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The diversity of animal form is astonishing 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 – that is, by 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 (Bose et al., 2012), Pristionchus nematodes develop into adults of one of two distinct feeding morphs ("eurystomatous" and "stenostomatous"). These nematodes thus show polyphenism, or discrete developmental plasticity. In this polyphenism, 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

Mouthpart polyphenism in P. pacificus

 

The ability to make major phenotypic differences from a single genotype, as shown by 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 for downstream molecular 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 ecology with genetic mechanisms for plasticity can be studied directly in this system.

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

The genetic basis for developmental polyphenism has been accessed 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 (eurystomatous-form-defective) – was found to execute a switch for the mouth dimorphism (Ragsdale et al., 2013). This factor is a gene that has functionally specialized following a series of gene duplications (Ragsdale & Ivers, 2016).

 

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

Expression of eud-1 in neurons channeling a polyphenism switch

 

We are now unraveling the genetic architecture of this polyphenism switch, and we are resonctructing the evolutionary origins of its mechanism. Using forward genetics, we have taken an unbiased approach to identify the causal genes, thereby isolating the factors forming a switch together with EUD-1. One of these factors is NHR-40, a nuclear receptor acting downstream of eud-1 to control the switch (Kieninger et al., 2016). The switch also hinges on another lineage-specific gene, which encodes the sulfotransferase SEUD-1 (suppressor-of-eud-1) and whose expression is both environmentally influenced and localized to polyphenic tissue (Bui et al., 2018). The discovery of SEUD-1 has given insight into how the genetic basis for plasticity evolves: in Pristionchus, the balance of transcriptional and genomic dosage between SEUD-1 and EUD-1 has changed to create divergent polyphenism thresholds. Consequently, how morph-specific target genes ("environmentally sensitive loci") are expressed, and thereby how often they are exposed to selection, changes through the influence of a regulatory switch. Using genetic manipulations in this system, we have identified these targets, whose expression indeed underlies phenotypic variation in the polyphenism (Bui & Ragsdale, 2019). Through a comparative functional approach, we are revealing how a plasticity switch has arisen and changed to produce divergent 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

 

To expand the macroevolutionary context of plasticity regulation and its consequences, we also study plasticity mechanisms in other nematodes. Allowing comparisons is a deep source of morphological and life-history variation for dozens of species of Pristionchus and close relatives that can be kept in 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, associated with fig wasps in Afrotropical and Australasian figs, has diverged to include five morphs, each with its own putative ecological function (Susoy et al., 2016). Given the diversity of plastic responses, associated morphologies, and ecological function in Diplogastridae, comparisons in this system can reveal the genetic parameters for the relationship between environment and form.

 

Correlation of polyphenism with mouthpart complexity and diversity in macroevolution

 

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