Developmental diversity in free-living flatworms

Abstract

Flatworm embryology has attracted attention since the early beginnings of comparative evolutionary biology. Considered for a long time the most basal bilaterians, the Platyhelminthes (excluding Acoelomorpha) are now robustly placed within the Spiralia. Despite having lost their relevance to explain the transition from radially to bilaterally symmetrical animals, the study of flatworm embryology is still of great importance to understand the diversification of bilaterians and of developmental mechanisms. Flatworms are acoelomate organisms generally with a simple centralized nervous system, a blind gut, and lacking a circulatory organ, a skeleton and a respiratory system other than the epidermis. Regeneration and asexual reproduction, based on a totipotent neoblast stem cell system, are broadly present among different groups of flatworms. While some more basally branching groups - such as polyclad flatworms - retain the ancestral quartet spiral cleavage pattern, most flatworms have significantly diverged from this pattern and exhibit unique strategies to specify the common adult body plan. Most free-living flatworms (i.e. Platyhelminthes excluding the parasitic Neodermata) are directly developing, whereas in polyclads, also indirect developers with an intermediate free-living larval stage and subsequent metamorphosis are found. A comparative study of developmental diversity may help understanding major questions in evolutionary biology, such as the evolution of cleavage patterns, gastrulation and axial specification, the evolution of larval types, and the diversification and specialization of organ systems. In this review, we present a thorough overview of the embryonic development of the different groups of free-living (turbellarian) platyhelminths, including the Catenulida, Macrostomorpha, Polycladida, Lecithoepitheliata, Proseriata, Bothrioplanida, Rhabdocoela, Fecampiida, Prolecithophora and Tricladida, and discuss their main features under a consensus phylogeny of the phylum.

Reconsidering regeneration in metazoans: an evo-devo approach

“…Recent phylogenetic work suggests this order is relatively late branching within the phylum as a whole, forming a clade with Bothrioplanida, and Neodermata united by a lack of spiral cleavage and centrosomes (Egger et al, 2015;Laumer et al, 2015), suggesting its derived nature. Neoblasts, however, and regenerative capabilities in general are also present in the more basally branching orders Macrostomorpha and Catenulida (Dirks et al, 2012;Martín-Durán and Egger, 2012). Egger and co-workers note that most flatworm taxa lack the ability to regenerate brain, eyes, pharynx and statocyst (Egger et al, 2007).…”

Ins and outs of Spiralian gastrulation

“…For example, ectolecithal development is common, in which yolk is extraembryonic, and must be incorporated into cells later in development (Martín-Durán and Egger, 2012). In some platyhelminth species, vegetally-derived "hull" cells envelop the embryo primordium by a process of reverse epiboly (Willems et al, 2009).…”

“…Likewise, this fate map framework allows one to identify differences in both the cellular and molecular (GRN) basis of specific gastrulation behaviors. Because gastrulation often results in the establishment of the alimentary canal, we can correlate variation in gastrulation types with life history modes, such as direct vs. indirect development, or planktotrophic vs. lecithotrophic larval forms (Kato, 1968;Anderson, 1973;Singley, 1977;Arenas-Mena, 2010;Martín-Durán and Egger, 2012;Arenas-Mena, 2014, this issue). Answers to these questions will provide the necessary information about gastrulation diversity in spiralians needed for making comparisons with other metazoans.…”

“…Gastrulation has undoubtedly undergone significant modification in extant species relative to the metazoan common ancestor; gastrulation is highly influenced by life history, and trophic, strategies (Anderson, 1973;Arendt and Nübler-Jung, 1999;Martín-Durán and Egger, 2012;ArenasMena, 2014, this volume). Adaptation played a role in generating the wide range of gastrulation modes found between extant taxa (Byrum and Martindale, 2004;Gerberding and Patel, 2004;Chea et al, 2005;Hejnol and Martindale, 2009).…”

“…Gastrulation also holds a pivotal role in evolutionary theories about the emergence and divergence of bilaterian body-plans (Arendt and Nübler-Jung,1997;Nielsen, 2001;Martindale and Hejnol, 2009 As evo-devo questions go, tracing the evolutionary history of gastrulation is particularly difficult, because the complex morphogenetic and fate specification events involved make gastrulation an emergent property of development. Gastrulation has undoubtedly undergone significant modification in extant species relative to the metazoan common ancestor; gastrulation is highly influenced by life history, and trophic, strategies (Anderson, 1973;Arendt and Nübler-Jung, 1999;Martín-Durán and Egger, 2012; ArenasMena, 2014, this volume). Adaptation played a role in generating the wide range of gastrulation modes found between extant taxa (Byrum and Martindale, 2004;Gerberding and Patel, 2004;Chea et al, 2005;Hejnol and Martindale, 2009).…”