Scientists stunned as island spider loses half its genome

Published in Molecular Biology and Evolution, the research marks the first time scientists have observed an animal species reducing its genome by almost 50% during the process of colonizing oceanic islands.

Challenging Long-Held Evolutionary Assumptions

Traditionally, scientists have believed that species colonizing islands tend to develop larger genomes with more repetitive DNA. This new discovery turns that idea on its head and deepens the debate over one of biology's central mysteries: how and why genome size changes during the evolution of life.

The research was led by Julio Rozas and Sara Guirao from the Faculty of Biology and the Biodiversity Research Institute (IRBio) at the University of Barcelona. The study's first author, Vadim Pisarenco (UB-IRBio), worked with collaborators from the University of La Laguna, the Spanish National Research Council (CSIC), and the University of Neuchâtel in Switzerland.

Scientists have long known that genome size -- the total number of DNA base pairs containing an organism's genetic instructions -- can vary widely between species, even among those with similar complexity. This new study provides a striking example of that phenomenon and suggests that evolution can move in unexpected directions.

An Evolutionary Puzzle in the Canary Islands

Spiders of the genus Dysdera have undergone remarkable diversification in the Canary Islands, a region often described as a natural laboratory for studying evolution in isolation. Nearly 50 endemic Dysdera species, about 14% of all known species in the genus, have evolved there since the islands emerged a few million years ago.

Using advanced DNA sequencing tools, researchers compared two closely related species: Dysdera catalonica, which inhabits parts of Catalonia and southern France, and D. tilosensis, native 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), which is almost double that of the species D. tilosensis (1.7 Gb). Interestingly, despite having a smaller genome, the species from the Canary Islands shows greater genetic diversity," explains Professor Julio Rozas, director of the Evolutionary Genomics and Bioinformatics research group at the University of Barcelona and a board member of the Bioinformatics Barcelona (BIB) platform.

A Rare Case of Genome Downsizing

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

"The genome downsizing of the spider D. tilosensis, associated with the colonization process of the Canary Island, is one of the first documented cases of drastic genome downsizing using high-quality reference genomes," says Professor Julio Rozas, director of the Evolutionary Genomics and Bioinformatics research group.

"This phenomenon is now being described for the first time in detail for phylogenetically closely related animal species," he continues.

Searching for the Causes of Genome Reduction

In such evolutionarily similar species, which share similar habitats and diet, "differences in genome size cannot easily be attributed to ecological or behavioural factors," says Professor Sara Guirao. "Phylogenetic analysis -- Guirao continues -- combined with flow cytometry measurements, reveals that the common ancestor had a large genome (about 3 Gb). This indicates that the drastic genome reduction occurred during or after the arrival on the islands."

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

Secondly, the findings contradict theories that argue that, on islands, the founder effect -- the process of colonization by a small number of individuals -- leads to a reduction in selective pressure and, as a result, genomes should be larger and richer in repetitive elements.

"In the study, we observed the opposite: island species have smaller, more compact genomes with greater genetic diversity," says doctoral student Vadim Pisarenco. This pattern suggests the presence of non-adaptive mechanisms, "whereby populations in 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, as a consequence, eliminate unnecessary DNA," says Pisarenco.

Shedding Light on Evolution's Genomic Mysteries

It remains unclear why some species accumulate large amounts of repetitive DNA while others evolve streamlined genomes. The findings could help explain this long-standing enigma in evolutionary biology.

Some scientists propose that genome size changes reflect direct adaptation to the environment. Others argue that these changes result from a balance between the accumulation of repetitive elements (such as transposons) and their removal through natural selection.

"This study supports the idea that, rather than direct adaptation, genome size in these species depends primarily on a balance between the accumulation and removal of this repetitive DNA," the researchers conclude.