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Developmental constraints shape the evolution of the nematode mid-developmental transition

Nature Ecology & Evolution volume 1, Article number: 0113 (2017) Cite this article

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Abstract

Evolutionary theory assumes that genetic variation is uniform and gradual in nature, yet morphological and gene expression studies have revealed that different life-stages exhibit distinct levels of cross-species conservation. In particular, a stage in mid-embryogenesis is highly conserved across species of the same phylum, suggesting that this stage is subject to developmental constraints, either by increased purifying selection or by a strong mutational bias. An alternative explanation, however, holds that the same ‘hourglass’ pattern of variation may result from increased positive selection at the earlier and later stages of development. To distinguish between these scenarios, we examined gene expression variation in a population of the nematode Caenorhabditis elegans using an experimental design that eliminated the influence of positive selection. By measuring gene expression for all genes throughout development in 20 strains, we found that variations were highly uneven throughout development, with a significant depletion during mid-embryogenesis. In particular, the family of homeodomain transcription factors, whose expression generally coincides with mid-embryogenesis, evolved under high constraint. Our data further show that genes responsible for the integration of germ layers during morphogenesis are the most constrained class of genes. Together, these results provide strong evidence for developmental constraints as the mechanism underlying the hourglass model of animal evolution. Understanding the pattern and mechanism of developmental constraints provides a framework to understand how evolutionary processes have interacted with embryogenesis and led to the diversity of animal life on Earth.

One of the most striking features of the living world is its sheer diversity. Accounting for how the process of evolution lends itself to the creation of diversity constitutes an important topic in evolutionary and developmental biology1–4. Although classical and population geneticists have made great progress towards an understanding of heredity and the process of natural selection, the structure of variation available to the latter remains largely unsolved1,2. Instead, the notion that “universal variability — small in amount but in every direction”5 exists for the agency of natural selection forms one of the founding pillars of modern evolutionary theory6. But research in the field of evolutionary developmental biology has challenged this view7,8, by invoking the concept of developmental constraints, defined as “a bias on the production of variant phenotypes or a limitation on phenotypic variability caused by the structure, character, composition, or dynamics of the developmental system”9. Thus, the development of a species may significantly influence its evolutionary trajectory in terms of biases for particular variations and constraints against others. However, the general patterns underlying how these constraints apply to developmental systems are not clear.

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Figure 1: Studying developmental constraints on temporal gene expression during development.
Figure 2: Mid-embryogenesis is highly conserved in MA strains.
Figure 3: Analysis of functional gene groups shows that homeodomain genes are highly conserved across MA strains.
Figure 4: The phylotypic stage is a conserved period of integration between the endoderm and ectoderm.

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Acknowledgements

We thank C. F. Baer of the University of Florida at Gainesville for providing the mutation accumulation strains and for his comments. We thank J. F. Ryan from the Whitney Institute for Marine Bioscience for comments. We also thank members of our laboratory for constructive comments. We thank the Technion Genome Center for technical assistance.

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Authors and Affiliations

  1. Faculty of Biology, Technion — Israel Institute of Technology, Haifa 3200003, Israel

    Harel Zalts

  2. Institute for Computational Medicine, New York University Langone Medical Center, New York

    Itai Yanai

  3. , New York 10016, USA

    Itai Yanai

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  1. Harel Zalts
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  2. Itai Yanai
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Contributions

H.Z. and I.Y. conceived and designed the project. H.Z. led the collection of samples, the processing of the samples for CEL-Seq and the initial bioinformatics. Both authors analysed the data and wrote the manuscript.

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Correspondence to Itai Yanai.

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The authors declare no competing financial interests.

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Supplementary Figures 1–4; Supplementary Table 1. (PDF 3985 kb)

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Zalts, H., Yanai, I. Developmental constraints shape the evolution of the nematode mid-developmental transition. Nat Ecol Evol 1, 0113 (2017). https://doi.org/10.1038/s41559-017-0113

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