Oikopleura dioica: An Emergent Chordate Model to Study the Impact of Gene Loss on the Evolution of the Mechanisms of Development

Abstract

The urochordate Oikopleura dioica is emerging as a nonclassical animal model in the field of evolutionary developmental biology (a.k.a. evo-devo) especially attractive for investigating the impact of gene loss on the evolution of mechanisms of development. This is because this organism fulfills the requirements of an animal model (i.e., has a simple and accessible morphology, a short generation time and life span, and affordable culture in the laboratory and amenable experimental manipulation), but also because O. dioica occupies a key phylogenetic position to understand the diversification and origin of our own phylum, the chordates. During its evolution, O. dioica genome has suffered a drastic process of compaction, becoming the smallest known chordate genome, a process that has been accompanied by exacerbating amount of gene losses. Interestingly, however, despite the extensive gene losses, including entire regulatory pathways essential for the embryonic development of other chordates, O. dioica retains the typical chordate body plan. This unexpected situation led to the formulation of the so-called inverse paradox of evo-devo, that is, when a genetic diversity is able to maintain a phenotypic unity. This chapter reviews the biological features of O. dioica as a model animal, along with the current data on the evolution of its genes and genome. We pay special attention to the numerous examples of gene losses that have taken place during the evolution of this unique animal model, which is helping us to understand to which the limits of evo-devo can be pushed off.

Massive Gene Loss and Function Shuffling in Appendicularians Stretch the Boundaries of Chordate Wnt Family Evolution

“…Gene loss, however, is not always adaptive, but in many occasions occurs under neutral conditions, as a consequence, for example, of a process of regressive evolution (reviewed in Albalat and Cañestro, 2016). Increase of mutational robustness or changes of environmental conditions can lead to an increase of the dispensability of certain genes, facilitating therefore selectively neutral gene loss without significant phenotypic impact (Albalat and Cañestro, 2016) as have been recently concluded after a comprehensive comparative genomic analysis across the metazoan tree of life (Fernández and Gabaldón, 2020). Gene losses have been frequently accompanied by events of function shuffling, in which paralogs or related gene families can co-opt redundant functions, and therefore increasing mutational robustness that can favor gene loss (McClintock et al, 2001;Cañestro et al, 2009).…”

“…This liberal pattern of evolution has been argued that might have contributed to the morphological diversification of tunicates ( Somorjai et al, 2018 ). In appendicularian tunicates, however, the evolution of the Wnt family remains unknown, and considering that these organisms are highly prone to lose genes ( Ferrández-Roldán et al, 2019 ) and other signaling pathways such as retinoic acid has been dismantled ( Martí-Solans et al, 2016 ), it appears as an attractive system to study the impact of gene loss and the limits of Wnt evolution in chordates.…”

Modular Evolution and Population Variability of Oikopleura dioica Metallothioneins

“…This species is emerging as a non-classical animal model in the field of evolutionary developmental biology (a.k.a. evo-devo) especially attractive for its unusually dynamic gene and genome evolution (reviewed in Ferrández-Roldán et al, 2019). At genome level, O. dioica has suffered numerous chromosomal rearrangements accompanied by a drastic process of compaction, becoming the smallest known chordate genome (Denoeud et al, 2010).…”

The filter‐house of the larvaceanOikopleura dioica. A complex extracellular architecture: From fiber production to rudimentary state to inflated house

“…Multicellular animals however, are unable to produce cellulose with a single exception: tunicates also called urochordates (Ferr andez-Rold an et al, 2019;Matthysse et al, 2004;Nakashima et al, 2004).…”

“…Multicellular animals however, are unable to produce cellulose with a single exception: tunicates also called urochordates (Ferrández‐Roldán et al, 2019; Matthysse et al, 2004; Nakashima et al, 2004). The last common ancestor of this group of approximately 3000 marine invertebrate species evolved a cellulose synthase enzyme, probably through lateral gene transfer from a bacterium (Sagane et al, 2010).…”