Journal Article

The mid-developmental transition and the evolution of animal body plans

Martindale, Mark Q., Winter, Eitan, Hashimshony, Tamar, Anavy, Leon, Khair, Sally, Yaniv, Karina, Arendt, Detlev, Senderovich, Naftalie, Jerafi-Vider, Ayelet, Degnan, Sandie M., Kovalev, Ekaterina, Liu, Shang-Yun, Levin, Michal, Rink, Jochen C., Mostov, Natalia, Silver, David H., Simmons, David, Yanai, Itai, Ryan, Joseph F., Cole, Alison G., Larsson, Tomas, Fernandez-Valverde, Selene L., Degnan, Bernard M., Nakanishi, Nagayasu, Feder, Martin, Simakov, Oleg

2016

Overview

Embryos in a particular phylum of the animal kingdom tend to most resemble one another at a stage in the middle of embryogenesis known as the phylotypic period; a transcriptional analysis of embryogenesis from single embryos of ten different phyla reveals that the transcripts expressed at the phylotypic stage (or mid-developmental transition) differ greatly between phyla, and a ‘phylum’ may be defined as a set of species sharing the same signals and transcription factor networks during the mid-developmental transition. Stage set for defining a phylum Embryos in a particular phylum tend to resemble one another closely at some point in the middle of embryogeny. This is known as the phylotypic stage, and it has been established that embryos at this stage tend to express a conserved set of genes that are evolutionarily older than the genes expressed before and after. This, however, only applies within a phylum, as Yanai and colleagues demonstrate in an analysis of transcriptomes from individual embryos of ten disparate phyla. Considered across the whole animal kingdom, the transcripts expressed at the phylotypic stage differ greatly between phyla and could be said to define the characters of a particular phylum. This work also provides an operational definition for a phylum as a set of species — with a common ancestor — that share the same molecular mechanisms at the phylotypic stage. Animals are grouped into ~35 ‘phyla’ based upon the notion of distinct body plans 1 , 2 , 3 , 4 . Morphological and molecular analyses have revealed that a stage in the middle of development—known as the phylotypic period—is conserved among species within some phyla 5 , 6 , 7 , 8 , 9 . Although these analyses provide evidence for their existence, phyla have also been criticized as lacking an objective definition, and consequently based on arbitrary groupings of animals 10 . Here we compare the developmental transcriptomes of ten species, each annotated to a different phylum, with a wide range of life histories and embryonic forms. We find that in all ten species, development comprises the coupling of early and late phases of conserved gene expression. These phases are linked by a divergent ‘mid-developmental transition’ that uses species-specific suites of signalling pathways and transcription factors. This mid-developmental transition overlaps with the phylotypic period that has been defined previously for three of the ten phyla, suggesting that transcriptional circuits and signalling mechanisms active during this transition are crucial for defining the phyletic body plan and that the mid-developmental transition may be used to define phylotypic periods in other phyla. Placing these observations alongside the reported conservation of mid-development within phyla, we propose that a phylum may be defined as a collection of species whose gene expression at the mid-developmental transition is both highly conserved among them, yet divergent relative to other species.

• Publisher: Nature Publishing Group UK,Nature Publishing Group
• Subject: 631/114/2114 / 631/136/2086 / 631/181/2806 / Animals / Body Patterning - genetics / Cell cycle / Conserved Sequence - genetics / Developmental biology / Embryonic development / Embryonic Development - genetics / Embryos / Evolution, Molecular / Gene expression / Gene Expression Regulation, Developmental / Gene Regulatory Networks / Genes, Developmental - genetics / Humanities and Social Sciences / letter / Models, Biological / Morphology / Morphology (Animals) / multidisciplinary / Phenotype / Phylogeny / Science / Species Specificity / Transcription factors / Transcriptome - genetics / Zoological research