Environmental cues can impact development to elicit distinct phenotypes in the adult. The consequences of phenotypic plasticity can have profound effects on morphology, life cycle, and behavior to increase the fitness of the organism. The molecular mechanisms governing these interactions are beginning to be elucidated in a few cases, such as social insects. Nevertheless, there is a paucity of systems that are amenable to rigorous experimentation, preventing both detailed mechanistic insight and the establishment of a generalizable conceptual framework. The mouth dimorphism of the model nematode Pristionchus pacificus offers the rare opportunity to examine the genetics, genomics, and epigenetics of environmental influence on developmental plasticity. Yet there are currently no easily tunable environmental factors that affect mouth-form ratios and are scalable to large cultures required for molecular biology. Here we present a suite of culture conditions to toggle the mouth-form phenotype of P. pacificus. The effects are reversible, do not require the costly or labor-intensive synthesis of chemicals, and proceed through the same pathways previously examined from forward genetic screens. Different species of Pristionchus exhibit different responses to culture conditions, demonstrating unique gene-environment interactions, and providing an opportunity to study environmental influence on a macroevolutionary scale.
Switching between alternative complex phenotypes is often regulated by "supergenes," polymorphic clusters of linked genes such as in butterfly mimicry. In contrast, phenotypic plasticity results in alternative complex phenotypes controlled by environmental influences rather than polymorphisms. Here, we show that the developmental switch gene regulating predatory versus non-predatory mouth-form plasticity in the nematode Pristionchus pacificus is part of a multi-gene locus containing two sulfatases and two α-N-acetylglucosaminidases (nag). We provide functional characterization of all four genes, using CRISPR-Cas9-based reverse genetics, and show that nag genes and the previously identified eud-1/sulfatase have opposing influences. Members of the multi-gene locus show non-overlapping neuronal expression and epistatic relationships. The locus architecture is conserved in the entire genus Pristionchus. Interestingly, divergence between paralogs is counteracted by gene conversion, as inferred from phylogenies and genotypes of CRISPR-Cas9-induced mutants. Thus, we found that physical linkage accompanies regulatory linkage between switch genes controlling plasticity in P. pacificus.
Phenotypic plasticity has been proposed as an ecological and evolutionary concept. Ecologically, it can help study how genes and the environment interact to produce robust phenotypes. Evolutionarily, as a facilitator it might contribute to phenotypic novelty and diversification. However, the discussion of phenotypic plasticity remains contentious in parts due to the absence of model systems and rigorous genetic studies. Here, we summarize recent work on the nematode Pristionchus pacificus, which exhibits a feeding plasticity allowing predatory or bacteriovorous feeding. We show feeding plasticity to be controlled by developmental switch genes that are themselves under epigenetic control. Phylogenetic and comparative studies support phenotypic plasticity and its role as a facilitator of morphological novelty and diversity.
Resource polyphenisms, where single genotypes produce alternative feeding strategies in response to changing environments, are thought to be facilitators of evolutionary novelty. However, understanding the interplay between environment, morphology, and behavior and its significance is complex. We explore a radiation of Pristionchus nematodes with discrete polyphenic mouth forms and associated microbivorous versus cannibalistic traits. Notably, comparing 29 Pristionchus species reveals that reproductive mode strongly correlates with mouth-form plasticity. Male-female species exhibit the microbivorous morph and avoid parent-offspring conflict as indicated by genetic hybrids. In contrast, hermaphroditic species display cannibalistic morphs encouraging competition. Testing predation between 36 co-occurring strains of the hermaphrodite P. pacificus showed that killing inversely correlates with genomic relatedness. These empirical data together with theory reveal that polyphenism (plasticity), kin recognition, and relatedness are three major factors that shape cannibalistic behaviors. Thus, developmental plasticity influences cooperative versus competitive social action strategies in diverse animals.
Nematodes such as Caenorhabditis elegans are powerful systems to study basically all aspects of biology. Their species richness together with tremendous genetic knowledge from C. elegans facilitate the evolutionary study of biological functions using reverse genetics. However, the ability to identify orthologs of candidate genes in other species can be hampered by erroneous gene annotations. To improve gene annotation in the nematode model organism Pristionchus pacificus, we performed a genome-wide screen for C. elegans genes with potentially incorrectly annotated P. pacificus orthologs. We initiated a community-based project to manually inspect more than two thousand candidate loci and to propose new gene models based on recently generated Iso-seq and RNA-seq data. In most cases, misannotation of C. elegans orthologs was due to artificially fused gene predictions and completely missing gene models. The community-based curation raised the gene count from 25,517 to 28,036 and increased the single copy ortholog completeness level from 86% to 97%. This pilot study demonstrates how even small-scale crowdsourcing can drastically improve gene annotations. In future, similar approaches can be used for other species, gene sets, and even larger communities thus making manual annotation of large parts of the genome feasible.
