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Lightfoot, J. W.

Publications and source records attributed to Lightfoot, J. W..

10 recordsLinked to original sources

Evidence of a predator-prey co-evolutionary arms race within a nematode microhabitat

Predator-prey interactions are key drivers of behavioural and life-history evolution, yet their mechanisms remain difficult to study in natural contexts. The nematode Pristionchus pacificus is a model predator, but most studies exploring its behaviours use Caenorhabditis elegans as prey, a species that it likely only rarely encountered in nature. Here, we examine predation within nematode communities associated with beetle carcasses, the native necromenic habitat of P. pacificus. We identify Oscheius myriophilus as a cohabiting species, likely representing natural prey. Using predatory assays, automated tracking, and machine-learning-based behavioural analysis, we show that P. pacificus actively kills and consumes O. myriophilus. Strikingly, predation rates are lower than those observed for C. elegans, suggesting partial resistance or reciprocal adaptation in O. myriophilus. Consistent with this, O. myriophilus exhibits a mixed reproductive strategy, with early oviposition followed by ovoviviparity and matricide. As later developmental stages are more resistant to predation, internal hatching may protect offspring while providing maternal resources for development. These findings establish these nematodes as a tractable model for investigating predator-prey interactions and their evolutionary consequences, highlighting how behavioural strategies and life-history traits can co-evolve in natural communities.

evolutionary biology↗

MEC-2/Stomatin is required for aversive behaviour but dispensable for prey detection in the predatory nematode Pristionchus pacificus

Sensory systems provide animals with essential information about their environment and are critical for generating appropriate behaviours. Mechanosensation is a fundamental component of this sensory repertoire, and disruption of mechanosensory pathways can have severe functional consequences. In the nematode Caenorhabditis elegans, mechanosensory circuits have been extensively characterized and mediate touch-driven navigation and avoidance. These circuits rely on conserved molecular components including the stomatin-like protein MEC-2 along with MEC-6, which function together in the mechanotransduction complex. In contrast, the predatory nematode Pristionchus pacificus has repurposed mechanosensory pathways to also enable prey detection, a derived ecological behaviour. As we previously demonstrated that Ppa-mec-6 is required for efficient predation, here we assessed if Ppa-mec-2 plays a similar role in P. pacificus prey detection. We find that while Ppa-mec-2 is required for the aversive touch response, it is dispensable for prey detection. This functional divergence reflects differential neuronal expression as Ppa-mec-2 is absent from the IL2 neurons that mediate prey detection and also robustly express Ppa-mec-6. These findings reveal that partitioning of mechanosensory components across neuronal types enables functional specialization, demonstrating how conserved sensory machinery can support distinct behavioural functions across evolution.

neuroscience↗

Contact-based kin discrimination is associated with specific surface lipids in the cannibalistic nematode Pristionchus pacificus

Kin-recognition is widespread, yet its molecular basis remains poorly understood. In the predatory nematode Pristionchus pacificus, kin-recognition prevents cannibalism of close relatives and depends on the peptide SELF-1. Here, we show this behavior is robust to environmental stress but disrupted by a surfactant wash, implicating lipids or other amphiphilic molecules as necessary components for this mechanism. Using 3D-OrbiSIMS, we profiled the outer cuticle of kin-recognition defective self-1 mutants and found these animals exhibit distinct surface lipids. Furthermore, analysis of surface chemistry defective daf-22 mutants alongside self-1;daf-22 double mutants revealed additional, non-overlapping surface lipid profiles, indicating that multiple pathways contribute to shaping surface lipid composition. Importantly, by combining automated behavioral tracking with state-based analysis, we show daf-22 mutants are also kin-recognition defective. Together, these findings demonstrate that the composition of the nematode surface is required to maintain kin identity, with the cuticle acting as a signaling interface that regulates contact-dependent behaviors. Teaser (125 characters)Surface lipid composition correlates with nematode kin-recognition signaling abilities.

animal behavior and cognition↗

Identity and functions of monoaminergic neurons in the predatory nematode Pristionchus pacificus reveal nervous system conservation and divergence

