Close

Annelid functional genomics reveal the origins of bilaterian life cycles

Yan Liang, Francisco M. Martín-Zamora, Kero Guynes, Allan M. Carrillo-Baltodano, Yongkai Tan, Giacomo Moggioli, Océane Seudre, Martin Tran, Kate Mortimer, Nicholas M. Luscombe, Andreas Hejnol, Ferdinand Marlétaz, José M. Martín-Durán

Posted on: 10 March 2022

Preprint posted on 6 February 2022

Article now published in Nature at http://dx.doi.org/10.1038/s41586-022-05636-7

Could the timing of trunk formation be a major driver in larval evolution?

Selected by Paul Bump

Background

There are several major hypotheses for the origin of larvae and one fundamental question is whether larvae are ancestral or have evolved secondarily. One major hypothesis is the “intercalation” hypothesis1-2, which suggests that larval stages were added to the life history of animals multiple times independently. Conversely, the “terminal addition”3-4 hypothesis suggests that larvae were an ancestral form that was shared across metazoans.

Liang and Martín-Zamora and colleagues take a comparative genetics approach using several annelid species, with a specific focus on the worm Owenia fusiformis clarify larval and adult origins. O. fusiformis is a species of annelid worm that branched off earlier than some of the other studied annelids and has a distinctive mitraria larva which lacks the characteristic ciliary bands of the trochophore larvae of other annelids (Figure 1).

DIC and confocal of O. fusiformis mitraria stained for DAPI and acetylated alpha-tubulin and image of adult O. fusiformis
Figure 1. From Liang and Martín-Zamora et al. 2022 Figure 1D. DIC and confocal of O. fusiformis mitraria stained for DAPI and acetylated alpha-tubulin and image of adult O. fusiformis. at: apical tuft; an: anus; he: head; mo: mouth; pt: prototroch; tt: telotroch. Made available under a CC-BY-NC-ND 4.0 International license.

 

Key findings

First, the authors utilized chromosome-scale genome sequencing in O. fusiformis and found 12 chromosomes with an almost complete set of metazoan BUSCO genes (97.5%) and these 12 chromosomes were linked to the 22 ancestral linkage groups in bilaterians. They developed stage-specific transcriptomes, which revealed two main phases of gene expression: one during larval formation and the second during larval growth and metamorphosis into the juvenile.

Next, they looked at the formation of the trunk in different annelid species. While there was a similar complement and arrangement of Hox genes in the annelids Capitella telata and Platynereis dumerilii, they found that O. fusiformis does not express Hox genes during embryogenesis, but instead activates them in the trunk rudiment during larval growth, similar to the echiuran annelid Urechis unicinctus and other marine invertebrate larvae referred to as “head” larvae5-6.

Using ATACseq, the authors discovered two different sets of cis-regulatory elements mirrored the transcriptional dynamics they had observed in their RNAseq data, corroborating their hypothesis that there are two distinct modules active during Owenia development.

Finally, they analyzed whether novel genes impact transcriptomic differences using phylostratigraphy, they showed that the changes in expression of novel/younger genes occurred in the juvenile stage, and that novel genes were not correlated with the larval stage. They then performed pairwise comparisons of the transcriptomes of O. fusiformis and C. telata and then applied this to other published transcriptomes of seven other metazoan species.

They concluded that neither the intercalation nor terminal addition hypothesis explain their findings, but instead suggest that mitiria larva of O. fusiformis develops from a head territory, while trunk differentiation occurs late in larval development before the start of metamorphosis (Figure 2). They point out that these deferred development patterns many apply to other annelid species and potentially bilaterians in general.

Figure 2. From Liang and Martín-Zamora et al. 2022 Figure 5A. Schematic drawing of the life cycle and patterning events in a bilaterian with indirect development with a feeding larva like the annelid O. fusiformis and Figure 5B. Schematic drawings of the three main types of life cycles and the timing of Hox gene expression in Bilaterians. Made available under a CC-BY-NC-ND 4.0 International license.

 

What I like about this work

I started graduate school in the Lowe Lab in 2016, when our lab had just published a paper on the role of Hox patterning in the species of indirect developing hemichordates we study (Schizocardium californicum)7. Similar to what Liang and Martín-Zamora have observed here, Paul Gonzalez had found expression of Hox genes late in larval development, again extending the hypothesis of larvae as swimming heads.

This paper is significant to me for several reasons. First, I appreciated the compelling biological story the authors told from an extensive genomics data set. The addition of colorimetric in-situs of Hox gene expression in O. fusiformis complemented the genomics and illustrated a clear expression pattern of trunk delay. They successfully overcame a continuing challenge for the Evo-Devo field, which will be turning large genomic data sets into meaningful biological studies.

