The slowly evolving genome of the xenacoelomorph worm Xenoturbella bocki
Curation statements for this article:-
Curated by eLife
eLife assessment
The authors provide a high quality genome of the xenacoelomorph worm Xenoturbella bocki and discuss its structure and evolution. Understanding the genomic structure of this group provides important insights into bilaterian evolution. The authors make a solid case that the data they present can support the placement of Xenacoelomorpha within the deuterostomes rather than as a sister group to all other bilaterians, but do not unequivocally reject the competing scenario.
This article has been Reviewed by the following groups
Listed in
- Evaluated articles (eLife)
Abstract
The evolutionary origins of Bilateria remain enigmatic. One of the more enduring proposals highlights similarities between a cnidarian-like planula larva and simple acoel-like flatworms. This idea is based in part on the view of the Xenacoelomorpha as an outgroup to all other bilaterians which are themselves designated the Nephrozoa (protostomes and deuterostomes). Genome data can help to elucidate phylogenetic relationships and provide important comparative data. Here we assemble and analyse the genome of the simple, marine xenacoelomorph Xenoturbella bocki , a key species for our understanding of early bilaterian and deuterostome evolution. Our highly contiguous genome assembly of X. bocki has a size of ∼111 Mbp in 18 chromosome like scaffolds, with repeat content and intron, exon and intergenic space comparable to other bilaterian invertebrates. We find X. bocki to have a similar number of genes to other bilaterians and to have retained ancestral metazoan synteny. Key bilaterian signalling pathways are also largely complete and most bilaterian miRNAs are present. We conclude that X. bocki has a complex genome typical of bilaterians, in contrast to the apparent simplicity of its body plan. Overall, our data do not provide evidence supporting the idea that Xenacoelomorpha are a primitively simple outgroup to other bilaterians and gene presence/absence data support a relationship with Ambulacraria.
Article activity feed
-
Author response:
Reviewer #1 (Public Review):
The authors report a high-quality genome assembly for a member of Xenacoelomorpha, a taxon that is at the center of the last remaining great controversies in animal evolution. The taxon and the species in question have "jumped around" the animal tree of life over the past 25 years, and seemed to have found their place as a sister-group to all remaining bilaterians. This hypothesis posits that the earliest split within Bilateria includes Xenacoelomorpha on the one hand and a clade known as Nephrozoa (Protostomia + Deuterostomia) on the other, and is thus referred to as the Nephrozoa hypothesis. Nephrozoa is supported by phylogenomic evidence, by a number of synapomorphic morphological characters in the Nephrozoa (namely, the presence of nephridia) and lack of some key bilaterian characters …
Author response:
Reviewer #1 (Public Review):
The authors report a high-quality genome assembly for a member of Xenacoelomorpha, a taxon that is at the center of the last remaining great controversies in animal evolution. The taxon and the species in question have "jumped around" the animal tree of life over the past 25 years, and seemed to have found their place as a sister-group to all remaining bilaterians. This hypothesis posits that the earliest split within Bilateria includes Xenacoelomorpha on the one hand and a clade known as Nephrozoa (Protostomia + Deuterostomia) on the other, and is thus referred to as the Nephrozoa hypothesis. Nephrozoa is supported by phylogenomic evidence, by a number of synapomorphic morphological characters in the Nephrozoa (namely, the presence of nephridia) and lack of some key bilaterian characters in Xenacoelomorpha, and by the presence of unique miRNAs in Nephrozoa.
The Nephrozoa hypothesis has been challenged several times by the authors' groups who alternatively suggest placing Xenacoelomorpha within Deuterostomia as a sister group to a clade known as Ambulacraria. This hypothesis (the Xenambulacraria hypothesis) is supported by alternative phylogenomic datasets and by the shared presence of a number of unique molecular signatures. In this contribution, the authors aim to strengthen their case by providing full genome data for Xenoturbella bocki.
