Structural and Evolutionary Analysis of Saci2-Like LTR Retrotransposons in Diphyllobothriidean Tapeworms

Cyclophyllideans, which diverged from diphyllobothriideans, have evolved compact genomes to meet ecological and biological demands associated with rapid development, early maturation, and prolific asexual reproduction. This streamlining is accompanied by inactivation of transposable elements (TEs), including retrotransposons. In contrast, diphyllobothriideans retain large, retrotransposon-rich genomes, but information on their individual retrotransposons is lacking. Here, Saci2-like long terminal repeat (LTR) retrotransposons, formerly annotated as lennie in taeniid cestodes, were identified in the diphyllobothriideans Spirometra erinaceieuropaei and Sparganum proliferum, along with orthologs from Schistocephalus solidus and Ligula intestinalis. The Saci2 homologs in these genomes diversified into at least eight families, exhibiting substantial variation in LTR and primer binding site sequences, reflecting ongoing regulatory diversification. Phylogenetic and divergence analyses indicated that they maintain structural and functional integrity under purifying selection, while early signs of inactivation appeared in S. proliferum. These findings suggest that diphyllobothriideans have faced little pressure for genome compaction, permitting the retention of functional retrotransposons, whereas cyclophyllideans, particularly taeniids, underwent genome streamlining linked to shortened life cycles and high fecundity, resulting in retrotransposon degradation. This contrast underscores the reciprocal relationship between biological demands and genome remodeling with TE inactivation in metazoans.