Another strength of the manuscript was how comprehensive the authors were in the choice of species and developmental staging. When they analyzed transcriptomic data from multiple species and stages, they used a correlative index (Jensen-Shannon Divergence) to suggest which stages were most similar transcriptionally across species. This is in contrast from relying on morphological landmarks than may be challenging to compare across the development of different species.

Open Questions

The pattern of trunk development in late larvae is particularly interesting. What causes Hox gene expression to occur when it does? And when Hox expression does start, do you think this expression is in larval cells (cells that may not continue into the adult) or cells that are specified for the adult?

To what extent do you think it will be possible to compare the cells in the rudiment of Owenia to other organisms with delayed trunk formation?

And finally, many annelids seem to have striking regenerative capacities of the trunk. Does Owenia? I’m curious if this delayed trunk program could be reactivated in regeneration responses or if a different genetic module would be deployed.

References

  1. Raff, R. A. Origins of the other metazoan body plans: the evolution of larval forms.
    Philos Trans R Soc Lond B Biol Sci 363, 1473-1479 (2008).
  2. Sly, B. J., Snoke, M. S. & Raff, R. A. Who came first – larvae or adults? Origins of
    bilaterian metazoan larvae. Int J Dev Biol 47, 623-632 (2003).
  3. Nielsen, C. Origin and evolution of animal life cycles. Biol Rev 73, 125-155 (1998).
  4. Davidson, E. H., Peterson, K. J. & Cameron, R. A. Origin of bilaterian body plans:
    evolution of developmental regulatory mechanisms. Science 270, 1319-1325 (1995).
  5. Lacalli, T. C. Protochordate body plan and the evolutionary role of larvae: old
    controversies resolved? Can. J. Zool. 83, 216-224 (2005).
  6. Strathman, R. Multiple origins of feeding head larvae by the Early Cambrian. Can. J.
    Zool.
    98, 761-776 (2020).
  7. Gonzalez, P., Uhlinger, K. R. & Lowe, C. J. The Adult Body Plan of Indirect Developing Hemichordates Develops by Adding a Hox-Patterned Trunk to an Anterior Larval Territory. Curr Biol 27, 87-95 (2017).

 

doi: https://doi.org/10.1242/prelights.31596

Read preprint (No Ratings Yet)

Author's response

Francisco M. Martín-Zamora and Yan Liang shared

The pattern of trunk development in late larvae is particularly interesting. What causes Hox gene expression to occur when it does?

This is definitely something we want to explore further. In particular, we want to identify the upstream signalling pathways and the genetic and epigenetic mechanisms driving Hox activation during trunk development in Owenia. It is also likely that spatiotemporal epigenetic differences are at least partially responsible for the heterochronic shifts we propose as drivers of the evolution of bilaterian life cycles. Therefore, we want to compare epigenetic programmes between “head larvae” and lecithotrophic larvae during trunk formation, to identify upstream Hox regulators and how their different deployment in time drives temporal changes in Hox activity.

And when Hox expression does start, do you think this expression is in larval cells (cells that may not continue into the adult) or cells that are specified for the adult?

In our work we saw that the first signs of Hox expression/activity from in situ hybridisations and RNA-seq data appear in the trunk rudiment of the competent larva, so the expression takes place in adult precursors rather than in temporary larval tissues. However, there are a few domains of expression for a couple of Hox genes in the mitraria larva (e.g., Hox3). We would like to explore whether (some) Hox genes play a role in specifying certain cell types in the larva or early specified juvenile adult cell types.

To what extent do you think it will be possible to compare the cells in the rudiment of Owenia to other organisms with delayed trunk formation?

This is very interesting, indeed, and definitely amenable. We can always compare the genetic signatures of these potentially homologous cell populations, whether that’s in a targeted manner (e.g., through in situ hybridisations of key genes) or through genome-wide approaches, either dissecting the trunk rudiments for transcriptomic and epigenomic profiling or through single-cell analyses of these “head larvae”.

And finally, many annelids seem to have striking regenerative capacities of the trunk. Does Owenia? I’m curious if this delayed trunk program could be reactivated in regeneration responses or if a different genetic module would be deployed.

Unlike other annelids that have been previously studied like Capitella teleta or Platynereis dumerilii, which only show posterior regeneration of the trunk, Owenia fusiformis can regenerate both trunk and head. This is naturally something we are very keen on exploring and is one of the current projects of the lab. It would not surprise us to see the Hox genetic program being deployed during trunk regeneration. However, we are intrigued as to whether they would be as preeminent as in the larval growth and metamorphosis phase of development, or whether other genetic modules would dominate the trunk regeneration process.