The actual sequencing and analysis are technically and methodologically excellent. Some of the analyses were done several years ago using approaches that may now seem obsolete, but there is no reason not to include them. As a detailed report of a newly sequenced genome, the manuscript meets the highest standards.
The authors emphasize a number of key findings. One is the fact that the genome is not as simple as one might expect from a "basal" taxon, and is on par with other bilaterian genomes and even more complex than the genome of secondarily simplified bilaterians. There is an implicit expectation here that the sister group to all Bilateria would represent the primitive state. This is of course not true, and the authors are aware of this, but it sometimes feels as though they are using this implicit assumption as a straw dog argument to say that since the genome is not as simple as expected, X. bocki must be nested within Bilateria. The authors get around this by acknowledging that their finding is consistent with a "weak version of the Nephrozoa hypothesis", which is essentially the Nephrozoa phylogenetic hypothesis without implicit assumptions of simplicity.
We were NOT suggesting that Xenacoels are ‘basal’ though others have certainly done so. We were testing, instead, whether their supposed simplicity is reflected in the compostion of the genome.
Another finding is a refutation of the miRNA data supporting Nephrozoa. This is an important finding although it is somewhat flogging a dead horse, since there is already a fair amount of skepticism about the validity of the miRNA data (now over 20 years old) for higher-level phylogenetics.
The missing bilaterian microRNAs was one of the early pieces of evidence excluding the Xenacoelomorpha from Nephrozoa. Our new data are an important refutation of this source of evidence and add to the picture that this phylum is not lacking characters of Bilateria as had been suggested (missing micro RNAs Hox genes explicitly interpreted in this way).
The finding that the authors feel is most important is gene presence-absence data that recovers a topology in which X. bocki is sister to Abulacraria. The problem is that the same tree does not support the monophyly of Xenacoelomorpha. This may be an artifact of fast evolving acoel genomes, as the authors suggest, but it still raises questions about the robustness of the data.
In sum, the authors' results and analyses leave an open window for the Xenambulacraria hypothesis, but do not refute the Nephrozoa hypothesis. The manuscript is a valuable contribution to the debate but does not go a significant way towards its resolution.
The manuscript has gone through several rounds of review and revision on a preprint server and is thus fairly clear of typos, inconsistencies and lack of clarity. The authors are honest and open in their interpretation of the results and their strengths.
We thank the reviewer for their assessment of our manuscript. We have responded to some of the points they make above. As there were no specific points to edit or change raised by reviewer 1, we are replying in detail only to reviewer 2. We like to note that we have modified the text and thus focus of our manuscript in accordance to with what we think reviewer 1 is suggesting in the last two paragraphs of their review.
Reviewer #2 (Public Review):
The manuscript describes the genome assembly and analysis of Xenoturbella bocki, a worm that bears many morphological features ascribed to basal bilateria. The authors aim to analyse this genome in an attempt to determine the phylogenetic position of X. bocki as a representative of Xenacoelomorpha and its associated acoelomorphs. In doing so, they want to inform the debate as to whether xenacoelomorph belong among, or is in fact paraphyletic to all bilaterians.
This paper presents a high-quality assembly of the X. bocki genome. By virtue of the phylogenetic position of this species, this genome has considerable scientific interest. This assembly appears to be highly complete and is a strength of the paper. The further characterisation of the genome is well executed and presented. Solid results from this paper include a comprehensive description of the Hox genes, miRNA and neruopeptide repertoire, as well as a description of the linkage group and how they relate to the ancestral linkage groups.
Where this paper is weaker is that for the central claims and questions of this paper, i.e,. the question of the phylogenetic position of xenacoelomorph and whether X. bocki is a slowly evolving, but otherwise representative member of this clade, remains insufficiently resolved.
The authors have achieved the goal of describing the X. bocki genome very well. By contrast, it is unclear, based on the presented evidence, whether xenacoelomorph is truly a monophyletic group. The balance of the evidence seems to suggest that the X. bocki genome belongs within the bilateria group. However, it is unclear as to what is driving the position of the other acoels. Assuming that X. bocki and the other two species in that group are monophyletic, then the evidence will favour the authors' conclusion (but without clearly rejecting the alternatives).
