasp vehicles with low conspecific numbers of nematodes. Through this exciting study, we have thus been able to pinpoint two opposing forces of natural selection – overcrowding and the presence of conspecifics that dictate vehicle choice. The trade-off between these two factors determines which vehicle the hitchhikers will select for dispersing from one host plant to another.

Read the paper

Read the full paper: Gupta, S. and Borges, R.M. (2020), Hopping on: Conspecific traveller density within a vehicle regulates parasitic hitchhiking between ephemeral microcosms. J Anim Ecol. Accepted Author Manuscript.

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