SummaryMany animal and plant species respond to population density by phenotypic plasticity. To investigate if specific age classes and/or cross-generational signaling affect density-dependent plasticity, we developed a dye-based method to differentiate co-existing nematode populations. We applied this method to Pristionchus pacificus, which develops a predatory mouth form to exploit alternative resources and kill competitors in response to high population densities. Remarkably, adult, but not juvenile, crowding induces the predatory morph in other juveniles. High-performance liquid chromatography-mass spectrometry of secreted metabolites combined with genetic mutants traced this result to the production of stage-specific pheromones. In particular, the P. pacificus-specific di-ascaroside#1 that induces the predatory morph is induced in the last juvenile stage and young adults, even though mouth forms are no longer plastic in adults. Cross-generational signaling between adults and juveniles may serve as an indication of rapidly increasing population size, arguing that age classes are an important component of phenotypic plasticity.
Developmental plasticity is the ability of a genotype to express multiple phenotypes under different environmental conditions and has been shown to facilitate the evolution of novel traits. However, while the associated cost of plasticity, i.e., the loss in fitness due to the ability to express plasticity in response to environmental change, and the cost of phenotype, i.e., the loss of fitness due to expressing a fixed phenotype across environments, have been theoretically predicted, empirically such costs remain poorly documented and little understood. Here, we use a plasticity model system, hermaphroditic nematode Pristionchus pacificus, to experimentally measure these costs in wild isolates under controlled laboratory conditions. P. pacificus can develop either a bacterial feeding or predatory mouth morph in response to different external stimuli, with natural variation of mouth-morph ratios between strains. We first demonstrated the cost of phenotype by analyzing fecundity and developmental speed in relation to mouth morphs across the P. pacificus phylogenetic tree. Then, we exposed P. pacificus strains to two distinct microbial diets that induce strain-specific mouth-form ratios. Our results indicate that the plastic strain does shoulder a cost of plasticity, i.e., the diet-induced predatory mouth morph is associated with reduced fecundity and slower developmental speed. In contrast, the non-plastic strain suffers from the cost of phenotype since its phenotype does not change to match the unfavorable bacterial diet but shows increased fitness and higher developmental speed on the favorable diet. Furthermore, using a stage-structured population model based on empirically derived life history parameters, we show how population structure can alleviate the cost of plasticity in P. pacificus. The results of the model illustrate the extent to which the costs associated with plasticity and its effect on competition depend on ecological factors. This study provides support for costs of plasticity and phenotype based on empirical and modeling approaches.
1Animals and plants can predict decreasing food supplies by recognition of population density, 2 and respond by adjusting behavioral and morphological traits. Population density in nematodes 3 is detected through pheromones, influencing dormant (dauer) stage entry, and in some lineages 4 alternative mouth-form decision (bacterivorous vs. predatory). Whether age is a relevant 5 parameter in recognizing population density is not well understood. Here, we utilized the mouth-6 form plasticity of the model nematode Pristionchus pacificus and developmental pheromone 7 profiling to study potential parent:progeny communication. Surprisingly, we observed adult-8 specific production of molecules that induce the predatory morph, even though adult mouth 9 forms are no longer plastic. We introduce a novel dye-based method to differentiate populations 10 in mixed-generation cultures, and found adults, but not peers, influence developing juvenile 11 mouth forms. Finally, we applied a logistic growth model that demonstrates adults both lower 12 the population carrying capacity and decrease the time until resource depletion. In the 13 necromenic life cycle of P. pacificus, we view mouth-form plasticity as an alternative 'Malthusian 14 escape' strategy to dauer that responds to age-specific population densities. The copyright holder for this preprint (which was not . http://dx.doi.org/10.1101/291591 doi: bioRxiv preprint first posted online Mar. 29, 2018; Population density is an important ecological parameter that correlates with increased 26 competition for resources 1 . In addition to density-dependent selection 2 , which operates on 27 evolutionary time scales, some organisms can respond dynamically to population density by 28 phenotypic plasticity. For example, plants can sense crowding by detecting the ratio of red 29 (chlorophyll absorbing) to far red (non-absorbing) light, and respond by various shade-30 avoidance strategies including higher shoots 3 . Locusts undergo solitary to swarm (i.e. 31 gregarious) transition, and aphids can develop wings, both as a result of increased physical 32 mechanosensory contact [4][5][6] . Intriguingly, population density can also have transgenerational 33 effects. For example, adult crowding of the desert locust Schistocerca gregaria 7,8 and migratory 34 locust Locusta migratoria 9 also influences the egg size, number, and morphology of their 35 progeny, and high population densities of red squirrels elicit hormonal regulation in mothers to 36 influence faster developing offspring 10 . Nevertheless, while incorporating age into population 37 structures has significantly advanced density-dependent selection theory 11 , surprisingly little 38age-specific refinement has been incorporated into models of phenotypic plasticity, especially at 39 the mechanistic level. This is partly due to the competing challenges of (1) studying population 40 ecology in the laboratory, and (2) the paucity of laboratory model organisms that are suitable for 41 ecological studies. The model nematode ...
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