Zoology - Worming Into The Origin of Bilaterians

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Zoology: Worming into the Origin of Bilaterians


taz
Ferdinand Marle
Molecular Genetics Unit, Okinawa Institute of Science & Technology, Onna-son, Japan
Correspondence: ferdinand.marletaz@gmail.com
https://doi.org/10.1016/j.cub.2019.05.006

Xenacoelomorphs, a group of worms with simple body organization, have been proposed to represent the
first offshoot of bilaterians. A new study shows that they might instead belong to the deuterostomes, just
as echinoderms and vertebrates.

The nature of the last common ancestor of by Herve  Philippe, Max Telford and insects, molluscs, annelids, flatworms)
all bilaterally symmetrical animals — the colleagues [1] in Current Biology brings and the deuterostomes (including
urbilaterian — is one of the key questions new elements to support this latter tree, in vertebrates, tunicates, sea urchins and
in zoology, partly because it reflects on particular a thorough evaluation of sea stars). This reclassification implied that
the origin of the key organ systems that methodological bias that can affect seemingly simple lineages may have
make us who we are. There are two phylogenetics reconstruction — such as originated through simplification and
opposing views of what this ancestor may the famous long-branch attraction. They secondary character losses from a more
have been like — either it was a rather conclude that xenacoelomorphs are the complex coelom-bearing urbilaterian
simple organism or a fairly complex one. sister-group of a clade called ancestor [3].
And, a lot of the debate surrounding this ‘Ambulacraria’, which includes sea stars, Then, in the late nineties, a study [4]
dichotomy revolves around the sea urchins and acorn worms. pointed out that a neglected lineage of
phylogenetic position of a handful of The idea that the urbilaterian was a flatworms — the acoels — might have
worms — the xenacoelomorphs. Two simple organism without a body cavity represented a sister-group to both
alternative positions were successively (coelom) reminiscent of the planula larva of protostomes and deuterostomes. This
proposed over the years: one suggests some cnidarians was mentioned a long reignited the debate concerning the nature
that this group of morphologically simple time ago, for instance in the famous of the bilaterian ancestor and propelled
worms is the sister-group to all other zoology textbook of Libbie Hyman [2]. At these overlooked animals to the front
bilaterians. This branching would mean this time, morphologically simple animals, stage of animal evolution. Acoel flatworms
that the bilaterian ancestor was a rather such as nematode roundworms and indeed show a very simple planula-like
unsophisticated organism. Alternatively, flatworms, were considered as early organization and do not possess
other researchers have proposed that branches of the animal tree of life. structures that are found in other
these xenacoelomorphs instead are a Morphological cladistics and molecular bilaterians, such as a coelomic cavity,
derived offshoot of deuterostomes, one of phylogeny then helped redefine our excretory organs, or nerve chords
the two main clades of bilaterians, which understanding of animal evolution by (Figure 1A). All bilaterians that are not
mean that their simplicity derives from splitting all bilaterian animals into two main acoels were dubbed ‘Nephrozoa’
secondary character loss. A new study clades: the protostomes (including (highlighting the presence of an excretory

Current Biology 29, R568–R591, June 17, 2019 ª 2019 Elsevier Ltd. R577
Current Biology

