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 interactions among development, ecology, and population genetics – particularly through developmental plasticity – drive 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, 2016). 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 using P. pacificus as a model. As a proof of principle, a switch gene 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). 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, as part of a grant by the National Science Foundation. 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 the sulfatase EUD-1, which evidence suggests to be a doage-dependent entry point into a novel neuroendrocrine signaling module. One of the factors we uncovered is a nuclear hormone receptor (NHR-40), which was found to carry out the polyphenism decision downstream of EUD-1 (Kieninger et al., 2016), likely as a threshold response to the amount of sulfatase-unmodified signal. 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 or changed to produce divergent developmental responses to the environment.


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


Given 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 includes some 30 species of Pristionchus and close relatives that have been recently discovered, described, and morphologically characterized (see publications page for more). Nearly all of these species have been brought into laboratory culture, making experiments in genetics and development feasible. Comparative analyses of dimorphism and teeth development will therefore be expanded with the ultimate aim of uncovering and tying together the mechanistic bases of micro- and macroevolution.


Correlation of polyphenism with mouthpart complexity and diversity in macroevolution


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