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Evodevo
2018 Jan 31;9:7. doi: 10.1186/s13227-018-0095-0.
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Embryonic lethality is not sufficient to explain hourglass-like conservation of vertebrate embryos.
Uchida Y
,
Uesaka M
,
Yamamoto T
,
Takeda H
,
Irie N
.
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Background: Understanding the general trends in developmental changes during animal evolution, which are often associated with morphological diversification, has long been a central issue in evolutionary developmental biology. Recent comparative transcriptomic studies revealed that gene expression profiles of mid-embryonic period tend to be more evolutionarily conserved than those in earlier or later periods. While the hourglass-like divergence of developmental processes has been demonstrated in a variety of animal groups such as vertebrates, arthropods, and nematodes, the exact mechanism leading to this mid-embryonic conservation remains to be clarified. One possibility is that the mid-embryonic period (pharyngula period in vertebrates) is highly prone to embryonic lethality, and the resulting negative selections lead to evolutionary conservation of this phase. Here, we tested this "mid-embryonic lethality hypothesis" by measuring the rate of lethal phenotypes of three different species of vertebrate embryos subjected to two kinds of perturbations: transient perturbations and genetic mutations.
Results: By subjecting zebrafish (Danio rerio), African clawed frog (Xenopus laevis), and chicken (Gallus gallus) embryos to transient perturbations, namely heat shock and inhibitor treatments during three developmental periods [early (represented by blastula and gastrula), pharyngula, and late], we found that the early stages showed the highest rate of lethal phenotypes in all three species. This result was corroborated by perturbation with genetic mutations. By tracking the survival rate of wild-type embryos and embryos with genetic mutations induced by UV irradiation in zebrafish and African clawed frogs, we found that the highest decrease in survival rate was at the early stages particularly around gastrulation in both these species.
Conclusion: In opposition to the "mid-embryonic lethality hypothesis," our results consistently showed that the stage with the highest lethality was not around the conserved pharyngula period, but rather around the early period in all the vertebrate species tested. These results suggest that negative selection by embryonic lethality could not explain hourglass-like conservation of animal embryos. This highlights the potential contribution of alternative mechanisms such as the diversifying effect of positive selections against earlier and later stages, and developmental constraints which lead to conservation of mid-embryonic stages.
Fig. 1. Pharyngula stages did not show the highest rate of lethal phenotypes following transient perturbations. a Representative embryos that showed malformation or lethal phenotype. (I–IV) Zebrafish embryos with (I) curled trunk, (II) bent trunk axis, (III) pericardial edema, and (IV) shortened trunk. (V–VIII) African clawed frog embryos with (V) curled trunk and small eyes, (VI) severely bent trunk, (VII) edema and abnormal head, and (VIII) bent trunk axis. (IX, X) Chicken embryos with (IX) abnormal head and growth arrest, and (X) small eyes. Scale bars represent 1 mm (I–VIII) and 5 mm (IX, X). b–d Rate of lethal phenotypes rate after transient perturbation in b zebrafish, c African clawed frog, and d chicken. Phenotype evaluation was performed at hatch period in zebrafish, st. 45 in African clawed frog, and HH25 in chicken. Blst blastula, Gst gastrula, Pha pharyngula, Lat late embryo, ctrl untreated control group. Data are displayed as means, and error bars denote SD. Only significant differences between each treated group and the control group are shown. *P < 0.05, **P < 0.01, ***P < 0.001 (Tukey–Kramer method)
Fig. 2. Survival rate after UV irradiation decreased in the gastrula period, but not the pharyngula period. Kaplan–Meier survival curves of a zebrafish and b African clawed frog embryos after UV irradiation at the MZT period. Note that the horizontal axis shows successive developmental stages rather than actual time length. For zebrafish, developmental stages described by Kimmel et al. [35] were numbered sequentially from 1 to 35. Images of the developmental stages are shown below, with the numbers on the line corresponding to those in the survival curve x axis. Blue arrowheads, most conserved developmental periods in previous reports [18, 20]; black line, control; red line, UV-irradiated embryos; shaded area, 95% CI (confidence interval); vertical dotted line, UV irradiation. Numbers of embryos used in this analysis: zebrafish control group, n = 72; zebrafish treated group, n = 216; African clawed frog control group, n = 72; and African clawed frog treated group, n = 108
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