Island spider loses half of its genome, defying evolutionary expectations

In a few million years, the spider Dysdera tilosensis, a species endemic to the Canary Islands, halved the size of its genome during the process of colonization and adaptation to its natural habitat. In addition to being smaller, this genome is more compact and contains more genetic diversity than that of other similar continental spiders.

The discovery, published in the journal Molecular biology and evolutionreveals for the first time how an animal species managed to shrink its genome by almost half during the colonization of oceanic islands.

This study contradicts the more traditional evolutionary view – on island-colonizing species, whose genomes are larger and often contain more repetitive elements – and broadens the scientific debate on a major enigma of evolutionary biology: how and why does genome size change during the evolution of living beings?

The study is led by Julio Rozas and Sara Guirao, experts from the Faculty of Biology and the Biodiversity Research Institute (IRBio) of the University of Barcelona. The article, whose first author is Vadim Pisarenco (UB-IRBio), also involves teams from the University of La Laguna, the Spanish National Research Council (CSIC) and the University of Neuchâtel (Switzerland).

This research offers a surprising perspective for explaining a phenomenon that has intrigued scientists for decades: genome size – the total number of DNA base pairs encoding an organism’s genetic information – varies enormously between species, even those with similar biological complexity.

A smaller genome in an island species: an evolutionary paradox?

Spiders of the genus Dysdera have diversified dramatically in the habitats of the Canary Islands. This archipelago is considered a true natural laboratory for analyzing the evolution of species and their genomes in a context of geographic isolation. Nearly 50 endemic species, or 14% of all species of this genus described in the world, have emerged since the formation of the islands a few million years ago.

Applying advanced DNA sequencing technologies, the team analyzed the genomes of two closely related spider species: Dysdera catalonica, a continental species found in the northern half of Catalonia and southern France, and D. tilosensis, endemic to the island of Gran Canaria.

“The species D. catalonica has a genome of 3.3 billion base pairs (3.3 GB, the letters of DNA), almost double that of the species D. tilosensis (1.7 GB). It is interesting to note that, despite a smaller genome, the Canary Islands species has greater genetic diversity,” explains Rozas, professor at the Department of Genetics, Microbiology and Statistics of the UB, director of the Department of Evolutionary Genomics and Bioinformatics Research Group and member of the board of directors of the Bioinformatics Barcelona (BIB) platform.

Genomic sequencing also reveals that D. catalonica has a haploid chromosome number of four autosomes and one X sex chromosome, while D. tilosensis has six autosomes plus the X chromosome.

“The genome reduction of the spider D. tilosensis, associated with the colonization process of the Canary Islands, is one of the first documented cases of drastic genome reduction using high-quality reference genomes,” explains Rozas.

“This phenomenon is now described for the first time in detail for phylogenetically close animal species,” he continues.

How to explain the reduction of the genome?

In these evolutionarily similar species, which share similar habitats and diet, “differences in genome size cannot be easily attributed to ecological or behavioral factors,” says Professor Guirao. “Phylogenetic analysis combined with flow cytometry measurements reveals that the common ancestor had a large genome (approximately 3 GB). This indicates that drastic genome reduction occurred during or after arrival on the islands.”

This result is clearly paradoxical for two reasons. On the one hand, although less common in animals, the most common pattern is increases in genome size via whole-genome duplications, “particularly in plants, where the appearance of polyploid species (with multiple chromosome endowments) is common. In contrast, such abrupt reductions in genome size over a relatively short period of time are much rarer,” explains Guirao.

Second, the results contradict theories that, on islands, the founder effect – the process of colonization by small numbers of individuals – leads to a reduction in selective pressure and, therefore, genomes should be larger and richer in repetitive elements.

“In the study, we observed the opposite: island species have smaller and more compact genomes with greater genetic diversity,” explains doctoral student Pisarenco. This pattern suggests the presence of non-adaptive mechanisms, “by which the populations of the Canary Islands would have remained relatively numerous and stable for a long time. This would have made it possible to maintain a strong selective pressure and, therefore, to eliminate unnecessary DNA”, explains Pisarenco.

Deciphering one of the great enigmas of evolutionary biology

It is still unclear why, in similar species, some genomes accumulate many repetitive DNA sequences while others are more compact. The study could offer a new perspective on resolving this open question in evolutionary biology.

According to some hypotheses, these changes in the genome have a direct adaptive value. Other explanations propose non-adaptive mechanisms, in which genome size is the result of a balance between the accumulation of repetitive elements (such as transposons) and their elimination by purifying selection.

“This study supports the idea that, rather than a direct adaptation, the genome size of these species depends mainly on a balance between the accumulation and elimination of this repetitive DNA,” the researchers conclude.