How can a small animal provide new tools for speciation genetics?

One diverse group of organisms little studied in the speciation field are nematodes, some of which are amenable to advanced genetics. We established Pristionchus nematodes as a new model of speciation genetics. The study provided a new insight into a role of chromosome evolution in speciation.
How can a small animal provide new tools for speciation genetics?

A single, small roundworm got stuck to the surface of the body of a stag beetle. Harmlessly and silently, the worm waited for the death of the insect host. This 'necromeric' association is a strategy for small bacterial feeding nematodes to get access to a rich bacterial environment on the insect carcass. The worm was in the arrested ‘dauer’ stage, a stage that does not feed but is long lived. Worms leave the dauer stage when surrounded by food and rapidly grow to adulthood to mate and reproduce while still being on the insect carcass. This prosperity was microscopically observed by a researcher that captured the stag beetle and put on a plate with E. coli in hope to find new species of Pristionchus nematodes. Over years this resulted in a collection of frozen nematode stocks of different Pristionchus species. Following investigation of the genetic relationship, the researcher crossed related species from the frozen stock to test their reproductive barriers.

This is just one picture of our world-wide hunting for new Pristionchus species, resulting in around 50 species in the genus Prisionchus in the last two decades. Pristionchus nematodes are soil nematodes frequently associated with different scarab beetles. They have short generation times, small genome sizes, can easily be cultured in small petri-dishes, frozen as live material, and genetically-modified by forward and reverse genetics (Sommer, 2015). Using these experimental advantages, one androdioecious species, Pristionchus pacificus has been studied as a model system for comparative biology with C. elegans. Phenotypic plasticity of its mouth morphology, predation of other nematodes and self-recognition related to nematode predation made P. pacificus an important model system in evolution and ecology (Lightfoot et al., 2019; Sieriebriennikov et al., 2020). The sampling efforts of Pristionchus nematodes also opened another research avenue for this nematode, speciation genetics.

Pristionchus sampling
Sampling of beetles, with which Pristionchus nematodes are associated, by light catch

Speciation and its associated mechanisms were classically well studied using model animals and plants but their empirical knowledge is still largely updated. Especially recent developments in speciation genomics highlighted the importance of inversions, which reduces recombination and facilitates evolution of hybrid incompatibility (reviewed in Wellenreuther and Bernatchez, 2018). However, one group of organisms that has been little studied with regard to reproductive isolation are nematodes. This is unfortunate as nematodes are the most abundant and diverse group of animals on this planet. However, given their small size and cryptic species, research on speciation and reproductive isolation is sparse in nematodes.    

Given our sampling strategy and efforts in the last decades, we found six dioecious species that produce F1 viable hybrids with the model P. pacificus, and thus, they represent some of the most closely-related nematode species described today (Yoshida et al., 2018). Estimates based on synonymous substitution rates in fully sequenced genomes indicate that the most closely related species pair, P. pacificus vs. P. exspectatus, has diverged 12-28 million generations ago.

Summary of the paper

Chromosome fusions that contribute to reproductive isolation between two Pristionchus species

Using their experimental advantages, in the present paper, we comprehensively studied the reproductive isolation and its genetic mechanisms including the new genome sequencing of the most closely related Pristionchus species and found multiple chromosome fusions between the species, having a role in speciation. Specifically, a chromosome-level genome assembly of P. exspectatus using single-molecule and Hi-C sequencing revealed a chromosome-wide rearrangement relative to P. pacificus. Unexpectedly, whole-genome characterization and cytogenetic studies of the outgroup species Pristionchus occultus indicated two independent fusions involving the same chromosome in P. pacificus and P. exspectatus, respectively. Surprisingly, genetic linkage analysis indicated that these fusions altered the chromosome-wide pattern of recombination, resulting in large low-recombination regions that likely facilitated the coevolution of round 15% of the genes across the entire genomes. Next, QTL analyses for hybrid sterility revealed that major QTLs mapped to the area of the fused chromosomes. Subsequent analysis indicates that abnormal hybrid meiosis that caused aneuploidy and hybrid-specific recombination in the fused chromosomes explained the hybrid sterility. Therefore, our study indicated that recent chromosome fusions repatterned the recombination rate and drove reproductive isolation during Pristionchus speciation. Thus, besides the well-known inversions, we have documented a key role of chromosome fusions for reproductive isolation and nematode speciation.

Lightfoot, James W., et al. "Small peptide–mediated self-recognition prevents cannibalism in predatory nematodes." Science 364.6435 (2019): 86-89.

Sieriebriennikov, Bogdan, et al. "Conserved nuclear hormone receptors controlling a novel plastic trait target fast-evolving genes expressed in a single cell." PLoS genetics 16.4 (2020): e1008687.

Sommer, Ralf J. Pristionchus pacificus: a nematode model for comparative and evolutionary biology. Brill, 2015.

Wellenreuther, Maren, and Louis Bernatchez. "Eco-evolutionary genomics of chromosomal inversions." Trends in ecology & evolution 33.6 (2018): 427-440.

Yoshida, Kohta, et al. "Two New Species of (Nematoda: Diplogastridae) from Taiwan and the Definition of the Species-Complex Sensu Stricto." Journal of Nematology 50.3 (2018): 355-368.

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