A recent and rapid genome expansion driven by the amplification of transposable elements in the Neotropical annual killifish Garcialebias charrua

Neotropical annual killifish survive in seasonal ponds due to their ability to undergo embryonic diapauses in the dry season and grow, reproduce and die in the span of a few months during the rainy season. The Austrolebias genus group is endemic to the South American basins and shows remarkable speciation and genetic plasticity. Within this fish group Garcialebias charrua is sympatric with another annual killifish, Cynopoecilus melanotaenia, belonging to a tribe that diverged about 25 million years ago. Despite being closely related species within the Rivulidae family, both species show important differences in genome size. Here, we explore the genomic structure of these species to understand their evolution and unique adaptations. We have sequenced the genomes of G. charrua and C. melanotaenia and determined that they show important structural differences between them. While C. melaotaenia has a genome size of around 1 Gb, similar to that of most characterized teleosts, G. charrua has undergone an evolutionarily recent and massive genome expansion, with a size three times larger (3 Gb). The expansion of the genome in G. charrua has occurred due to amplification of repetitive elements, most recently from the LINE class of elements. We explore and characterize in detail the contribution to genome expansion of repetitive elements at the level of superfamilies, as well as analyze the relationship between these elements and coding genes in G. charrua. We also examine the selection pressures on gene sequences and identify functions that are under positive or purifying selection, and compare these data with that derived from other species. Our study adds a crucial element to the understanding of annual fish evolution and life history. We show that the genetic variability and plasticity in G. charrua is accompanied by a recent genome-wide expansion with an important contribution of repetitive elements. By comparing these findings with data from other species, we show that G. charrua has undergone bursts of repetitive element expansion, with specific superfamilies of retrotransposons and DNA transposons being the most prevalent and recent. In addition, we characterize genes that are potentially implicated in adaptive traits because of their interaction with mobile elements or because they display evidence of intensified selection. These genes are candidates for functional studies aimed at unraveling the genetic basis of annualism.