Sea cucumbers: an emerging system in evo-devo

Abstract

A challenge for evolutionary developmental (evo-devo) biology is to expand the breadth of research organisms used to investigate how animal diversity has evolved through changes in embryonic development. New experimental systems should couple a relevant phylogenetic position with available molecular tools and genomic resources. As a phylum of the sister group to chordates, echinoderms extensively contributed to our knowledge of embryonic patterning, organ development and cell-type evolution. Echinoderms display a variety of larval forms with diverse shapes, making them a suitable group to compare the evolution of embryonic developmental strategies. However, because of the laboratory accessibility and the already available techniques, most studies focus on sea urchins and sea stars mainly. As a comparative approach, the field would benefit from including information on other members of this group, like the sea cucumbers (holothuroids), for which little is known on the molecular basis of their development. Here, we review the spawning and culture methods, the available morphological and molecular information, and the current state of genomic and transcriptomic resources on sea cucumbers. With the goal of making this system accessible to the broader community, we discuss how sea cucumber embryos and larvae can be a powerful system to address the open questions in evo-devo, including understanding the origins of bilaterian structures.

Larval development of Holothuria tubulosa, a new tractable system for evo-devo

“…We next characterized embryonic and larval development using light and confocal microscopy. As previously reported, the first embryonic divisions give rise to 2 equal blastomeres 2 hours after fertilization (hpf) and 4 blastomeres 3 hpf (Rakaj et al, 2018;Perillo et al, 2024) (Figures 1L, M). Blastulae (12 hpf) are round and F-actin staining showed polarization of ectodermal cells, with apical polarity opposite to the blastocoel (Figure 2A).…”

“…In a recent review paper (Perillo et al, 2024), we have thoroughly discussed how sea cucumber embryos and larvae can be valuable systems to address the open questions in evo-devo, including understanding the origins of bilaterian structures. Among sea cucumbers, developmental and evo-devo studies have relied almost exclusively on A. parvimensis from the US Pacific Coast and A. japonicus from Asia (Pacific Ocean), both species belonging to the same genus Apostichopus (Clark, 1913;Yang et al, 2015).…”

“…A bottleneck that prevented the use of these animals in the laboratory has been lack of methods to obtain embryonic cultures without depending on natural spawning (Perillo et al, 2024) and difficulty of having a species locally available. We addressed this challenge with our microsurgery method that enables the extraction of small pieces of gonads from H. tubulosa by making a cut along the anterior ventral-left side of the animals.…”

“…Adult sea cucumbers are also studied for their incredible regenerative capacities (Garcıá-Arraraś et al, 1999;Mashanov and Garcıá-Arraraś, 2011). While there is an increasing number of studies exploring the biology and aquaculture use of adult sea cucumbers (Perillo et al, 2024), the molecular basis of their embryonic and larval development are poorly investigated beyond two Pacific species, Apostichopus japonicus and Apostichopus parvimensis (Perillo et al, 2024). With the goal of identifying an experimentally tractable sea cucumber model in Europe, we established Holothuria tubulosa (Gmelin, 1788) for cell and developmental biology.…”