Large-scale phylogenomics of the genus Macrostomum (Platyhelminthes) reveals cryptic diversity and novel sexual traits

Jeremias N Brand,Gudrun Viktorin,R Axel W Wiberg,Christian Beisel,Lukas Schärer

doi:10.1016/j.ympev.2021.107296

Jeremias N Brand, Gudrun Viktorin + Show 3 more

Open Access

https://doi.org/10.1016/j.ympev.2021.107296

Copy DOI

Abstract

Free-living flatworms of the genus Macrostomum are small and transparent animals, representing attractive study organisms for a broad range of topics in evolutionary, developmental, and molecular biology. The genus includes the model organism M. lignano for which extensive molecular resources are available, and recently there is a growing interest in extending work to additional species in the genus. These endeavours are currently hindered because, even though >200 Macrostomum species have been taxonomically described, molecular phylogenetic information and geographic sampling remain limited. We report on a global sampling campaign aimed at increasing taxon sampling and geographic representation of the genus. Specifically, we use extensive transcriptome and single-locus data to generate phylogenomic hypotheses including 145 species. Across different phylogenetic methods and alignments used, we identify several consistent clades, while their exact grouping is less clear, possibly due to a radiation early in Macrostomum evolution. Moreover, we uncover a large undescribed diversity, with 94 of the studied species likely being new to science, and we identify multiple novel morphological traits. Furthermore, we identify cryptic speciation in a taxonomically challenging assemblage of species, suggesting that the use of molecular markers is a prerequisite for future work, and we describe the distribution of putative synapomorphies and suggest taxonomic revisions based on our finding. Our large-scale phylogenomic dataset now provides a robust foundation for comparative analyses of morphological, behavioural and molecular evolution in this genus.

Highlights

The genus Macrostomum (Macrostomorpha, Platyhelminthes) is a large clade of free-living flatworms with a global distribution in marine, brackish and freshwater environments (Ferguson, 1954)
We identify cryptic speciation in a taxonomically challenging assemblage of species, suggesting that the use of molecular markers is a prerequisite for future work, and we describe the distribution of putative synapomorphies and suggest taxonomic revisions based on our finding
We present a phylogenomic analysis based on a combination of transcriptome and Sanger-sequencing, thereby significantly expand ing the phylogenetic and genomic resources available for the genus

Summary

Introduction

The genus Macrostomum (Macrostomorpha, Platyhelminthes) is a large clade of free-living flatworms with a global distribution in marine, brackish and freshwater environments (Ferguson, 1954). Primarily due to the discovery of a whole genome dupli cation and accompanying karyotype instability in M. lignano (Zadese nets et al, 2016, 2017), there is increased interest in expanding the genomic resources and molecular phylogenetic placement of additional species in the genus,. To this end, recent work has provided tran scriptomic resources for additional species (Brand et al, 2020) and fieldcollections have revealed similar karyological rearrangements to the ones observed in M. lignano in some closely related species, while others were found to have stable diploid genomes (Scharer et al, 2020; Zadesenets et al, 2020). A better phylogeny will permit to study the (co)evolution of the large diversity of morphological and behavioural traits in this genus (see below)

Methods

Results

Conclusion