A comparative genome study of earthworms and their marine relatives led by the IBE with participation of the UAB shows that marine worms shattered their genome and rebuilt it in a radically different form when they first emerged from the sea 200 million years ago. The study, published in Nature Ecology and Evolution, could challenge Darwin's theory of evolution by showing that worms colonisedland in evolutionary jumps.
In 1859, Darwin imagined evolution as a slow, gradual progress, with species accumulating small changes over time. But even he was surprised to find the fossil record offered no missing links: the intermediate forms which should have told this story step by step. In 1972, the scarcity of intermediate forms led the palaeontologists Stephen Jay Gould and Niles Eldredge to propose the idea of the punctuated equilibrium. According to this theory, rather than changing slowly, species remain stable for millions of years and then suddenly make rapid, radical evolutionary jumps. These large changes would happen suddenly and in small, isolated populations, well off the palaeontological radar. Although some fossils support this pattern, the scientific community remains divided: is this a rule of evolution, or an eye-catching exception?
Now a study points for the first time to a mechanism of rapid, massive genomic reorganisation which could have played a part in the transition of marine to land animals 200 million years ago. The research was led by the Institute of Evolutionary Biology (IBE), a mixed research centre belonging to the Spanish National Research Council (CSIC) and Pompeu Fabra University (UPF), and was carried out by the research group led by Aurora Ruiz-Herrera, researcher at the Institute of Biotechnology and Biomedicine (IBB-UAB), full professor at the Department of Cell Biology, Physiology and Immunology, and ICREA Academy.
The research team has shown that marine annelids (worms) reorganised their genome from top to bottom, leaving it unrecognisable, when they left the oceans. Their observations are consistent with a punctuated equilibrium model, and could indicate that not only gradual but sudden changes in the genome could have occurred as these animals adapted to terrestrial settings. The genetic mechanism identified could transform our concept of animal evolution and revolutionise the established laws of genome evolution.
The team sequenced for the first time the high-quality genome of various earthworms, and compared to them to other closely related annelid species (leeches and bristle worms or polychaetes). Until now, the lack of complete genomes had prevented the study of chromosomal-level patterns and characteristics for many species, limiting research to smaller-scale phenomena – population studies of a handful of genes, rather than macroevolutionary changes at the full-genome level.
After putting together each of the genomic jigsaw puzzles, the team was able to travel back in time with great precision more than 200 million years, to when the ancestors of the sequenced species were alive. «This is an essential episode in the evolution of life on our planet, given that many species, such as worms and vertebrates, which had been living in the ocean, now ventured onto land for the first time,» comments Rosa Fernández, lead researcher of the IBE's Metazoa Phylogenomics and Genome Evolution Lab.
The analysis of these genomes has revealed an unexpected result: the annelids' genomes were not transformed gradually, as Neo-Darwinian theory would predict, but in isolated explosions of deep genetic remodelling. «The enormous reorganisation of the genomes we observed in the worms as they moved from the ocean to land cannot be explained with the parsimonious mechanism Darwin proposed; our observations chime much more with Gould and Eldredge's theory of punctuated equilibrium,» Fernández adds.
A radical genetic mechanism which could provide evolutionary responses
The international team of scientists has discovered that certain marine worms shattered their genome into thousands of fragments—only to reassemble it and continue evolving on land. This phenomenon challenges current models of genome evolution, which show that in most species—from sponges and corals to mammals—genomic structures remain remarkably conserved over time. «The entire genome of these marine worms was broken down and then reorganized in a completely random way, in a very short period on the evolutionary scale,» explains lead researcher Fernández. «I had my team repeat the analysis over and over because I simply couldn't believe it.»
One of the keys to understanding why this drastic genomic upheaval didn't lead to extinction may lie in the three-dimensional (3D) structure of the genome. In this regard, the group led by Aurora Ruiz-Herrera contributed with their expertise in 3D genome architecture. The work revealed that the chromosomes of these modern worms are significantly more flexible than those of vertebrates and other model organisms.
«The 3D organization of the genome provides a structural framework that allows genes to remain functionally connected, even when their linear order is dramatically altered,» says Aurora Ruiz-Herrera. «This plasticity could be what made such extreme genome reconfiguration compatible with survival and adaptation.» Thanks to this flexibility, genes located in different parts of the genome may have been able to shift positions while still functioning together. This ability could have been essential in allowing major DNA rearrangements without compromising the organism's viability.
The researchers suggest that these genetic transformations may have helped the worms adapt rapidly to terrestrial life, reorganizing their genes to better respond to new challenges such as breathing air or exposure to sunlight. The study also proposes that these adjustments not only relocated genes but also fused previously separated fragments, creating new 'genetic chimeras' that may have fueled their evolution. «You could think this kind of genomic chaos would doom a species, but it's possible that some lineages owe their evolutionary success to exactly this kind of superpower,» Fernández concludes.
The observations in the study are consistent with a punctuated equilibrium model, where we observe an explosion of genomic changes after a long period of stability. However, the lack of experimental data for or against - in this case, 200-million-year-old fossils - makes it difficult to validate this theory.
Chromosomal chaos: problem or solution?
It seems from this study that conserving the genomic structure at the linear level - i.e., where the genes are more or less in the same place in different species - may not be as essential as had been thought. «In fact, stability could be the exception and not the rule in animals, which could benefit from a more fluid genome,» Fernández says.
This phenomenon of extreme genetic reorganisation had previously been observed in the progression of cancer in humans. The term chromoanagenesis covers several mechanisms which break down and reorganise chromosomes in cancerous cells, where we see similar changes to those observed in the earthworms. The only difference is that while these genomic breakdowns and reorganisations are tolerated by the worms, in humans they lead to diseases. The results of this study open the door to a better understanding of the potency of this radical genomic mechanism, with implications for human health.
The study has also reawakened one of the liveliest scientific debates of our time. «Both visions, Darwin's and Gould's, are compatible and complementary. While Neo-Darwinism can explain the evolution of populations perfectly, it has not yet been able to explain some exceptional and crucial episodes in the history of life on Earth, such as the initial explosion of animal life in the oceans over 500 million years ago, or the transition from the sea to land 200 million years ago in the case of earthworms,» Fernández notes. «This is where the punctuated equilibrium theory could offer some answers.»
In the future, a larger investigation of the genomic architecture of less-studied invertebrates could shed light on the genomic mechanisms shaping the evolution of the species. «There is a great diversity we know nothing about, hidden in the invertebrates, and studying them could bring new discoveries about the diversity and plasticity of genomic organisation, and challenge dogmas on how we think genomes are organised,» Fernández concludes.
The study involved the collaboration of research staff from the Universitat Autònoma de Barcelona, Trinity College, the Universidad Complutense de Madrid, the University of Köln, and the Université Libre de Bruxelles.
The study received support from SEA2LAND (Starting Grant funded by the European Research Council), and from the Catalan Biogenome Project, which funded the sequencing of one of the worm genomes.
Reference article: Vargas-Chávez, C., Benítez-Álvarez, L., Martínez-Redondo, G. I., Álvarez-González, L., Salces-Ortiz, J., Eleftheriadi, K., Escudero, N., Guiglielmoni, N., Flot, J.-F., Novo, M., Ruiz-Herrera, A., McLysaght, A., & Fernández, R. (2025). «A punctuated burst of massive genomic rearrangements by chromosome shattering and the origin of non-marine annelids». Nature Ecology and Evolution. DOI 10.1038/s41559-025-02728-1
