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Comparative Transcriptome Analysis Reveals Vertebrate Phylotypic Period During Organogenesis

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Comparative Transcriptome Analysis Reveals Vertebrate Phylotypic Period During Organogenesis ARTICLE Received 11 Nov 2010 | Accepted 21 Feb 2011 | Published 22 Mar 2011 DOI: 10.1038/ncomms1248 Comparative transcriptome analysis reveals vertebrate phylotypic period during organogenesis Naoki Irie1 & Shigeru Kuratani1 One of the central issues in evolutionary developmental biology is how we can formulate the relationships between evolutionary and developmental processes. Two major models have been proposed: the ‘funnel-like’ model, in which the earliest embryo shows the most conserved morphological pattern, followed by diversifying later stages, and the ‘hourglass’ model, in which constraints are imposed to conserve organogenesis stages, which is called the phylotypic period. Here we perform a quantitative comparative transcriptome analysis of several model vertebrate embryos and show that the pharyngula stage is most conserved, whereas earlier and later stages are rather divergent. These results allow us to predict approximate developmental timetables between different species, and indicate that pharyngula embryos have the most conserved gene expression profiles, which may be the source of the basic body plan of vertebrates. 1 Laboratory for Evolutionary Morphology, RIKEN Center for Developmental Biology, 2-2-3 Minatojima-minami, Chuo-ku, Kobe, Hyogo 650-0047, Japan. Correspondence and requests for materials should be addressed to N.I. (email: [email protected]). NATURE COMMUNICATIONS | 2:248 | DOI: 10.1038/ncomms1248 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. ARTICLE NatUre cOMMUNicatiONS | DOI: 10.1038/ncomms1248 he relationship between ontogeny and phylogeny has long been an intriguing question in comparative and evolution- Tary embryology1. Biogenetic law of Ernst Haeckel assumed a parallelism between ontogeny and phylogeny, and asserted that embryogenesis is a recapitulation of ancient organisms because all animals start their existence from a one-celled stage and develop into morula, blastula and then gastrula stages2,3. Although it is now widely accepted that embryogenesis cannot simply be a repetition of evolution, none of the alternative formulations has reached a con- Hox sensus, even with contemporary evolutionary developmental (‘evo- devo’) theories2. For example, we still do not know how to explain the common early embryonic stages, such as the morula, blastula and gastrula, in evolutionary terms. Is this because earlier stages of embryogenesis tend to be more evolutionarily conserved? One of the major controversies, which are limiting the formulation of an evolutionary model of embryogenesis, is whether the earliest or organogenesis phase of the embryonic period is more resistant to Funnel-like model Hourglass model evolutionary change and, hence, more conserved among vertebrate embryos (Fig. 1). Early ity Haeckel’s biogenetic law has been rehashed and can now be sum- ity marized as the concept that the highest conservation occurs at the earliest stage of embryogenesis4–7, which is the funnel-like model Mid (Fig. 1a). Theoretical studies support this model by arguing that mutations or perturbations, which affect earlier stages in develop- iptome similar ment, should be more likely to have widespread downstream effects, iptome similar Late such as embryonic lethality, which are more difficult to be inher- anscr 4–7 anscr ited . In addition, molecular studies have suggested the existence Tr Tr of strong genomic constraints at the early stages of embryogenesis by showing the sequence conservation of genes, which are expressed Early Mid Late Early Mid Late during such phases8,9. Karl von Baer proposed a different idea that the highest morpho- Figure 1 | The two major hypotheses about how developmental logical similarities can be found during mid-embryonic or organo- processes are conserved against evolutionary changes. In both models, genesis stages, such as the pharyngula stage10. Re-examination of embryogenesis proceeds from the bottom to the top, and the width this idea in terms of the morphological divergence in early embry- represents the phylogenetic diversity of developmental processes, ogenesis, such as variations in cleavage, germ layer formation or which are deduced from morphological similarities. (a) The funnel-like gastrulation, has led to the development of the ‘egg-timer’11 and model predicts conservation at the earliest embryonic stage. During ‘hourglass’ models11,12 (Fig. 1b). Two hypotheses have been proposed embryogenesis, diversity increases additively and progressively. This model to provide a rationale for the conservation of mid-embryonic stages. is based upon the extreme case of developmental burden or generative One is that the spatial and temporal colinearity of the Hox gene clus- entrenchment, in which the viability of any developmental feature