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The Oikopleura dioica, a small organism found in marine plankton, has been a model animal in genetic and evolutionary studies for years. It is a tiny animal, with a short and rapid life cycle, very prolific, with a fully sequenced genome and easy to maintain in the laboratory. It is a benchmark in the study of gene loss as an evolutionary driver, genomic analyses and embryonic development in our phylum (the chordates). Now, an article published in the journal Genome Research questions the previous knowledge of this model species and opens up new questions about speciation and the location of genes in the genome.
The study is led by the experts Cristian Cañestro, from the Genetics Section at the Faculty of Biology and the Biodiversity Research Institute (IRBio) of the University of Barcelona, and Charles Plessy, from the Genomics and Regulatory Systems Unit at the Okinawa Institute of Science and Technology (OIST) in Japan, with the participation of teams from the University of Osaka, among other institutions.
The genomic tower of Babel
Although the genome of Oikopleura dioica was completely sequenced (Science, 2010), the new study reveals confusing aspects of the genomic structure of the species. Specifically, the team analyzed the genome in three lineages of Oikopleura dioica, from the Seto Inland Sea and the Okinawa Islands (Japan), the Mediterranean and the Pacific Ocean. The findings show that the morphological, ecological and behavioural characteristics of the lineages are almost identical, but the genomes differ greatly in the distribution of genes on the chromosomes, suggesting that they are cryptic species. Cryptic species are animal populations that are morphologically very similar and may have passed through a single species, but which belong to different species and are therefore not fertile with each other.
The comparison of the genetic sequences of the three cryptic species lineages led to the conclusion that they shared a common ancestor about 25 million years ago. The genetic lineages of the organisms analysed in Barcelona and Osaka appear to be more closely related than that of Okinawa, which diverged about seven million years ago. For comparison, humans diverged from mice about 75-90 million years ago.
Cristian Cañestro, professor at the UB’s Department of Genetics, says that “this study challenges the concept of a reference genome for some species, and highlights the need to sequence animals from different parts of the world, since, although in some cases they look like the same species, some could be different cryptic species”.
Evolution at breakneck speed
“Oikopleura is opening up new avenues into genomic research”, says Plessy, from OIST’s Genomics and Regulatory Systems Unit and co-author of the paper. “As a model animal, it allows us to study the mechanisms for genome changes in the lab as they happen at a very large scale and speed, which is an enormous opportunity”. The rate of genomic rearrangements is a quantifiable measure of the speed at which species evolve. In the case of Oikopleura dioica, it is more than ten times faster than in comparable species. As Michael J. Mansfield (OIST) notes, “the Oikopleura is one of the fastest evolving animals in the world. Animals, especially chordates, don’t normally rearrange their genomes to this extent, at this speed”. The new genome-wide perspective among Oikopleura dioica lineages leads us to a puzzling question: how have they been able to retain such similar characteristics among themselves? “We went into this study thinking that all Oikopleura dioica were the same, but we have shown the opposite. How often is this also true for other species? How much more do we need to know about the mechanisms of genome coding?” says Plessy. “Our results suggest that while genomic organization is important, especially for something as complex as human beings, we should not forget the individual genes.”
“We have used the expression genome scrambling because it is an expression that really reflects the low degree of conservation of the order of genes along the genome, an unheard-of fact when we compare other species that are so similar to each other,” says Cañestro.
A leading team in evolutionary developmental biology
The Evo-Devo-Genomics group at the UB is one of the few scientific teams in the world studying Oikopleura dioica from the perspective of evolutionary developmental biology (EVO-DEVO). It is also the only group in Spain that has promoted a scientific infrastructure – there are three more, in Bergen (Norway) and in Osaka and Okinawa (Japan) – with the capacity to develop and study this new model organism, considered a benchmark of international outreach.
Alfonso Ferrández, a postdoctoral researcher in the Evo-Devo-Genomics group, remarks that it is incredible “that such morphologically similar animals can have such different genomes”. Experts Marc Fabregà and Gaspar Sánchez, doctoral students in the Evo-Devo-Genomics group, note that “it is also surprising that the genes studied in the study were all in different regions of the genomes of all the cryptic species that have been analysed”.
For the team, this paper is the culmination of a long process of cultivating different lineages of Oikopleura dioica and developing bioinformatics tools capable of analysing their chaotic genomes. “We want to use Oikopleura to learn more about the nature of genomic rearrangements, how they affect gene regulation, while studying whether they may be linked to the high rate of gene loss in these fascinating organisms”, the experts conclude.
Reference article:
Plessy, Charles; Mansfield, Michael J.; Bliznina, Aleksandra, et al. “Extreme genome scrambling in marine planktonic Oikopleura dioica cryptic species”. Genome Research, April 2024. DOI: 10.1101/gr.278295.123
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