How Did Evolution Halve Genome Size During an Oceanic Island Colonization?

Abstract

Red devil spiders of the genus Dysdera colonized the Canary Islands and underwent an extraordinary diversification. Notably, their genomes are nearly half the size of their mainland counterparts (∼1.7 vs. ∼3.3 Gb). This offers a unique model to solve long-standing debates regarding the roles of adaptive and nonadaptive forces on shaping genome size evolution. To address these, we conducted comprehensive genomic analyses based on three high-quality chromosome-level assemblies, including two newly generated ones. We find that insular species experienced a reduction in genome size, affecting all genomic elements, including intronic and intergenic regions, with transposable element (TE) loss accounting for most of this contraction. Additionally, autosomes experienced a disproportionate reduction compared to the X chromosome. Paradoxically, island species exhibit higher levels of nucleotide diversity and recombination, lower TE activity in recent times, and evidence of intensified natural selection, collectively pointing to larger long-term effective population sizes in species from the Canary Islands. Overall, our findings align with the nonadaptive mutational hazard hypothesis, supporting purifying selection against slightly deleterious DNA and TE insertions as the primary mechanism driving genome size reduction.