A New “Asexual Scandal”: Independent Evolution of Ancient Planarian Fissiparous Lineages Challenges Phylogenetic Reconstruction Methods

Abstract

Phylogenetic methods typically generate bifurcating trees reflecting monophyletic groups formed by populations. However, unexpected topologies sometimes emerge, raising questions about whether they stem from methodological artifacts or biological phenomena. In a recent transcriptome-based study of Dugesia species, asexual populations displayed an unusual phylogenetic pattern: instead of forming monophyletic groups, each individual emerged as a long-branched independent lineage, resulting in a distinctive "ladder-pattern." While such a pattern could result from methodological issues, its exclusive presence in asexual populations suggests a biological explanation—long-term asexuality. Traditionally considered evolutionary dead ends due to reduced genetic diversity and weakened purifying selection, extant long-term asexual lineages challenge these assumptions, being popularly known as "asexual scandals". Here, we test both hypotheses: first, assessing whether the ladder-pattern arises from methodological artifacts, and second, examining expected genomic signatures of prolonged asexuality or hybridization. Using transcriptomic and nuclear marker datasets, we employ state-of-the-art phylogenetic methodologies and intraindividual genetic diversity analyses. Our results confirm that the ladder-pattern is not an artifact. Comparative analyses with other fissiparous planarian lineages support the deep evolutionary history of these asexual populations. Furthermore, we demonstrate that retained ancestral polymorphisms obscure phylogenetic signals. Our findings highlight the limitations of traditional phylogenetic methods in the context of asexuality and underscore the need to renew the models traditionally used in evolutionary studies.