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The diversity of form in animals is an astonishing phenomenon to behold. One can see it among even some of the smallest multicellular organisms, the nematodes, and above all in their feeding structures. Nematodes lead virtually every lifestyle known to animals and include microbivores, omnivores, predators, and parasites of insects, vertebrates, and plants. The functional diversity of nematodes, which may be the most abundant and species-rich animals on earth, is reflected in their mouthparts. Our lab aims to understand the evolution of this diversity through approaches integrating developmental genetics, phylogenetics, genomics, and natural history.

Research in the lab examines how development and ecology interact to translate genotypes to phenotypes – particularly, through developmental plasticity – and how this interaction influences the evolution and diversification of form. The reference point and central model system for this research is the nematode Pristionchus pacificus. This species has a structural innovation, moveable teeth that allow omnivorous feeding on bacteria, fungi, and even other nematodes.

 

Predatory feeding by P. pacificus

 

In response to starvation and, as sensed by pheromones, crowding and competition (Bose et al., 2012), Pristionchus nematodes develop into adults of one of two distinct feeding morphs ("eurystomatous" and "stenostomatous"). The stenostomatous morph grows rapidly on a diet of bacteria, whereas the eurystomatous morph, which is more complex in form, has higher fitness than the stenostomatous morph when fed nematode prey (Serobyan et al., 2014).

 

Ppa-dimorphism

Mouth polyphenism in P. pacificus

 

The ability to make major phenotypic differences from a single genotype, as in P. pacificus, may act as a facilitator of novelty and diversity (Susoy et al., 2015). Research in the lab tests this principle at a genetic level by investigating directly the genes that regulate developmental plasticity and their significance in the signatures of evolution. Making this research practical is the sophisticated analytical toolkit available for P. pacificus, a self-fertilizing species with a short (four-day) generation time. Because teeth are what allow nematodes to be predators, the interplay of genetic plasticity mechanisms with ecoogy can be studied directly in this system.

A few ultimate goals of our research include:
1. A genetic understanding of the regulation of developmental plasticity;
2. To know how regulators of plasticity diverge to produce new phenotypes;
3. To use a polyphenism as an inroad to discover the genes that build morphological novelties.

The genetic basis for developmental dimorphism has recently become accessible, especially through the use of P. pacificus as a model (Projecto-Garcia et al., 2017). As a proof of principle, a switch gene – which encodes the sulfatase EUD-1 – was found to execute a developmental switch for the mouth dimorphism (Ragsdale et al., 2013). This switch regulator is a novel gene, the result of specialization following serial gene duplications in Pristionchus (Ragsdale & Ivers, 2016).

 

Neuronal expression of a switch gene eud-1 for a morphological dimorphism

Neuronal expression of eud-1 indicates the initiation sites of a polyphenism switch

 

Building on this understanding, we are now (i) unraveling the genetic pathway making up this polyphenism switch and (ii) determining the evolutionary origins of its mechanism. We are doing this by forward genetics, which allows the unbiased identification of the causal genes. Consequently, we have isolated the factors forming a switch together with EUD-1, which evidence suggests to be a doage-dependent entry point into a novel neuroendrocrine signaling module. One of the factors we have uncovered is a nuclear hormone receptor (NHR-40), which was found to carry out the polyphenism decision downstream of EUD-1 and possibly at the transcriptional terminal of the switch (Kieninger et al., 2016). More recently, we discovered that the polyphenism switch hinges on the activity of another lineage-specific gene, which encodes the sulfotransferase SEUD-1, is environmentally influenced and expressed in polyphenic tissue. The discovery of this gene has giveninsight into how the genetic basis for how plasticity responses evolves: in Pristionchus, the balance of transcriptional or genomic dosage between SEUD-1 and EUD-1 has changed to create divergent polyphenism thresholds (Bui et al., 2018). As we reconstruct the genetic architecture of the switch, we are taking a comparative functional approach to learn how such a switch has been built and changed to produce divergent developmental responses to the environment.

 

Neuronal expression of a switch gene eud-1 for a morphological dimorphism

seud-1 expression in cells that produce dimorphic mouthparts in P. pacificus

 

With the ability to study the genes that transduce environmental signals to novel structures, mechanistic advances can be extended to the study of macroevolution. To link these advances to regulatory and, ultimately, morphological divergence, mechanisms are being tested in other nematodes. Allowing comparisons is a robust phylogenetic infrastructure that now includes over 40 species of Pristionchus and close relatives that have been recently discovered, described, morphologically characterized, and in many cases brought into laboratory culture (Ragsdale et al., 2015). Moreover, the novel feeding morphologies that characterize Diplogastridae (the family including Pristionchus) are being empirically placed into an increasingly rich ecological context (Ledón-Rettig et al., 2018). In a particularly striking example, polyphenism in one clade of Pristionchus species, discovered from within African and Australasian figs, has diverged so far as to control as up to five adult morphs, each putatively with its own ecological function (Susoy et al., 2016). Given the richness of plastic responses, associated morphologies, and ecological function in Pristionchus and other Diplogastridae, comparative analyses of the polyphenism can reveal the genetic parameters for relationships among environment, development, and form.

 

Correlation of polyphenism with mouthpart complexity and diversity in macroevolution

 

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