Molecular evidence of anteroposterior patterning in adult echinoderms

• Why I chose this preprint:

There are three main reasons to consider this paper as disruptive in the evolutionary biology field. Firstly, because of its novelty; spatial transcriptomics is a cutting-edge technology, which is finally reaching evolutionary biology to empower its research. Secondly, because this -omics data, at the same time, overthrows current theories about patterning in echinoderms and leaves the door open for a new paradigm in echinoderm body plan evolution. And last, but not least, due to the thought-provoking head-like theory. The segregation of posterior markers to the mesoderm, and anterior markers to the ectoderm is fascinating, although not unique. The separation between both anterior and posterior gene regulatory networks could have opened up doors for body plan evolution.

• Background:

Living beings are extremely diverse, so to understand their evolutionary relationships, evolutionary developmental biologists have classified them by key features such as the order of appearance of mouth-anus (protostome/deuterostome) or the existence of bilateral symmetry (Cavalier-Smith, 2004). Although echinoderms, like sea urchins and starfish, display a non-bilateral pentaradial symmetry, they are included in the Bilateria clade. The reason behind this allocation is hidden in its larval development.

After gastrulation, the feeding larvae display a bilateral symmetry with several paired arms. However, subsequent metamorphosis leads to a reabsorption of anterior structures into a stacked shape with five not-paired rays (McEdward & Janies, 1993). From a developmental point of view, these early processes have been proven to be shared by sister group hemichordates and chordates. The gastrulation and early patterning of echinoderm bilaterian larvae are guided by Wnt, chordin and BMPs signalling – common pathways for all deuterostomes (Hinman & Burke, 2018; Holland & Anderson, 2015). However, after metamorphosis, the bilateral symmetry must be remodelled into radial symmetry, and the role of patterning genes in this process or even in the metamorphosed adult echinoderm remains a mystery (Figure 1a, b).

In order to explore the expression of these patterning genes in the larvae, the adult, and during metamorphosis, it is key to understand the evolution of radial echinoderms from a bilateral ancestor.  Over time, several hypotheses have been proposed to explain adult divergence: bifurcation, circularization, duplication, and stacking (Adachi et al., 2018; Byrne et al., 2016; Luttrell et al., 2012; Peterson et al., 2000; Popodi, E., Andrews, M., & Raff, 1994; Rozhnov & Rozhnov, 2014; Smith, 2008). Bifurcation and circularization have been cast aside due to inconsistency with molecular data. However, duplication and stacking are still under consideration. In the duplication hypothesis (Byrne et al., 2016; Popodi, E., Andrews, M., & Raff, 1994), each of the five echinoderm rays is a copy of the ancestral AP axis, with the anterior ray displaying anterior markers and vice-versa for the posterior ray. In the stacking hypothesis (Adachi et al., 2018; Peterson et al., 2000; Smith, 2008), the oral-aboral axis of adult echinoderms is homologous to the bilaterian AP axis. Thus, the oral part would express anterior markers and the aboral posterior markers; or vice-versa. This hypothesis has been supported by Hox gene expression of the posterior mesoderm. However, broad bilaterian comparisons are normally based on ectodermal expression domains, as the authors of this preprint highlight.

Figure 1: Deployment of the antero-posterior patterning system in deuterostomes. a, Expression map of the conserved transcription factors and signalling ligands involved in ectoderm patterning along the AP axis, as observed in the hemichordate S. kowalveskii. b, Previous work in chordates and hemichordates has demonstrated extensive regulatory conservation in ectodermal AP patterning, establishing the ancestral regulatory characteristics of early deuterostomes. How this system is deployed in echinoderms remains unclear. c, Four hypotheses have been proposed for the deployment of the AP patterning system in establishing the echinoderm adult body plan: bifurcation, circularization, duplication and stacking. Extracted from Figure 1 (Formery et al., 2023).

• Key findings:

The co-opted medio-lateral patterning. Antero-posterior patterning genes, which are responsible for regionalisation across deuterostomes, are expressed in an unexpected manner in echinoderm ectoderm. The markers defining anterior in deuterostomes are expressed in the midline of each array, while those marking posterior are expressed in the most lateral regions. The characterisation of evolutionary co-opted medio-lateral patterning is the major advancement  described in this preprint (Figure 2).

Figure 2: Ambulacral-anterior model of echinoderm body plan evolution. a, Expression map of the conserved transcription factors and signalling ligands involved in ambulacral ectoderm patterning in P. miniata and organized from the midline of the ambulacrum (left) towards the interambulacrum (right). b, Diagram of the ambulacral-anterior model in a generalized asteroid with a cross-section through one of the arms. Only genes expressed in the ectoderm are shown. Extracted from Figure 4 (Formery et al., 2023).

Overthrown of current theories. These medial-lateral expression patterns do not match any of the mechanistical hypotheses out there (Formery et al., 2023). Thus, this finding overthrows all current theories about how echinoderm pentaradial symmetry evolved and leaves the door open for speculation.

Lack of trunk genetic markers on echinoderm ectoderm. In the echinoderm mesoderm, HOX genes are expressed in a stacked manner: anterior markers (Hox1-3) are expressed closer to the mouth and posterior genes (Hox11/13) closer to the anus. This patterning model favoured the stacked hypothesis, but now it conflicts with ectoderm expression, which displays a latero-medial expression of anterior (“head”) deuterostome markers. Thus, the mesoderm displays a “trunk” stacked patterning and the ectoderm shows a “head” latero-medial patterning.

