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 bring this diversity into the realm of evolutionary developmental biology (evo-devo).

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 model system and central reference point 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 undergo an irreversible decision in larval development to assume 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 morphologically more complex, has higher fitness than the former morph when fed on nematode prey (Serobyan et al., 2014).



Mouth polyphenism in P. pacificus


The ability to exhibit 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 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 enable predation in nematodes, the interplay of ecology and genetic plasticity mechanisms 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 is expressed in polyphenic tissue (Bui et al., 2018). Following this discovery, we have identified a genetic basis for how plasticity responses evolve: specifically, the balance of transcriptional or genomic dosage between SEUD-1 and EUD-1 can change to create divergent polyphenism thresholds. As we continue to reconstruct the genetic architecture of the switch, we are taking a comparative functional approach to learn how such a switch has been built or 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 plasticity and specify 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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