On 2016 Mar 15, Lionel Christiaen commented:
In this article, the author presents an extensive account of the extreme diversity of adult anatomies and life histories encountered across the thousands of tunicate species that roam the oceans worldwide, and occupy multitudes of ecological niches. The author then emphasizes that tunicate genomes are markedly more compact and evolve faster than the genomes of their chordate relatives, the cephalochordates and vertebrates. Several recent studies support this notion, and the argument that rapid genome diversification may have fostered tunicate evolution is reasonable. Since the early development of tunicates, in particular ascidians, has been considerably simplified and streamlined in a manner analogous to what is observed in nematodes, the author argues that tunicates must have lost most ancestral genomic, developmental and anatomical features that could inform reconstruction of the evolutionary history of vertebrate traits. We wish to provide alternative interpretations and propose a more inclusive approach to the problems posed by tunicates in building models for the evolution of vertebrates. First, the argument about faster evolutionary rates implies that every part of the genome evolves at similarly faster rates; yet, phylogenomic analyses of concatenated coding sequences unequivocally revealed that tunicates and vertebrates form a monophyletic group referred to as olfactores [1, 2]. Moreover, conserved anatomical features including the notochord, the dorsal neural tube and the pharyngeal gill slits depend upon ancestral regulatory inputs from conserved transcription factors, as noted by the author. These simple examples argue against a complete relaxation of evolutionary constraints on ancestral features in tunicates, especially in ascidians. In other words, high average rates of sequence evolution and profound morphological changes are not incompatible with deep conservation of cellular and molecular mechanisms for embryonic patterning and cell fate specification. Instead, the apparent incompatibility between high rates of genome divergence and the maintenance of ancestral olfactores features over long evolutionary distances hints at the notion of developmental system drift (DSD), whereby mechanistically connected developmental features may be conserved between distantly related species exhibiting extensive divergence of the intervening processes [3]. Ascidians provide an attractive test-bed to study DSD since their early embryos have barely changed in almost half a billion years, despite considerable genomic divergence [4]. This is a lively area of research as illustrated by the 11 tunicate genomes recently made openly available to the worldwide research community [4-6]. We argue that comparative developmental studies are poised to identify additional features conserved between tunicates and vertebrates, such as those recently reported for the neural crest, the cranial placodes and the cardiopharyngeal mesoderm [7-10]. These "islands of conservation" will continue to shed light on the mechanisms of tunicate diversification and the deep evolutionary origins of the vertebrate body plan.
REFERENCES
1. Delsuc, F., Brinkmann, H., Chourrout, D., and Philippe, H. (2006). Tunicates and not cephalochordates are the closest living relatives of vertebrates. Nature 439, 965-968.
2. Putnam, N.H., Butts, T., Ferrier, D.E., Furlong, R.F., Hellsten, U., Kawashima, T., Robinson-Rechavi, M., Shoguchi, E., Terry, A., Yu, J.K., et al. (2008). The amphioxus genome and the evolution of the chordate karyotype. Nature 453, 1064-1071.
3. True, J.R., and Haag, E.S. (2001). Developmental system drift and flexibility in evolutionary trajectories. Evolution & development 3, 109-119.
4. Stolfi, A., Lowe, E.K., Racioppi, C., Ristoratore, F., Brown, C.T., Swalla, B.J., and Christiaen, L. (2014). Divergent mechanisms regulate conserved cardiopharyngeal development and gene expression in distantly related ascidians. eLife 3, e03728.
5. Voskoboynik, A., Neff, N.F., Sahoo, D., Newman, A.M., Pushkarev, D., Koh, W., Passarelli, B., Fan, H.C., Mantalas, G.L., Palmeri, K.J., et al. (2013). The genome sequence of the colonial chordate, Botryllus schlosseri. eLife 2, e00569.
6. Brozovic, M., Martin, C., Dantec, C., Dauga, D., Mendez, M., Simion, P., Percher, M., Laporte, B., Scornavacca, C., Di Gregorio, A., et al. (2016). ANISEED 2015: a digital framework for the comparative developmental biology of ascidians. Nucleic acids research 44, D808-818.
7. Abitua, P.B., Gainous, T.B., Kaczmarczyk, A.N., Winchell, C.J., Hudson, C., Kamata, K., Nakagawa, M., Tsuda, M., Kusakabe, T.G., and Levine, M. (2015). The pre-vertebrate origins of neurogenic placodes. Nature 524, 462-465.
8. Abitua, P.B., Wagner, E., Navarrete, I.A., and Levine, M. (2012). Identification of a rudimentary neural crest in a non-vertebrate chordate. Nature 492, 104-107.
9. Diogo, R., Kelly, R.G., Christiaen, L., Levine, M., Ziermann, J.M., Molnar, J.L., Noden, D.M., and Tzahor, E. (2015). A new heart for a new head in vertebrate cardiopharyngeal evolution. Nature 520, 466-473.
10. Stolfi, A., Ryan, K., Meinertzhagen, I.A., and Christiaen, L. (2015). Migratory neuronal progenitors arise from the neural plate borders in tunicates. Nature 527, 371-374.
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