Have your say

Your email address will not be published. Required fields are marked *

This site uses Akismet to reduce spam. Learn how your comment data is processed.

Sign up to customise the site to your preferences and to receive alerts

Register here

Also in the developmental biology category:

Cellular signalling protrusions enable dynamic distant contacts in spinal cord neurogenesis

Joshua Hawley, Robert Lea, Veronica Biga, et al.

Selected by 15 November 2024

Ankita Walvekar

Developmental Biology

Actin-based deformations of the nucleus control multiciliated ependymal cell differentiation

Marianne Basso, Alexia Mahuzier, Syed Kaabir Ali, et al.

Selected by 30 October 2024

Ryan Harrison

Developmental Biology

HIF1A contributes to the survival of aneuploid and mosaic pre-implantation embryos

Estefania Sanchez-Vasquez, Marianne E. Bronner, Magdalena Zernicka-Goetz

Selected by 11 October 2024

Anchel De Jaime Soguero

Developmental Biology

Also in the evolutionary biology category:

Enhancer-driven cell type comparison reveals similarities between the mammalian and bird pallium

Nikolai Hecker , Niklas Kempynck , David Mauduit, et al.

Selected by 02 July 2024

Rodrigo Senovilla-Ganzo

Bioinformatics

Modular control of time and space during vertebrate axis segmentation

Ali Seleit, Ian Brettell, Tomas Fitzgerald, et al.

AND

Natural genetic variation quantitatively regulates heart rate and dimension

Jakob Gierten, Bettina Welz, Tomas Fitzgerald, et al.

Selected by 24 June 2024

Girish Kale, Jennifer Ann Black

Developmental Biology

Fetal brain response to maternal inflammation requires microglia

Bridget Elaine LaMonica Ostrem, Nuria Dominguez Iturza, Jeffrey Stogsdill, et al.

Selected by 24 April 2024

Manuel Lessi

Neuroscience

preLists in the developmental biology category:

BSDB/GenSoc Spring Meeting 2024

A list of preprints highlighted at the British Society for Developmental Biology and Genetics Society joint Spring meeting 2024 at Warwick, UK.

 



List by Joyce Yu, Katherine Brown

GfE/ DSDB meeting 2024

This preList highlights the preprints discussed at the 2024 joint German and Dutch developmental biology societies meeting that took place in March 2024 in Osnabrück, Germany.

 



List by Joyce Yu

‘In preprints’ from Development 2022-2023

A list of the preprints featured in Development's 'In preprints' articles between 2022-2023

 



List by Alex Eve, Katherine Brown

preLights peer support – preprints of interest

This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.

 



List by preLights peer support

The Society for Developmental Biology 82nd Annual Meeting

This preList is made up of the preprints discussed during the Society for Developmental Biology 82nd Annual Meeting that took place in Chicago in July 2023.

 



List by Joyce Yu, Katherine Brown

CSHL 87th Symposium: Stem Cells

Preprints mentioned by speakers at the #CSHLsymp23

 



List by Alex Eve

Journal of Cell Science meeting ‘Imaging Cell Dynamics’

This preList highlights the preprints discussed at the JCS meeting 'Imaging Cell Dynamics'. The meeting was held from 14 - 17 May 2023 in Lisbon, Portugal and was organised by Erika Holzbaur, Jennifer Lippincott-Schwartz, Rob Parton and Michael Way.

 



List by Helen Zenner

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

Alumni picks – preLights 5th Birthday

This preList contains preprints that were picked and highlighted by preLights Alumni - an initiative that was set up to mark preLights 5th birthday. More entries will follow throughout February and March 2023.

 



List by Sergio Menchero et al.

CellBio 2022 – An ASCB/EMBO Meeting

This preLists features preprints that were discussed and presented during the CellBio 2022 meeting in Washington, DC in December 2022.

 



List by Nadja Hümpfer et al.

2nd Conference of the Visegrád Group Society for Developmental Biology

Preprints from the 2nd Conference of the Visegrád Group Society for Developmental Biology (2-5 September, 2021, Szeged, Hungary)

 



List by Nándor Lipták

Fibroblasts

The advances in fibroblast biology preList explores the recent discoveries and preprints of the fibroblast world. Get ready to immerse yourself with this list created for fibroblasts aficionados and lovers, and beyond. Here, my goal is to include preprints of fibroblast biology, heterogeneity, fate, extracellular matrix, behavior, topography, single-cell atlases, spatial transcriptomics, and their matrix!

 



List by Osvaldo Contreras

EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)

A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.

 



List by Alex Eve

EMBL Conference: From functional genomics to systems biology

Preprints presented at the virtual EMBL conference "from functional genomics and systems biology", 16-19 November 2020

 



List by Jesus Victorino

Single Cell Biology 2020

A list of preprints mentioned at the Wellcome Genome Campus Single Cell Biology 2020 meeting.

