Nathaniel Holmes

Interactions between organisms can vary broadly, spanning mutually beneficial cooperation, bi-directional antagonism and unilateral exploitation. In extreme cases of cooperation, individuals or species can become wholly dependent on one another and neither can survive alone. The precise conditions and mechanisms that lead to the evolution of “obligate” dependency are still largely unclear.

One proposed explanation is that frequent interactions that contribute towards a vital function for an organism - such as metabolism, reproduction or defence - can compensate for subsequent reduction in the organism's own suite of capabilities. Due to these losses, solitary lifestyles become non-viable. Compensated trait loss is readily observed in "micromutualisms" (e.g. cooperative host-microbe interactions) and also in many parasites. Despite this, specific examples of reduced or lost gene function in "macro-"mutualistic systems remain elusive. 

The prevalence of compensated trait loss in defensive relationships is also hard to discern. In these interactions, the costs and benefits for partners are dependent on pressure from other species and outcomes can be difficult to predict across varying contexts. 

My project aims to explore the role of compensated trait-loss in these context-dependent systems, using perhaps the most iconic example of a defensive macromutualism: the relationship between myrmecophytes (ant-plants) and plant-ants. The most specialised myrmecophytic plants provide a combination of housing and expensive food-rewards to ant partners. In exchange, they receive protection from herbivores, pathogens and competitors. 

Intriguingly, some plant-ants have come to reject all food sources except those provided by a host plant.  Many myrmecophytes rapidly succumb to disease or herbivory in the absence of ants. These dependencies may reflect identifiable losses in ant and plant genomes altering their defensive responses and metabolic networks.

Comprehensive characterisation of materials transferred between mutualists - like plant food bodies and nectar, or ant oral secretions - allows contributions to partner nutrition or defence to be explicitly assessed. Combining these data with comparative analyses of ant metabolic networks and plant defensive responses may allow us to identify essential pathways and responses rendered redundant in mutualist species. Using this approach, I aim to uncover those "compensated" genes, pathways and traits that may have undergone trait-loss or exhibit signatures of relaxed selection. 

I’m working with three convergently evolved systems of ants and plants, all found within Costa Rica. Locating and characterising trait losses will help us understand the evolution of obligacy in these relationships, and factors that favour and fix interdependencies across the tree of life. 

Study Systems:

• Vachellia (Acacia s.l.) trees and Pseudomyrmex ants
• Cecropia trees and Azteca ants
• Piper plants and Pheidole bicornis ants
• (Other projects): Philidris nagasau ants and farmed Squamellaria plants
• (Other projects): Cyrtophora citricola spiders