Multiple and diversified transposon lineages contribute to early and recent bivalve genome evolution

Abstract

Background Transposable elements (TEs) can represent one of the major sources of genomic variation across eukaryotes, providing novel raw materials for species diversification and innovation. While considerable effort has been made to study their evolutionary dynamics across multiple animal clades, molluscs represent a substantially understudied phylum. Here, we take advantage of the recent increase in mollusc genomic resources and adopt an automated TE annotation pipeline combined with a phylogenetic tree-based classification, as well as extensive manual curation efforts, to characterize TE repertories across 27 bivalve genomes with a particular emphasis on DDE/D class II elements, long interspersed nuclear elements (LINEs), and their evolutionary dynamics. Results We found class I elements as highly dominant in bivalve genomes, with LINE elements, despite less represented in terms of copy number per genome, being the most common retroposon group covering up to 10% of their genome. We mined 86,488 reverse transcriptases (RVT) containing LINE coming from 12 clades distributed across all known superfamilies and 14,275 class II DDE/D-containing transposons coming from 16 distinct superfamilies. We uncovered a previously underestimated rich and diverse bivalve ancestral transposon complement that could be traced back to their most recent common ancestor that lived ~ 500 Mya. Moreover, we identified multiple instances of lineage-specific emergence and loss of different LINEs and DDE/D lineages with the interesting cases of CR1- Zenon, Proto2, RTE-X, and Academ elements that underwent a bivalve-specific amplification likely associated with their diversification. Finally, we found that this LINE diversity is maintained in extant species by an equally diverse set of long-living and potentially active elements, as suggested by their evolutionary history and transcription profiles in both male and female gonads. Conclusions We found that bivalves host an exceptional diversity of transposons compared to other molluscs. Their LINE complement could mainly follow a “stealth drivers” model of evolution where multiple and diversified families are able to survive and co-exist for a long period of time in the host genome, potentially shaping both recent and early phases of bivalve genome evolution and diversification. Overall, we provide not only the first comparative study of TE evolutionary dynamics in a large but understudied phylum such as Mollusca, but also a reference library for ORF-containing class II DDE/D and LINE elements, which represents an important genomic resource for their identification and characterization in novel genomes.

Effective population size does not explain long-term variation in genome size and transposable element content in animals

“…Genome size and TE content have already been reported as tightly linked in eukaryotes (Elliott and Gregory 2015; Kidwell 2002), arthropods (Sproul et al 2023; Wu and Lu 2019) and vertebrates (Chalopin et al 2015). Our results are consistent with this perspective across all the animal species analysed, as well as at the level of ray-finned fishes (Reinar et al 2023), insects (Heckenhauer et al 2022; Mérel et al 2024; Petersen et al 2019; Sessegolo et al 2016), mammals (Osmanski et al 2023), and molluscs (Martelossi et al 2023), strongly indicating TEs as major drivers of genome size variation in metazoans. It should be noted however that we mainly focused on some vertebrate groups and insects, while leaving out many animal taxa with less genomic resources currently available including much of the animal tree of life, such as most molluscs, annelids, sponges, cnidarians and nematodes.…”

Chromosome-level genome assembly of the disco clam,Ctenoides ales, a first for the bivalve order Limida

“…Other factors, such as decreased TE silencing (Liu et al 2022) may also contribute to TE expansion. The genome expansion we found in C. ales along with recent evidence for highly variable TE content across bivalves (Martelossi et al 2023) highlight the importance of this genomically understudied group of animals for exploring the genomic and biological influences on TE evolution.…”

Comparative Analysis of Bivalve and Sea Urchin Genetics and Development: Investigating the Dichotomy in Bilateria

“…For instance, the average observed transposable element content in the genomes of 27 bivalve species is reported to be 38.97%. However, Pectinidae exhibit a relatively lower proportion of TEs, at around 20% [77]. Compared to the genomes of cephalopods and gastropods, there is a higher prevalence of LINE retrotransposons, specifically RTE-X and CR1-Zenon.…”

“…The types of DNA transposons, namely Kolobok, Zator, and Academ, are mainly found in bivalves, whereas the Zisrupton, Novosib, and Merlin superfamilies are predominantly restricted to the analyzed cephalopods [77].…”