Through the looking glass: Phoresy as seen in the light of mutualism

Abstract

Phoresy is the dispersal of small organisms on larger ones to move out of an unfavourable habitat. Although these interactions are transient, they can form tight links with mutualistic interactions if the phoretic organisms are dependent on both mutualistic partners, one serving as a vehicle with the other providing a substratum for development. These linked tripartite interactions may further lead to increase in host specificity in phoretic organisms. Therefore, to understand the effects of phoretic interactions on the entire mutualistic system and factors that can help the phoretic organisms to gain host-specificity, I investigated the phoretic nematode community associated with the fig–fig wasp brood-site pollination mutualism. I chose Ficus racemosa, a wide-spread and a common tropical keystone fig species, which shows a mutualistic relationship with a unique pollinating fig wasp species and harbours a host-specific phoretic nematode community. Ficus racemosa has an Indo-Australian distribution and is known to be associated with several nematode species throughout its range. A few nematode species have also been reported from India, but they lacked comprehensive detail on their morphology and also molecular characterization, thus making it difficult to carry out further species-specific studies. Therefore, we firstly characterised the phoretic nematode community associated with the Ficus racemosa system in south India, using both morphological and molecular approaches and found a mixture of plant-parasitic, animal-parasitic and possibly omnivorous taxa. We found that the nematode community consisted of three new nematode species out of which one species showed phenotypic plasticity. The phylogenetic analysis based upon near-full-length small subunit (SSU) and D2–D3 expansion segments of large subunit (LSU) rRNA genes showed that the species have close affinities with sister nematode species reported from Ficus racemosa from other geographical locations outside India. To determine the effects of phoretic nematodes on the entire mutualism, we performed various bioassays and determined the fitness effects of phoretic organisms on both mutualistic partners, i.e., figs and pollinator fig wasps. We found that not only did the nematodes negatively affect the survival, flight ability, offspring number and predation risk faced by their fig wasp vehicles, but they also negatively impacted fruit seed number and size in a density-dependent manner. Furthermore, wasps arriving at their destinations carried lower phoretic nematode load compared to dispersing wasps suggesting that there is selection on hitchhiker numbers within a vehicle during the dispersal process. Using choice experiments with single nematodes and employing conspecific as well as heterospecific co-travellers, we showed that these phoretic organisms were able to distinguish between vehicles with different hitchhiker density and physiological states. Plant-parasitic nematodes preferred vehicles devoid of conspecifics and likely hitchhiked in pairs, while animal-parasitic nematodes preferred vehicles with conspecifics within a certain density range. Both types of nematodes were insensitive to the presence of heterospecific co-travellers. The nematodes used volatiles and carbon dioxide for this intra-specific vehicular discrimination. We also characterized the volatiles emitted by the pollinator wasps and identified the possible set of compounds that might elicit an attraction response in the nematodes towards their vehicles. Overall, we show that phoretic nematodes have a density-dependent negative effect on the mutualism between figs and their pollinating fig wasps and that they use parameters such as vehicle physiology and existing traveller load within the vehicle to select a vehicle for their dispersal.