How do environmental factors influence life cycles and development? An experimental framework for early-diverging metazoans

Abstract

Ecological developmental biology (eco-devo) explores the mechanistic relationships between the processes of individual development and environmental factors. Recent studies imply that some of these relationships have deep evolutionary origins, and may even pre-date the divergences of the simplest extant animals, including cnidarians and sponges. Development of these early diverging metazoans is often sensitive to environmental factors, and these interactions occur in the context of conserved signaling pathways and mechanisms of tissue homeostasis whose detailed molecular logic remain elusive. Efficient methods for transgenesis in cnidarians together with the ease of experimental manipulation in cnidarians and sponges make them ideal models for understanding causal relationships between environmental factors and developmental mechanisms. Here, we identify major questions at the interface between animal evolution and development and outline a road map for research aimed at identifying the mechanisms that link environmental factors to developmental mechanisms in early diverging metazoans. Also watch the Video Abstract.

Keywords: Cnidaria; corals; environmental genomics; holobiont; hydra; sponges; symbiosis.

Figure 1

Environmental stress has substantial impact on cnidarian life cycles. In Turritopsis nutricula, stress can reverse the development and make a medusa transforming into a polyp. A: Free-living healthy medusa. B: Stress-triggered transforming medusa. C: Balllike stage of transforming medusa. BrdU staining of replicating nuclei. D: Butterfly-shape remnant of adult medusa producing a hydrorhizal stolon characteristic of the polyp stage (black arrow). E: A newly formed polyp from reverse development of a medusa. Scale bars: A: 1 mm; B: 500 μm; C: 300 μm; D and E: 500 μm. Taken from Piraino et al. [14].

Figure 2

Phylogeny of basal metazoan animals. Two lineages, the phylogenetic position of which remains contentious (placozoans and ctenophores), have been omitted.

Figure 3

A: A single larva of Stylophora pistillata, about 5 h after release, right at the moment it first contacts a possible settlement surface. Larvae from Stylophora pistillata are typically pear-shaped and have a mean length of 1 mm (photo credit: Peter J Edmunds; http://www.eoearth.org/view/article/150659/). B: Pelmatohydra oligactis polyp. Polyps are up to 10 mm long. C: Female Pelmatohydra oligactis carrying several eggs. Gametogenesis is triggered by a temperature shift. D and E: Acropora clathrata at 5 m in a sheltered location (D), at 20 m in a high current location (E). Reproduced with permission from Zoe Richards. F and G: Typical morphotypes of Dysidea avara sponges from depth sites of 8.8 m (F) and 14.3 m (G); pictures from Mendola et al. [58]. H: Hydra vulgaris under normal culture conditions. I: Hydra vulgaris cultured in the absence of bacteria and infected by fungi.