The eventful history of nonembryonic development in tunicates

Abstract

Tunicates encompass a large group of marine filter‐feeding animals and more than half of them are able to reproduce asexually by a particular form of nonembryonic development (NED) generally called budding. The phylogeny of tunicates suggests that asexual reproduction is an evolutionarily plastic trait, a view that is further reinforced by the fact that budding mechanisms differ from one species to another, involving nonhomologous tissues and cells. In this review, we explore more than 150 years of literature to provide an overview of NED diversity and we present a comparative picture of budding tissues across tunicates. Based on the phylogenetic relationships between budding and nonbudding species, we hypothesize that NED diversity is the result of seven independent acquisitions and subsequent diversifications in the course of tunicate evolution. While this scenario represents the state‐of‐the‐art of our current knowledge, we point out gray areas that need to be further explored to refine our understanding of tunicate phylogeny and NED. Tunicates, with their plastic evolution and diversity of budding, represent an ideal playground for evolutionary developmental biologists to unravel the genetic and molecular mechanisms regulating nonembryonic development, as well as to better understand how such a profound innovation in life‐history has evolved in numerous metazoans.

Nuclear Receptors and Development of Marine Invertebrates

“…Juvenile polyps of Medusozoan cnidarians, for example, can undergo strobilation, leading to segmentation of the polyp into so-called ephyras, which will subsequently grow into adults [ 61 ]. Furthermore, several tunicate lineages independently gained the capacity for asexual reproduction using different budding strategies [ 62 , 63 ].…”

Evolution of animal coloniality and modularity: Emerging themes

“…His comparative study mainly focuses on benthic and sessile colonial animals because of the intrinsic functional differences with pelagic colonies (e.g., particular adaptations resulting from distinct susceptibilities to water currents among benthic and pelagic colonies). As a result, R. Strathmann raises many questions and hypotheses about the consequence of brooding, or in some cases not‐brooding, for the life history and reproduction of the different taxa (Strathmann, 2021, This issue)⁠.Unsatisfied with the all the attention given to genetic relatedness and inclusive fitness as major evolutionary drivers for the evolution of polymorphism in eusocial insects, C. Simpson—in the fourth article (research article)—develops a new theoretical framework to propose a new hypothesis that he terms the “life‐history ratchet.” The focus of this hypothesis is placed on the evolution of new body types (i.e., polymorph types) as a way to release colonies from ancestral life history strategy constraints, generated by the reduced numbers of body types. Mechanisms of colonial development Dias et al (2021, This issue)⁠ (research article) contribute with an elegant ecological study and experimental transplantation in a marina; they document phenotypic responses of bryozoan colonies to heteregeneous environments that affect overall morphology of the colonies, as well as the composition of polymorphic zooids in the colony, demonstrating a trade‐off between clonal growth and defense (density of avicularia).By comparing developmental mechanisms of budding, Alié et al (2021, This issue)⁠ (review) do a superb job to highlight the different cells and tissues that have been coopted in budding in the different groups of ascidians, suggesting a highly plastic nature of cell and tissues in this phylum. They raise the importance of tunicate diverse mechanisms of budding, as a goldmine to study evolutionary plastic developmental traits.By using positive selection tests on orthologous genes, followed by independent gene tree analyses, using several transcriptomes of entoprocts, bryozoans, and phoronids, Santagata (2021, This issue)⁠ (research article) identifies a pool of genes potentially related to the convergent evolution of coloniality among entoprocts and bryozoans, and probably also the “colonial‐like” (highly aggregate) phoronids. Signaling in colony regeneration and patterning In a laboratory experimental setting, Luz et al (2021, This issue)⁠ (research article) report predominant effects of fragment size in the process of regeneration in a group of invasive colonial dendrophylliid corals and show that Wnt and FGF—signaling pathways known to function in regeneration—are expressed during whole‐body regeneration in Tubastraea coccinea , a calcified anthozoan species fostered by the authors as a laboratory model.Cartwright et al (2021, This issue)⁠ (review) review variation and plasticity of colony forms in the hydrozoans and hypothesize that Wnt signaling may play an important role in colony patterning and morphology. From unicellular to multicellular colonies Cellular behaviors and developmental mechanisms that regulate the formation of colonies in aggregative bacteria have evolved multiple times.…”

The Diversity of Muscles and Their Regenerative Potential across Animals

“…While solitary tunicates reproduce strictly sexually and have limited regenerative capabilities, colonial species can also reproduce asexually and regenerate an entire body via diverse modes of budding, also referred to as non-embryonic development. The result is often a colony of connected, genetically identical zooids [ 160 , 161 ]. Budding can be part of the life cycle, which accounts for colony growth, replication and reproduction, or regeneration, i.e., passive forms triggered by injury [ 162 ].…”

“…The blastozooid, the adult produced by non-embryonic development, generally has a bauplan and a muscle architecture that is comparable to the oozooids, i.e., the individuals formed by embryonic development [ 165 , 174 ]. However, budding bypass fertilization, embryogenesis, larval stage, and metamorphosis [ 24 , 160 , 171 ]. Contrary to their embryonic development, which displays a remarkable level of conservation among almost all the tunicate orders, non-embryonic development encompasses a clade-specific assortment of cells, tissues, and ontogenesis, all displaying different degrees of interaction between epithelial and mesenchymal cells [ 161 ].…”