This paper will likely further animate the debate regarding this basal species, and also questions related to the ancestral characters of bilateria as a whole. In particular the results from the HOX and paraHOX clusters, may provide an interesting counterpoint to the previous results based on the acoels.
We thank the Reviewer for their extended comments on our manuscript. We would firstly like to point out that our work was not aiming to resolve the phylogenetic position of X. bocki. We discussed this question at length, as it was and is a major and important question in evolutionary biology, however we think that we had phrased any conclusions in this regard very cautiously as we are well aware of limitations in our data to resolve the conundrum.
In this revision we have further modified our text, specifically in the Introduction and Abstract, to make it clear that we are contributing to the understanding of the evolution and biology of a fascinating organism that cannot easily be cultured in the laboratory.
In addition, we have supplied more explanation on why Xenacoelomorpha are generally seen as a monophyletic group and which lines of evidence point to this. Again, it should be noted here that colleagues who regard the Nephrozoa hypothesis as true, do not doubt the monophyly of Xenacoelomorpha.
-
eLife assessment
The authors provide a high quality genome of the xenacoelomorph worm Xenoturbella bocki and discuss its structure and evolution. Understanding the genomic structure of this group provides important insights into bilaterian evolution. The authors make a solid case that the data they present can support the placement of Xenacoelomorpha within the deuterostomes rather than as a sister group to all other bilaterians, but do not unequivocally reject the competing scenario.
-
Reviewer #1 (Public Review):
The authors report a high-quality genome assembly for a member of Xenacoelomorpha, a taxon that is at the center of the last remaining great controversies in animal evolution. The taxon and the species in question have "jumped around" the animal tree of life over the past 25 years, and seemed to have found their place as a sister-group to all remaining bilaterians. This hypothesis posits that the earliest split within Bilateria includes Xenacoelomorpha on the one hand and a clade known as Nephrozoa (Protostomia + Deuterostomia) on the other, and is thus referred to as the Nephrozoa hypothesis. Nephrozoa is supported by phylogenomic evidence, by a number of synapomorphic morphological characters in the Nephrozoa (namely, the presence of nephridia) and lack of some key bilaterian characters in Xenacoelomorpha, …
Reviewer #1 (Public Review):
The authors report a high-quality genome assembly for a member of Xenacoelomorpha, a taxon that is at the center of the last remaining great controversies in animal evolution. The taxon and the species in question have "jumped around" the animal tree of life over the past 25 years, and seemed to have found their place as a sister-group to all remaining bilaterians. This hypothesis posits that the earliest split within Bilateria includes Xenacoelomorpha on the one hand and a clade known as Nephrozoa (Protostomia + Deuterostomia) on the other, and is thus referred to as the Nephrozoa hypothesis. Nephrozoa is supported by phylogenomic evidence, by a number of synapomorphic morphological characters in the Nephrozoa (namely, the presence of nephridia) and lack of some key bilaterian characters in Xenacoelomorpha, and by the presence of unique miRNAs in Nephrozoa.
The Nephrozoa hypothesis has been challenged several times by the authors' groups who alternatively suggest placing Xenacoelomorpha within Deuterostomia as a sister group to a clade known as Ambulacraria. This hypothesis (the Xenambulacraria hypothesis) is supported by alternative phylogenomic datasets and by the shared presence of a number of unique molecular signatures. In this contribution, the authors aim to strengthen their case by providing full genome data for Xenoturbella bocki.
