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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

Preprint posted on February 06, 2022 https://www.biorxiv.org/content/10.1101/2022.02.05.479245v1

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).

 

Posted on: 10th March 2022

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

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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.

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