depends ter constrains the mid-embryonic stage; therefore, morphological on an earlier one (arrows). (b) The hourglass model predicts conservation diversification at this stage is unlikely11. Another hypothesis focuses of the organogenesis stage. Circles beside the model indicate inductive on the peculiar modularity of developmental programs during mid- general features of signals observed during each stage. During this stage, embryogenesis. Specifically, it proposes that intricate networks of a highly intricate signalling network is established consisting of inductive both global and local inductive signals12 during these stages make signals, including the Hox genes11, which leads to conservation of the the development of different organ primordia highly interdepend- animal body plan12. Figure 1b was adapted with permission from 11 and 12. ent. As a result, any change in the developmental events during (c) Hypothetical data supporting the funnel-like (left) and hourglass (right) these stages would increase the risk of mortality, and therefore, lead models. For both examples, the transcriptome data of M. musculus embryos to evolutionary conservation by eliminating such changes. (early, middle and late stages) were compared with X. laevis embryos An important prediction of the hourglass model is the establish- (early, middle and late stages) in an all-to-all manner. The data, which ment of a ‘phylotypic progression’ or ‘phylotype’ in the mid-embry- are consistent with the funnel-like model, show that the transcriptome onic stages11–15. The phylotypic progression (or period) imposes similarity is highest in the early versus early comparison (shaded point on constraints on morphological diversification; thereafter, it becomes the blue line; left). Data that are consistent with the hourglass model show the source of the basic body plan for each individual major taxon (or that the transcriptome similarity is highest in the middle versus middle phylum). Some researchers have expanded the phylotype to include comparison (right). protostomes, calling it the ‘zootype’16 because similar expression patterns of Hox genes can be found among these organisms. Distinguishing between these two models of conservation during embryogenesis is important to explain how the basic body morphological elements, such as those seen in early embryos, plan of vertebrates develops in an evo-devo context. The vertebrate because this model predicts that the greatest morphological simi- body plan, which includes an overt head, trunk with segmented larity occurs at the earliest developmental stage. vertebrae and a segmented pharynx, is defined as a set of shared Owing to the difficulty in evaluating evolutionary distances morphological traits of adult vertebrates and is assumed to originate between embryos of different species quantitatively, the identification from a conserved pattern of embryogenesis. However, if the ‘funnel- of the most conserved embryonic stage remains controversial8,9,17–21. like’ model were held true, then this assumption would need to be For example, there does not seem to be any consensus about how reconsidered. In this case, it should be possible to distill the mor- the difference between qualitatively different morphological traits, phological elements of the vertebrate body plan into even simpler such as somites, pharyngeal arches and cleavage patterns, should be NatUre cOMMUNicatiONS | 2:248 | DOI: 10.1038/ncomms1248 | www.nature.com/naturecommunications © 2011 Macmillan Publishers Limited. All rights reserved. NatUre cOMMUNicatiONS | DOI: 10.1038/ncomms1248 ARTICLE 1.0 1.0 1.0 Mm–Gg Mm–XI Mm–Dr E1.5 E8.5 E14.5 ρ 0.8 10954 0.8 6317 0.8 5773 E2.5 E9.5 0.6 0.6 0.6 E16.5 M. musculus E3.5 E10.5 0.4 0.4 0.4 man coefficient E18.5 0.2 0.2 0.2 E7.5 E12.5 Spear 0 0 0 1.0 1.0 1.0 HH27 Gg–Mm Gg–XI Gg–Dr HH1 HH11 ρ 5447 HH2 0.8 10954 0.8 0.8 4922 HH14 HH32 HH4 0.6 0.6 0.6 HH6 HH16 G. gallus HH34 0.4 0.4 0.4 man coefficient HH8 HH19 0.2 0.2 0.2 HH38 Spear HH9 HH24 0 0 0 1.0 1.0 1.0 XI–Mm Xl–Gg XI–Dr 2 19 ρ 31 0.8 6317 0.8 5447 0.8 3608 5 21 0.6 0.6 0.6 9 37 23 X. laevis 11 0.4 0.4 0.4 26 43 man coefficient 13 0.2 0.2 0.2 17 28 Spear 48 0 0 0 1.0 1.0 1.0 Dr–Mm Dr–Gg Dr–XI 1 Cell 10 h ρ 32 h 0.8 5773 0.8 4922 0.8 3608 Shield 12 h 48 h 0.6 0.6 0.6 75% D. rerio 0.4 0.4 0.4 Epiboly 16 h 4 day man coefficient 0.2 0.2 0.2 9 h 24 h 5 day Spear 0 0 0 Figure 2 | Transcriptome similarities of different embryos. Spearman correlation coefficients ρ( ) of the transcriptome data from pairs of embryos from different species at different developmental stages. Higher ρ values indicate higher transcriptome similarity. The sampled stages are shown on the left. Different coloured lines indicate different developmental stages. For example, in the chart for the Dr–Xl comparison, the left end of the blue line indicates the Spearman correlation coefficients of a one-cell D. rerio embryo and a stage two X. laevis embryo. As the comparison proceeds to later developmental stages of X.
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