Dispatches

A Protostomia Nephrozoa Protostomia Protostomia


eliminate spurious sequences from their
datasets, such as contaminants of
Chordata Deuterostomia Chordata Deuterostomia Chordata
technical or biological origin.
Ambulacraria Ambulacraria Xen-
Ambulacraria Xen-
ambulacraria ambulacraria
While more data generally improve
Xenacoelomorpha Xenacoelomorpha Xenacoelomorpha phylogenetic signal, they did not alleviate
Cnidaria Cnidaria Cnidaria reconstruction artefacts such as long-
Nephrozoa hypothesis Xenambulacraria hypothesis Xenambulacraria first hypothesis branch attraction. This is the second issue
C
addressed by Philippe and colleagues [1].
B
Phylogenetic reconstruction relies on a
Site-homogeneous model probabilistic description of the substitution
process between amino acid or nucleotide
GAVLI...KRH Equilibrium frequencies residues in the dataset, called the
KSDRLIFGSNKQKRAMHSRLKNKISEDSIH evolutionary model. Such a model is used
KVDLCIFGTSKQKRALNSRRMNAVGNDIVS
KNDRLTFGSSRKQRALESRLRSAVTSQALE
to compute the probability of different trees
KVDSLIFGTIKQKHALNSRRLNQVGNETLQ given the sequence alignment data and to
KNDRLVFGGAKKKRAMESRLRDKVKREALE ultimately pick the best tree. Long branch
KNDILTFGSSKKKRAVESRLNSKLEVDALG
KVDALIFGSHKQKRALSARRMNQVGGESLQ attraction occurs when the model cannot
cope anymore with the amount of changes
observed in one lineage. This artefact
... usually results in grouping such fast-
evolving lineages together or placing them
GAVLI...KRH GAVLI...KRH GAVLI...KRH
at the base of the tree. Acoel flatworms are
Site-heterogeneous model
among the fastest evolving lineages of
Current Biology bilaterian animals, closely followed by
nemertodermatids, while xenoturbellids,
Figure 1. The placement of xenacoelomorphs and the impact of phylogenetic inference however, evolve at a much slower pace. A
models.
(A) Two examples of acoelomorph flatworms: Diopisthoporus longitubus (top) shows a planula-like
possible solution to this problem is to use a
organisation with a posteroterminal mouth deemed to represent a more ancestral organisation in more realistic description of the patterns of
this lineage; Symsagitiferra schultzei (bottom) is a symbiotic acoel hosting photosynthetic microalgae mutation at play in the genome. For
(photos: Ulf Jondelius). (B) Alternative hypothesis regarding the phylogenetic position of xenacoelomorphs
instance, instead of considering that all
discussed in [1,12,15]. (C) While site-homogeneous models estimate respective abundance of each residue
once in the dataset — the equilibrium frequency — the site-heterogeneous approach considers that each amino acids in the proteins evolve in the
position could be assigned to different categories or profiles, each defined by a specific equilibrium frequency. same way, a model named ‘CAT’ allows
each site to use a distinct profile
system) (Figure 1B). Acoels thus became hypothesis; Figure 1B) [11]. More characterized by its own set of amino acid
attractive models for comparative recently, two new ambitious studies frequencies (Figure 1C) [14]. This new ‘site-
developmental biology [4] or regeneration based on next-generation transcriptome heterogenous’ model appears to be much
studies [5]. sequencing (RNA-seq) introduced an better at coping with fast evolving phyla
Over the years, acoels were joined as the exhaustive dataset of multiple and is therefore far less sensitive to long-
possible earliest bilaterian offshoot xenacoelomorph species including four branch attraction. The only caveat of this
by another group of worms, the new species of Xenoturbella [12,13]. Yet, model, called CAT-GTR, is that it needs to
nemertodermatids [6], and later studies in their paper, Philippe and colleagues [1] estimate many parameters from the
supported another group to join the club, show that precautions should be taken to dataset, which makes it computationally
the xenoturbellids, which constituted handle such a massive amount of data. A more intensive than simpler models.
their own phylogenetic enigma [7,8]. first problem is to decide which genes to The first application of the CAT-GTR
Xenoturbellids were originally represented use and how best to construct a dataset model to investigate the position of the
by a single species (Xenoturbella amenable to phylogenetic reconstruction. xenacoelomorphs rejected their early
bockix; Figure 1B) which was — just like Instead of using a pre-existing set of divergence and suggested instead that
acoels — originally associated with other genes, Philippe and colleagues [1] they belonged to deuterostomes [15]. In
flatworms (platyhelminthes); these three committed to detecting all the available their new study, Philippe and colleagues [1]
animal groups make up the single-copy orthologous genes by attempt to apply the CAT-GTR model to
Xenoacoelomorpha clade [9]. reciprocally aligning all genes for an array the broadest collection of genes so far. To
Philippe and colleagues [1] are not of species including an acoelomorph and do that, they ran many independent trees
the first to address the position of Xenoturbella. If fast evolution can affect using smaller sets of genes randomly
xenacoelomorphs. The first studies tree reconstruction, it can also affect the sampled from their main collection (the
dealing with acoels only used a handful of way genes are gained and lost, and an ‘jack-knife’ approach). As they obtained
genes, notably the small subunits of existing collection of orthologues can be markedly different results with many
ribosomal RNA (rRNA) [10]. The first plagued by hidden duplications or losses alternative sets, they showed that genes
phylogenomic studies placed them as the in the case of xenacoelomorphs. More yielding strong support for unambiguous
sister-group of bilaterians (the Nephrozoa directly, the authors meticulously animal groups also provided a stronger

R578 Current Biology 29, R568–R591, June 17, 2019


Current Biology

Dispatches

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