Xenoturbella, Acoela, and Nemertodermatida are
worm-like simple bilateral animals, which might give insights into the earliest
steps in the evolution of Bilateria.
Phylogenomic analyses (Philippe
et al. 2011; Cannon et al.
2016) and some ultrastructural characters (Franzén &
Afzelius 1987; Lundin 1998) group
them into a monophyletic group, which has been named Xenacoelomorpha (Philippe et al. 2011; Tyler &
Schilling 2011).
Xenoturbella has been kind of a puzzle for zoologists since
it was described in 1949. First considered to be a primitive turbellarian
flatworm, occasionally affiliated with Hemichordata, suggested to be a sister
group to other bilaterians, for a moment mistaken for a mollusc, then suggested
to be a deuterostome,
then again together with Acoelomorpha (Acoela and Nemertodermatida) as a sister
group to Bilateria, and then back to deuterostome affinity, as a sister group
to Ambulacraria (Echinodermata
and Hemichordata) (Telford 2008; Hejnol et al. 2009; Philippe et al. 2011). It is exciting
that four new species of Xenoturbella have now
been found in the Pacific ocean (Rouse et al. 2016). Before,
only one small (up to 4 cm) species (X.
bocki) was known from the west coast of Sweden (the second, X. westbladi, from the same place is
probably the same species). Three of the new species are much bigger than X. bocki, some of them 20 cm or
longer, but all are otherwise anatomically and in their habits (feeding on
bivalves on the muddy ocean floor) quite similar to each other, which is also
consistent with the genetic data. I heard about a new large Xenoturbella species found in the
Pacific in 2010 while at EDIT
taxonomy course in Kristineberg ,
Sweden . Sounded
pretty unbelievable. I was hoping that this amazing new discovery will help to
solve the phylogenetic position of Xenoturbella
and Xenacoelomorpha more reliably, but it seems that the debate will continue
for years to come.
Rouse et
al. (2016) gathered also
phylogenomic data for one of the new species and sequenced complete
mitochondrial genomes of all the new species. Their phylogenetic analyses were
incongruent to each other. Phylogenomic analyses based on nearly 1200 nuclear
protein coding genes found Xenacoelomorpha (composed in this dataset of one
Acoela and two Xenoturbella species)
as sister group to other Bilateria (Nephrozoa) (using site homogeneous models)
or as a sister group to Protostomia (using site heterogeneous CAT model).
Analyses based on mitochondrial proteins grouped Xenacoelomorpha (4 acoels and
4 xenoturbellid species) with deuterostomes. In the same issue of Nature where Rouse et al's paper was
published, Cannon et al. (2016)
investigated the placement of Xenacoelomorpha more thoroughly, although using
only one Xenoturbella species, but
with many more Acoela species (7) and including Nemertodermatida (4 species). Cannon
et al. (2016) added
impressive amount of new transcriptome data (including for Xenoturbella), which enabled them to have pretty complete datasets
for phylogenetic analyses (phylogenomic datasets tend to be gappy if not based
on fully sequenced genomes). Cannon et al. (2016) results were much more
consistent compared to Rouse et al. (2016), finding support only
for sister-group relationship between Xenacoelomorpha and Nephrozoa (all other Bilateria, hypothetically having ancestrally nephridia
in contrast to Xenacoelomorpha, which lack them). However, when fast-evolving
acoelomorphs where excluded (retaining only clearly slower evolving Xenoturbella), statistical support for
Nephrozoa and Deuterostomia decreased (from 99–100% to 81% in both cases).
Unfortunately, Cannon et al. (2016)
did not analyse this dataset with more complex CAT model and I suspect if they
had, support for Nephrozoa and Deuterostomia would have disappeared entirely
and Xenoturbella might have jumped
next to Ambulacraria (as in Philippe
et al. 2011). Cannon et al. (2016)
did analyze their main dataset (which included Acoelomorpha) also with CAT
model fully supporting Nephrozoa and Deuterostomia, but the internal branches
leading to Nephrozoa and Deuterostomia of the resulting phylogenetic tree were
clearly shorter (barely visible in the published figure) than in the analyses
using simpler phylogenetic models. Simpler site homogeneous models
underestimate the amount of sequence evolution compared to site heterogeneous models
(like CAT) and can therefore produce artefactual groupings (grouping of fast-evolving,
long-branch taxa with each other or with a distant out-group, regardless of
their actual phylogenetic affinities). It could be that the fast-evolving
Acoelomorpha (which is clearly evident in the long branches they display in
phylogenetic analyses, the shortest ones perhaps still about twice as long as
the Xenoturbella branch) caused the
whole Xenacoelomorpha to shift artefactually at the base of Bilateria, away
from more slowly evolving Deuterostomia and this way creating the Nephrozoa.
CAT model was able to shorten the branches supporting monophyly of Nephrozoa
and Deuterostomia, but not entirely to overcome possible non-phylogenetic
signal present in the fast-evolving Acoelomorpha.
In
conclusion, I think it is too early to exclude deuterostome affinity of Xenacoelomorpha.
Curiously, while looking at the pictures of the new large species of Xenoturbella, I thought
that they looked a bit like enteropneusts (Hemichordata). Could it
be that the ring furrow of Xenoturbella,
which divides the body into the head and tail region, is homologous to the collar
(or to part of it) of Hemichordata (Deuterostomia: Ambulacraria)?
References
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