Changes in neurotransmitter usage in homologous neurons may drive evolutionary adaptations in neural circuits across animal phylogeny. The predatory nematode Pristionchus pacificus can be used as a model system to examine nervous system evolution by comparing neurotransmitter expression with that of C. elegans and other nematodes. Here we characterize P. pacificus neurotransmitter expression and function in specific neurons, focusing on its complete set of monoaminergic neurons. We discover patterns of conservation as well as novelties. We examine the roles of monoamines in specific behaviors using neurotransmitter synthesis and vesicular transporter mutants, finding possible differences in the control of host-finding and dispersal behavior.

neuroscience↗

Evolution of sensory systems underlies the emergence of predatory feeding behaviours in nematodes

Understanding how animal behaviour evolves remains a major challenge, with few studies linking genetic changes to differences in neural function and behaviour across species. Here, we identify specific sensory adaptations associated with the emergence of predatory feeding behaviours in the nematode Pristionchus pacificus. While Caenorhabditis elegans uses contact-dependent sensing primarily to avoid threats, Pristionchus pacificus has co-opted this modality to support both avoidance and prey detection, enabling context-dependent predatory behaviour. To uncover a potential mechanism underlying the evolution of P. pacificus prey perception, we mutated 27 canonical mechanosensory genes and assessed their function using behavioural assays, automated behavioural tracking, and a machine learning analysis of behavioural states. While several mutants showed mechanosensory defects, Ppa-mec-6 mutants specifically also impaired prey detection, indicating the emergence of a novel mechanosensory module linked to predatory behaviour. Furthermore, disrupting both mechanosensation alongside chemosensation revealed a synergistic influence for these modalities. Crucially, both mechanosensation and chemosensation pathways converge in the same environmentally exposed IL2 neurons, and silencing these cells induced severe predation defects validating their importance for prey sensing. Thus, predation evolved through the co-option of mechanosensory and chemosensory systems that act together to shape the evolution of complex behavioural traits.

neuroscience↗

Predatory aggression evolved through adaptations to noradrenergic circuits

Behaviors are adaptive traits evolving through natural selection. Crucially, the genetic, molecular, and neural modifications that shape behavioral innovations are poorly understood. Here, we identify specialized adaptations linked to the evolution of aggression in the predatory nematode Pristionchus pacificus. Using machine learning, we identified robust behavioral states associated with aggressive episodes. These depend on modifications to the invertebrate noradrenergic pathway, with octopamine promoting predatory bouts, and tyramine antagonistically suppressing predation. Strikingly, aggression coincides with rewiring of key circuits across nematode evolution. We find additional octopaminergic neurons with morphological adaptations, including neurites extending to teeth-like structures, and expanded receptor expression throughout head sensory neurons gating prey detection. Thus, evolutionary adaptations in noradrenergic circuits facilitated the emergence of aggressive behavioral states associated with complex predatory traits.

animal behavior and cognition↗

Molecular surface chemistry defines nematode development, identity and behaviour

ABSTRACT/SUMMARYChemical signalling facilitates organismal communication and coordinates physiological and behavioural processes. In nematodes, signalling has predominantly focused on secreted molecules leaving the surfaces communicative potential unexplored. By utilising 3D-OrbiSIMS, an advanced surface-sensitive mass spectrometry method, we directly characterised the molecular composition of the outermost regions (50 nm in depth) of Caenorhabditis elegans and Pristionchus pacificus to improve the understanding of surface-mediated chemical communication. We found that nematode surfaces consist of a lipid-dominated landscape (> 81 % C. elegans and > 69 % P. pacificus of all surveyed chemistries) with distinct compositions, which enrich in granularity and complexity through development. The surface-anchored lipids are also species-specific, reflecting evolutionary and ecological adaptations to their environmental niches. By exploring the effect of mutations on lipid production we found the peroxisomal fatty acid {beta}-oxidation component daf-22 is essential for defining the surface molecular fingerprint. This pathway is conserved across species in producing distinct chemical profiles, indicating its fundamental role in lipid metabolism and for maintaining surface integrity and function. Furthermore, we discovered that variations in surface-anchored lipids of C. elegans daf-22 larvae contribute to significantly increased susceptibility to predation by P. pacificus. Therefore, our findings reveal that the nematode surface is not just a passive boundary but a dynamic signalling platform with evolved, species-specific signatures. These molecular mechanisms are pivotal in shaping identity and communication strategies, providing new insights into the evolutionary and ecological dynamics of chemical signalling across organisms. HIGHLIGHTSO_LINematode surfaces are lipid-rich, changing with development. C_LIO_LISurface lipids are species-specific, reflecting adaptations. C_LIO_LIThe daf-22 gene is key in shaping the surface lipid profile. C_LIO_LISurface lipids mediate predator-prey interactions in nematodes. C_LI

