Susoy, Vladislav et al. (2014) Evolutionary Biology of Caenorhabditis and Other Nematodes "EVOLUTIONARY DIVERSIFICATION THROUGH THE GAIN AND LOSS OF DEVELOPMENTAL PLASTICITY"

Sommer, Ralf J., Susoy, Vladislav, Ragsdale, Erik J.

[Evolutionary Biology of Caenorhabditis and Other Nematodes, 2014]

Developmental plasticity is common among plants and animals, yet its role in mediating evolutionary processes is debated. Several species of Rhabditina, including Pristionchus pacificus, can execute two alternative mouth phenotypes, one of which is associated with predatory feeding. Studies in P. pacificus have revealed that environmental factors act through a conserved genetic pathway that enables a rapid developmental response to the environment (Bento et al., 2010). In addition, a developmental switch that controls the expression of the alternative mouth phenotypes was recently identified (Ragsdale et al., 2013). In contrast, little is known about the macroevolutionary potential of the mouth plasticity. We studied the relationship between plasticity and morphological change by a macroevolutionary analysis of nematode mouthparts when accompanied by a dimorphism. To test whether plasticity facilitates or hinders morphological change, we analyzed variation in form and complexity in 90 nematode species with or without a mouth dimorphism. Our analyses revealed a two-step process of morphological diversification associated with the gain and loss of plasticity. First, acquisition of a dimorphism was accompanied by an increase in complexity, including structural innovations such as moveable teeth. Second, the fixation of a single mouth-phenotype in several nematode lineages was associated with a decrease in mouth complexity but a sharp increase in evolutionary rates when measured as change of shape and size. Thus, plasticity facilitates phenotypic diversification by fostering evolutionary novelties, whereas subsequent loss of the dimorphism enables acceleration of evolution by releasing novel morphologies from developmental constraints. 1. G. Bento, A. Ogawa, R. J. Sommer. Nature 466, 494-497 (2010). 2. E. J. Ragsdale, M. R. Muller, C. Rodelsperger, R. J. Sommer, Cell 155, 922-933 (2013).

Susoy, Vladislav et al. (2019) International Worm Meeting "Mapping circuit-wide neuronal dynamics to a complex goal-directed behavior in C. elegans."

Venkatachalam, Vivek, Hung, Wesley, Zhen, Mei, Susoy, Vladislav, Samuel, Aravinthan, Whitener, Joshua, Wu, Min

[International Worm Meeting, 2019]

A central question in neuroscience is how brain circuits generate animal behavior. Addressing this question would benefit from knowing the system-wide activity patterns during complex, naturalistic tasks, along with synaptic and cellular features of all relevant neurons. We use the mating behavior of C. elegans males as such a paradigm. The mating behavior is an important self-motivated task, consisting of multiple steps with different temporal dynamics. Using customized microscopes build in our laboratory, we performed simultaneous continuous recordings of the activity of all neurons in the male mating circuit over the entirety of mating, while simultaneously tracking the animal's behavior. We have performed in-depth analyses of seven datasets, lasting 5-10 minutes each, that capture a wide range of mating sub-behaviors. Traces of neuronal activity were extracted for more than 60 identified neurons per dataset. Using these recordings in combination with cell-specific interventions, we were able to assign new specific functions to numerous neurons, as well as follow the progression of neuronal responses from sensory inputs to motor outputs. We have identified and confirmed multiple neurons involved in distinct mating steps including searching, scanning, turning, vulva location, excretory pore detection, insemination, and resting. By integrating the neuronal activity time series across experiments, we inferred an underlying functional network. By comparing the functional network with the known anatomical network of synaptic connectivity, we were able to assess the computational significance of electrical and chemical synapses and the sign and strength of interactions between synaptic partners. Our work creates a framework for a complete predictive model of a complex naturalistic behavior from underlying neuronal and circuit activity and connectivity patterns.

Lightfoot, James et al. (2015) International Worm Meeting "Self-Recognition Prevents Cannibalism in Predatory Nematodes."

Lightfoot, James, Moreno, Eduardo, Susoy, Vladislav, Sommer, Ralf, Wilecki, Martin, Rodelsperger, Christian

[International Worm Meeting, 2015]

Self-recognition described as the capacity to discriminate between identical and foreign tissue is observed abundantly throughout nature and is exploited for a plethora of diverse biological functions. These range from the adaptive immune response in jawed vertebrates to neuronal wiring and dendrite self-avoidance in fruit flies to inducing swarming behaviour in bacteria. However, although self-recognition is observed ubiquitously in nature, relatively little is known about the mechanisms behind this phenomenon and surprisingly, despite the pre-eminence of Caernorhabditis elegans as a model organism, evidence of self-recognition has thus far never been described in nematodes. Our recent investigations explored the feeding dynamics in the predatory nematode Pristionchus pacificus and revealed P. pacificus to be voracious killers of C. elegans. We have subsequently, analysed predatory interactions in the context of self-recognition by investigating predation between P. pacificus and its self-progeny. Predation occurs interspecifically between a wide range of closely related nematode species however never on self-progeny, a mechanism that is conserved amongst other Pristionchus species. Furthermore, the ability to determine self from non-self is highly specific with even closely related strains of P. pacificus perceived as prey, while self-progeny are ignored. The identification of self-progeny is dependent on interactions with surface bound molecules, a process which is maintained despite severe starvation and additionally, not disrupted in a host of cuticle morphology mutants. Finally as even closely related P. pacificus strains predate one another while distinguishing and ignoring self-progeny, we have exploited single nucleotide polymorphisms between two strains and generated recombinant inbred lines (RILs) to isolate the genetic component of self-recognition. Each of the RILs was successfully predated by only a single parental lineage facilitating quantitative trait locus (QTL) mapping resulting in the identification of a putative candidate gene and the underlying molecular mechanism. We thus present the first evidence of self-recognition in nematodes, a phenomenon that enables P. pacificus to avoid cannibalism while also promoting the killing of larvae from potential competing nematodes.