Nuclear genomic signals of the ‘microturbellarian’ roots of platyhelminth evolutionary innovation

Abstract

Flatworms number among the most diverse invertebrate phyla and represent the most biomedically significant branch of the major bilaterian clade Spiralia, but to date, deep evolutionary relationships within this group have been studied using only a single locus (the rRNA operon), leaving the origins of many key clades unclear. In this study, using a survey of genomes and transcriptomes representing all free-living flatworm orders, we provide resolution of platyhelminth interrelationships based on hundreds of nuclear protein-coding genes, exploring phylogenetic signal through concatenation as well as recently developed consensus approaches. These analyses robustly support a modern hypothesis of flatworm phylogeny, one which emphasizes the primacy of the often-overlooked ‘microturbellarian’ groups in understanding the major evolutionary transitions within Platyhelminthes: perhaps most notably, we propose a novel scenario for the interrelationships between free-living and vertebrate-parasitic flatworms, providing new opportunities to shed light on the origins and biological consequences of parasitism in these iconic invertebrates.

DOI: http://dx.doi.org/10.7554/eLife.05503.001

eLife digest

Flatworms are relatively simple invertebrates with soft bodies. They can be found living in nearly every aquatic environment on the planet, are well-known for their ability to regenerate, and some species live as parasites in humans and other animals. Studies of the physical characteristics of flatworms have provided us with clues about how some groups, for example, the parasitic flatworms, have evolved, but the evolutionary origins of other groups of flatworms are less clear.

The genetic studies of flatworm evolution have focused on a single gene that makes a molecule called ribosomal ribonucleic acid, which is required to make all the proteins in flatworms and other animals. By comparing the sequences of this gene in different species of flatworm, it is possible to infer how they are related in evolutionary terms—that is, species with shared gene sequence features are likely to be more closely related than two species with less similar gene sequences. Although this approach has proved to be useful, it has also produced some results that conflict with the conclusions of previous studies.

Here, Laumer et al. studied the evolution of flatworms using an approach called RNA sequencing. This approach made it possible to sequence many hundreds of genes in all major groups of flatworms, and compare these genes in different species. Laumer et al. used the data to build a ‘phylogenetic tree’ that infers the evolutionary relationships between the different groups of flatworms.

This tree provides evidence that supports some of the ideas about flatworm evolution produced by the previous studies based on both physical features and ribosomal ribonucleic acid. It also presents several unexpected evolutionary relationships; for example, it suggests that the parasitic flatworms are most closely related to a group of small flatworms called Bothrioplanida, which are predators of other invertebrates. Bothrioplanida can live in many freshwater environments, and the physical characteristics that allow them to survive might resemble those found in the earliest parasitic flatworms.

The phylogenetic tree made by Laumer et al. represents a guide for researchers seeking clues to the origins of the genetic and developmental innovations that underlie the various physical features found in different flatworms.

DOI: http://dx.doi.org/10.7554/eLife.05503.002