There is currently only limited understanding for the mechanisms facilitating the emergence of novel behaviours which may be generated through the co-option and neo-functionalisation of existing pathways or alternatively by the establishment of newly evolved regulatory networks. In particular, the absence of comparative organisms and their phylogenetic context has prevented a full comprehension of the molecular and cellular contribution to the emergence of behavioural diversity. To overcome these challenges, our research group utilises the nematode species Caenorhabditis elegans and Pristionchus pacificus. These species share numerous similarities however, there are also fundamental differences between them. Indeed, some of the most striking differences can be seen in their behaviours and more specifically in their feeding habits as while C. elegans is a microbial feeder, P. pacificus is an omnivorous species and predates on other nematode larvae. The increased feeding complexity and predation in P. pacificus is dependent on the presence of teeth like structures which they use to attack and kill their prey. Importantly, P. pacificus has also acquired a kin-recognition system which prevents the predation of their close relatives. Therefore, we use mutants generated by CRISPR/Cas9, neuronal activity imaging and behavioural assays including recently developed automated tracking methods to functionally and systematically assess behaviours across comparative organisms. With this we aim to establish the proximate (mechanistic) and ultimate (evolutionary) processes generating novel behavioural adaptations.

Pristionchus pacificus adult nematode attacking and killing a C. elegans larvae (Movie is 2x normal speed and taken by Dr Marianne Roca)

(1) The evolution of predation behaviours

Pristionchus are omnivorous nematodes and feed on both microbes and also other nematode larvae. In order to do this, they utilise sophisticated sensory mechanisms to seek out and find food. This food is then taken into the organism through the actions of the pharynx which pumps rhythmically to either draw microbes into its mouth or in the case of predation must utilise the teeth to attack and kill their prey before feeding. Accordingly, P. pacificus demonstrates a greatly increased feeding complexity compared to the strict microbial feeder C. elegans. This includes more sophisticated pharyngeal rhythms and expanded neurotransmitter functions. To understand the evolutionary events behind these behavioural adaptations, we are currently investigating these processes at the genetic, molecular mechanistic and neuronal level to identify the prey detection and predatory mechanisms in P. pacificus.

SEM image looking into the mouth of a predatory nematode. (Image from Lightfoot and Wilecki, 2019, Science).

(2)  The evolution of kin-recognition

Pristionchus nematodes have evolved sophisticated mechanisms to avoid killing their own progeny. To understand how this is possible, we have previously isolated the first component involved in the kin-recognition signalling system which functions through the sensing of a small peptide called self-1. This small peptide is essential to maintain the kin signal however it is not the only component involved. Therefore we are currently attempting to identify other elements involved in this process to begin to understand how Pristionchus larvae ensure they are not cannibalised by their parents. Additionally, we currently understand little of how these signals are received and processed. As the kin-recognition behaviour requires direct contact between the nose of the predator and the nematode larvae, the head sensory circuit of these nematodes are prime candidates for mediating these interactions. Therefore, we are currently investigating the receptors and circuits involved to elucidated the mechanism behind prey sensing and understand how this system may have evolved. 

P. pacificus can distinguish friend from foe upon contact. Here two strains of P. pacificus are stained with different colour fluorescent dyes to track their interactions. (Image from Fumie Hiramatsu)

(3) Tools and techniques

We are continuously trying to improve the molecular methods available in P. pacificus as well as develop new techniques for the community. We are particularly interested in developing new transgenic methods including for the genomic integration of transgenes and developing methods for tracking the distinct P. pacificus behaviour's.

Expression pattern of the kin-recognition component self-1. Transgeneic reporter is made by fusing the promoter of self-1 to TurboRFP.(Image from Lightfoot and Wilecki, 2019, Science).