The actual sequencing and analysis are technically and methodologically excellent. Some of the analyses were done several years ago using approaches that may now seem obsolete, but there is no reason not to include them. As a detailed report of a newly sequenced genome, the manuscript meets the highest standards.The authors emphasize a number of key findings. One is the fact that the genome is not as simple as one might expect from a "basal" taxon, and is on par with other bilaterian genomes and even more complex than the genome of secondarily simplified bilaterians. There is an implicit expectation here that the sister group to all Bilateria would represent the primitive state. This is of course not true, and the authors are aware of this, but it sometimes feels as though they are using this implicit assumption as a straw dog argument to say that since the genome is not as simple as expected, X. bocki must be nested within Bilateria. The authors get around this by acknowledging that their finding is consistent with a "weak version of the Nephrozoa hypothesis", which is essentially the Nephrozoa phylogenetic hypothesis without implicit assumptions of simplicity.
Another finding is a refutation of the miRNA data supporting Nephrozoa. This is an important finding although it is somewhat flogging a dead horse, since there is already a fair amount of skepticism about the validity of the miRNA data (now over 20 years old) for higher-level phylogenetics.
The finding that the authors feel is most important is gene presence-absence data that recovers a topology in which X. bocki is sister to Abulacraria. The problem is that the same tree does not support the monophyly of Xenacoelomorpha. This may be an artifact of fast evolving acoel genomes, as the authors suggest, but it still raises questions about the robustness of the data.
In sum, the authors' results and analyses leave an open window for the Xenambulacraria hypothesis, but do not refute the Nephrozoa hypothesis. The manuscript is a valuable contribution to the debate but does not go a significant way towards its resolution.
The manuscript has gone through several rounds of review and revision on a preprint server and is thus fairly clear of typos, inconsistencies and lack of clarity. The authors are honest and open in their interpretation of the results and their strengths. -
Reviewer #2 (Public Review):
The manuscript describes the genome assembly and analysis of Xenoturbella bocki, a worm that bears many morphological features ascribed to basal bilateria. The authors aim to analyse this genome in an attempt to determine the phylogenetic position of X. bocki as a representative of Xenacoelomorpha and its associated acoelomorphs. In doing so, they want to inform the debate as to whether xenacoelomorph belong among, or is in fact paraphyletic to all bilaterians.
This paper presents a high-quality assembly of the X. bocki genome. By virtue of the phylogenetic position of this species, this genome has considerable scientific interest. This assembly appears to be highly complete and is a strength of the paper. The further characterisation of the genome is well executed and presented. Solid results from this …
Reviewer #2 (Public Review):
The manuscript describes the genome assembly and analysis of Xenoturbella bocki, a worm that bears many morphological features ascribed to basal bilateria. The authors aim to analyse this genome in an attempt to determine the phylogenetic position of X. bocki as a representative of Xenacoelomorpha and its associated acoelomorphs. In doing so, they want to inform the debate as to whether xenacoelomorph belong among, or is in fact paraphyletic to all bilaterians.
This paper presents a high-quality assembly of the X. bocki genome. By virtue of the phylogenetic position of this species, this genome has considerable scientific interest. This assembly appears to be highly complete and is a strength of the paper. The further characterisation of the genome is well executed and presented. Solid results from this paper include a comprehensive description of the Hox genes, miRNA and neruopeptide repertoire, as well as a description of the linkage group and how they relate to the ancestral linkage groups.
Where this paper is weaker is that for the central claims and questions of this paper, i.e,. the question of the phylogenetic position of xenacoelomorph and whether X. bocki is a slowly evolving, but otherwise representative member of this clade, remains insufficiently resolved.
The authors have achieved the goal of describing the X. bocki genome very well. By contrast, it is unclear, based on the presented evidence, whether xenacoelomorph is truly a monophyletic group. The balance of the evidence seems to suggest that the X. bocki genome belongs within the bilateria group. However, it is unclear as to what is driving the position of the other acoels. Assumign that X. bocki and the other two species in that group are monophyletic, then the evidence will favour the authors' conclusion (but without clearly rejecting the alternatives).
This paper will likely further animate the debate regarding this basal species, and also questions related to the ancestral characters of bilateria as a whole. In particular the results from the HOX and paraHOX clusters, may provide an interesting counterpoint to the previous results based on the acoels.
-
-
-
-
-