systems biology↗

Kin-recognition shapes collective behaviors in the cannibalistic nematode Pristionchus pacificus

Kin-recognition is observed across diverse species forming an important behavioral adaptation influencing organismal interactions. In most species, proximate level mechanisms are poorly characterized, but in the nematode Pristionchus pacificus molecular components regulating its kin-recognition system have been identified which determine its predatory behaviors. This ability prevents the killing of kin however, its impact on other interactions including collective behaviors is unknown. Utilizing pairwise aggregation assays between distinct strains of P. pacificus, we observed aggregation between kin but not distantly related con-specifics. In these assays, only one strain aggregates with solitary behavior induced in the rival. Abolishing predation through Ppa-nhr-40 mutations results in rival strains successfully aggregating together. Additionally, interactions between P. pacificus populations and Caenorhabditis elegans are dominated by P. pacificus which also disrupts C. elegans aggregation dynamics. Thus, aggregating strains of P. pacificus preferentially group with kin, revealing competition and nepotism as previously unknown components influencing collective behaviors in nematodes.

animal behavior and cognition↗

Conserved nuclear receptors controlling a novel trait target fast-evolving genes expressed in a single cell

Environment shapes development through a phenomenon called developmental plasticity. Deciphering its genetic basis has implications for understanding evolution and adaptation to novel environments, yet molecular studies are scarce. Here, we expanded the gene regulatory network controlling predatory vs. non-predatory morphology in the nematode Pristionchus pacificus. First, we isolated a mutant in the nuclear hormone receptor nhr-1 with a previously unseen phenotypic effect. It disrupts mouth-form determination and results in animals combining features of both wild-type morphs. Further, we identified common targets of NHR-1 and the previously identified nuclear hormone receptor NHR-40 through transcriptomics. Unlike their highly conserved regulators, the target genes have no orthologs in Caenorhabditis elegans and likely result from lineage-specific expansions. An array of transcriptional reporters revealed co-expression of all tested targets in the same pharyngeal gland cell. The morphological remodeling of this cell accompanied the evolution of teeth and predation, linking rapid gene turnover with morphological innovations.

developmental biology↗

Bacterial derived vitamin B12 enhances predatory behaviors in nematodes

The microbiome is known to affect host development, metabolism and immunity, however, its impact on behaviors is only beginning to be understood. Here, we investigate how bacteria modulate complex behaviors in the nematode model organism Pristionchus pacificus. P. pacificus is a predator feeding on the larvae of other nematodes including Caenorhabditis elegans. Growing P. pacificus on different bacteria and testing their ability to kill C. elegans reveals drastic differences in killing efficiencies with a Novosphingobium species showing the strongest enhancement. Strikingly, increased killing was not accompanied by an increase in feeding, a phenomenon known as surplus-killing whereby predators kill more prey than necessary for sustenance. RNA-seq revealed widespread metabolic rewiring upon exposure to Novosphingobium, which facilitated the screening for bacterial mutants leading to an altered transcriptional response. This identified bacterial derived vitamin B12 as a major micronutrient enhancing predatory behaviors. Vitamin B12 is an essential cofactor for detoxification and metabolite biosynthesis and has previously been shown to accelerate development in C. elegans. In P. pacificus vitamin B12 supplementation amplified, whereas mutants in vitamin B12-dependent pathways reduced surplus-killing. This demonstrates that bacterial vitamin B12 affects complex behaviors and thus establishes a connection between microbial diet and the nervous system.

microbiology↗