Figure 3: Antero-posterior organization of anatomical elements at postmetamorphic stages (Mouth-anus distributed). Hox gene assignments in square brackets represent complementary data from other taxa. Vertical purple arrows represent the somatocoelar hox vectors. Other anatomical elements are indicated in the left scheme. Adapted from David & Mooi, 2014.

The authors of this preprint don’t dwell on this controversy, but they do highlight the concept of “head-like” animals. For Formery and co-authors, this “head-like” [sic] model is a sign of uncoupling between posterior and anterior programs, which seems  common in other Echinodermata and Hemichordata (Lacalli, 2014). The decoupling between both tissues, quite unusual for chordates, could have allowed more evolutionary flexibility and could have driven its body plan evolution.

Transcriptomic tool. This article provides an extense transcriptomic resource for the community to consult markers and discuss about a new theory about echinoderm body plan evolution. A valuable contribution to open access science.

 

• Future directions and questions for the authors (Answers below, at Author’s response)

What new theory is shaped by this data? Could you propose a new paradigm explaining pentaradial symmetry? Can the stacking theory still be plausible for mesoderm, but a new theory might be needed for ectoderm?

What are the patterning differences between larvae and adults? Is echinoderm adult patterning an exacerbation of the differences between echinoderm larvae and hemichordate?

Some of these antero-posterior genes (such as hedgehog, nkx2.1) are dorso-ventral in vertebrates. Did you already observe a different patterning in these vertebrate dorso-ventral genes? Is there a dorso-ventral patterning in echinoderms?

 

• Bibliography.

 Adachi, S., Niimi, I., Sakai, Y., Sato, F., Minokawa, T., Urata, M., Sehara-Fujisawa, A., Kobayashi, I., & Yamaguchi, M. (2018). Anteroposterior molecular registries in ectoderm of the echinus rudiment. Developmental Dynamics : An Official Publication of the American Association of Anatomists, 247(12), 1297–1307. https://doi.org/10.1002/DVDY.24686

Byrne, M., Martinez, P., & Morris, V. (2016). Evolution of a pentameral body plan was not linked to translocation of anterior Hox genes: the echinoderm HOX cluster revisited. Evolution & Development, 18(2), 137–143. https://doi.org/10.1111/EDE.12172

Cavalier-Smith, T. (2004). Only six kingdoms of life. Proceedings of the Royal Society B: Biological Sciences, 271(1545), 1251. https://doi.org/10.1098/RSPB.2004.2705

David, B., & Mooi, R. (2014). How Hox genes can shed light on the place of echinoderms among the deuterostomes. EvoDevo, 5(1), 1–19. https://doi.org/10.1186/2041-9139-5-22/FIGURES/6

Formery, L., Peluso, P., Kohnle, I., Malnick, J., Pitel, M., Uhlinger, K. R., Rokhsar, D. S., Rank, D. R., & Lowe, C. J. (2023). Molecular evidence of anteroposterior patterning in adult echinoderms. BioRxiv, 2023.02.05.527185. https://doi.org/10.1101/2023.02.05.527185

Hinman, V. F., & Burke, R. D. (2018). Embryonic neurogenesis in echinoderms. Wiley Interdisciplinary Reviews: Developmental Biology, 7(4), e316. https://doi.org/10.1002/WDEV.316

Holland, L. Z., & Anderson, P. A. V. (2015). Evolution of basal deuterostome nervous systems. Journal of Experimental Biology, 218(4), 637–645. https://doi.org/10.1242/JEB.109108

Lacalli, T. (2014). Echinoderm conundrums: Hox genes, heterochrony, and an excess of mouths. EvoDevo, 5(1), 1–4. https://doi.org/10.1186/2041-9139-5-46/FIGURES/1

Luttrell, S., Konikoff, C., Byrne, A., Bengtsson, B., & Swalla, B. J. (2012). Ptychoderid Hemichordate Neurulation without a Notochord. Integrative and Comparative Biology, 52(6), 829–834. https://doi.org/10.1093/ICB/ICS117

McEdward, L. R., & Janies, D. A. (1993). Life Cycle Evolution in Asteroids: What is a Larva? Https://Doi.Org/10.2307/1542444, 184(3), 255–268. https://doi.org/10.2307/1542444

Peterson, K. J., Arenas-Mena, C., & Davidson, E. H. (2000). The A/P axis in echinoderm ontogeny and evolution: evidence from fossils and molecules. Evolution & Development, 2(2), 93–101. https://doi.org/10.1046/J.1525-142X.2000.00042.X

Popodi, E., Andrews, M., & Raff, R. A. (1994). Evolution of body plans: using homeobox genes to examine the development of the radial CNS of echinoderms. Developmental Biology, 163, 540.

Rozhnov, S. V., & Rozhnov, S. V. (2014). Symmetry of echinoderms: From initial bilaterally-asymmetric metamerism to pentaradiality. Natural Science, 6(4), 171–183. https://doi.org/10.4236/NS.2014.64021

Smith, A. B. (2008). Deuterostomes in a twist: the origins of a radical new body plan. Evolution & Development, 10(4), 493–503. https://doi.org/10.1111/J.1525-142X.2008.00260.X

 

 

Tags: ambulacra, echinoderms, evolution, omics, patterning, spatialomics

Posted on: 3 May 2023

doi: https://doi.org/10.1242/prelights.34443

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