 



List by Alex Eve

Society for Developmental Biology 79th Annual Meeting

Preprints at SDB 2020

 



List by Irepan Salvador-Martinez, Martin Estermann

FENS 2020

A collection of preprints presented during the virtual meeting of the Federation of European Neuroscience Societies (FENS) in 2020

 



List by Ana Dorrego-Rivas

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.

 



List by Ana Dorrego-Rivas

Cell Polarity

Recent research from the field of cell polarity is summarized in this list of preprints. It comprises of studies focusing on various forms of cell polarity ranging from epithelial polarity, planar cell polarity to front-to-rear polarity.

 



List by Yamini Ravichandran

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

3D Gastruloids

A curated list of preprints related to Gastruloids (in vitro models of early development obtained by 3D aggregation of embryonic cells). Updated until July 2021.

 



List by Paul Gerald L. Sanchez and Stefano Vianello

ASCB EMBO Annual Meeting 2019

A collection of preprints presented at the 2019 ASCB EMBO Meeting in Washington, DC (December 7-11)

 



List by Madhuja Samaddar et al.

EDBC Alicante 2019

Preprints presented at the European Developmental Biology Congress (EDBC) in Alicante, October 23-26 2019.

 



List by Sergio Menchero et al.

EMBL Seeing is Believing – Imaging the Molecular Processes of Life

Preprints discussed at the 2019 edition of Seeing is Believing, at EMBL Heidelberg from the 9th-12th October 2019

 



List by Dey Lab

SDB 78th Annual Meeting 2019

A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.

 



List by Alex Eve

Lung Disease and Regeneration

This preprint list compiles highlights from the field of lung biology.

 



List by Rob Hynds

Young Embryologist Network Conference 2019

Preprints presented at the Young Embryologist Network 2019 conference, 13 May, The Francis Crick Institute, London

 



List by Alex Eve

Pattern formation during development

The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.

 



List by Alexa Sadier

BSCB/BSDB Annual Meeting 2019

Preprints presented at the BSCB/BSDB Annual Meeting 2019

 



List by Dey Lab

Zebrafish immunology

A compilation of cutting-edge research that uses the zebrafish as a model system to elucidate novel immunological mechanisms in health and disease.

 



List by Shikha Nayar

Also in the evolutionary biology category:

‘In preprints’ from Development 2022-2023

A list of the preprints featured in Development's 'In preprints' articles between 2022-2023

 



List by Alex Eve, Katherine Brown

preLights peer support – preprints of interest

This is a preprint repository to organise the preprints and preLights covered through the 'preLights peer support' initiative.

 



List by preLights peer support

EMBO | EMBL Symposium: The organism and its environment

This preList contains preprints discussed during the 'EMBO | EMBL Symposium: The organism and its environment', organised at EMBL Heidelberg, Germany (May 2023).

 



List by Girish Kale

9th International Symposium on the Biology of Vertebrate Sex Determination

This preList contains preprints discussed during the 9th International Symposium on the Biology of Vertebrate Sex Determination. This conference was held in Kona, Hawaii from April 17th to 21st 2023.

 



List by Martin Estermann

EMBL Synthetic Morphogenesis: From Gene Circuits to Tissue Architecture (2021)

A list of preprints mentioned at the #EESmorphoG virtual meeting in 2021.

 



List by Alex Eve

Planar Cell Polarity – PCP

This preList contains preprints about the latest findings on Planar Cell Polarity (PCP) in various model organisms at the molecular, cellular and tissue levels.

 



List by Ana Dorrego-Rivas

TAGC 2020

Preprints recently presented at the virtual Allied Genetics Conference, April 22-26, 2020. #TAGC20

 



List by Maiko Kitaoka et al.

ECFG15 – Fungal biology

Preprints presented at 15th European Conference on Fungal Genetics 17-20 February 2020 Rome

 



List by Hiral Shah

COVID-19 / SARS-CoV-2 preprints

List of important preprints dealing with the ongoing coronavirus outbreak. See http://covidpreprints.com for additional resources and timeline, and https://connect.biorxiv.org/relate/content/181 for full list of bioRxiv and medRxiv preprints on this topic

 



List by Dey Lab, Zhang-He Goh

1

SDB 78th Annual Meeting 2019

A curation of the preprints presented at the SDB meeting in Boston, July 26-30 2019. The preList will be updated throughout the duration of the meeting.

 



List by Alex Eve

Pattern formation during development

The aim of this preList is to integrate results about the mechanisms that govern patterning during development, from genes implicated in the processes to theoritical models of pattern formation in nature.

 



List by Alexa Sadier
Close