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The evolution of hierarchical gene regulatory networks

Nature Reviews Genetics volume 10, pages 141–148 (2009)Cite this article

Abstract

Comparative developmental evidence indicates that reorganizations in developmental gene regulatory networks (GRNs) underlie evolutionary changes in animal morphology, including body plans. We argue here that the nature of the evolutionary alterations that arise from regulatory changes depends on the hierarchical position of the change within a GRN. This concept cannot be accomodated by microevolutionary nor macroevolutionary theory. It will soon be possible to investigate these ideas experimentally, by assessing the effects of GRN changes on morphological evolution.

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Figure 1: Key features of gene regulatory networks (GRNs), and consequences of changes in GRN components.
Figure 2: Developmental effect of gene regulatory network change depends on location.

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Acknowledgements

We appreciate the helpful comments from several reviewers. D.H.E. acknowledges support from the NASA Astrobiology Program, and E.H.D. from the National Science Foundation (IOS 0641398).

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Authors and Affiliations

  1. Douglas H. Erwin is at the Department of Paleobiology, MRC-121, National Museum of Natural History, PO BOX 37012, Washington, Washington DC 20013-7012, USA; and the Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, New Mexico 87501, USA.,

    Douglas H. Erwin

  2. and the Santa Fe Institute, 1399 Hyde Park Road, Santa Fe, New Mexico 87501, USA.,

    Douglas H. Erwin

  3. Eric H. Davidson is at the Division of Biology 156-29, California Institute of Technology, Pasadena, California 91125, USA,

    Eric H. Davidson

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Correspondence to Douglas H. Erwin.

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Biotapestry

Glossary

Additive genetic variation

The portion of genetic variance that is attributable to the average effect of substitution of one allele for another at a locus; it is used to predict the rate of response to selection for quantitative traits.

Body plan

The conserved aspects of morphology that define major clades, recognized in a Linnean hierarchy as phyla, classes and perhaps orders.

Fixation

Describes the situation in which a mutation has achieved a frequency of 100% in a natural population.

Haltere

Club-shaped modified hind wings on Drosophila species that serve as gyroscopic sense organs.

Heterochronic

An evolutionary change in the timing of a developmental process, so that a character or process occurs earlier or later in ontogeny, or grows at a different rate.

Imaginal disc

Epidermal thickenings in the larvae of holometabolous insects. The discs contain mesodermal cells that give rise to adult organs.

Integumental

Relating to the skin; appendages that grow out of the skin.

Lockdown

Establishment of a stable regulatory state by instituting positive feedback between regulatory genes that ensures continued transcription of the participating genes and those operating downstream of them in the GRN.

Macroevolution

Evolution above the species level, including species-level trends, and putatively encompassing selection at the level of species and clades.

Microevolution

Evolution within species and often the formation of new species; this is experimentally accessible through studies of shifting gene frequencies in populations.

Neofunctionalization

Acquisition by a duplicated gene of a new function compared with the original common ancestral function.

Notum

The dorsal portion of an insects thoracic segment.

Outgroup

The most distantly related group in a phylogenetic analysis; it is used to establish the sequence and polarity of evolutionary changes.

Pleisiomorphic

Character states of an organism that were present before the last common ancestor of a clade.

Purifying internal selection

The elimination of genetic variation except around a single mode, by selection against non-viable developmental mutants.

Regulatory state

The set of active transcription factors in every cell at any time point.

Subfunctionalization

Retention by duplicated genes of different components of the original common ancestral function, which allows both gene copies to be preserved.

Trichome

Small hairs, specifically on the epidermis of Drosophila species.

Uniformitarianism

The assumption that studies of present processes are sufficient to understand past events, because there is a single common underlying evolutionary process that accounts for changes at every level.

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Erwin, D., Davidson, E. The evolution of hierarchical gene regulatory networks. Nat Rev Genet 10, 141–148 (2009). https://doi.org/10.1038/nrg2499

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