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  • Review Article
  • Published:

Evolution of development in closely related species of flies and worms

Nature Reviews Genetics volume 3, page 907 (2002)Cite this article

Key Points

  • The extensive knowledge of the genetic basis for development of the model organisms Drosophila melanogaster and Caenorhabditis elegans, together with their complete genome sequences, provides a useful tool for comparing their development with that of other closely related species.

  • To identify the genetic changes that underlie small morphological differences, recent studies have used either a candidate-gene approach or, where hybrids are viable, direct classical genetics. This approach can allow the rapid identification of genes that contribute to phenotypic change.

  • Evolution of cis-regulatory sequences that alters gene expression might contribute to phenotypic change.

  • Regulatory modules of developmental genes are subject to continuous sequence change and to stabilizing selection in the absence of morphological change.

  • Co-evolution of transcription factors and their binding sequences can be readily shown using comparisons between closely related species.

  • The redundant cellular interactions that underlie the development of a structure and that contribute to its robustness are also subject to continuous change.

  • Studies of satellite species should help to bridge the gap between evolutionary genetics and comparative embryology.

Abstract

One of the main challenges in evolutionary biology is to identify the molecular changes that underlie phenotypic differences that are of evolutionary significance. Comparative studies of early development have shown that changes in the spatio-temporal use of regulatory genes, as well as changes in the specificity of regulatory proteins, are correlated with important differences in morphology between phylogenetically distant species. However, it is not known how such changes take place in natural populations, and whether they result from a single, or many small, additive events. Extending this approach to the study of development of closely related species promises to enrich this debate.

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Figure 1: Evolution of the bicoid gene in Diptera.
Figure 2: Evolution of sexually dimorphic pigmentation in Drosophila.
Figure 3: Conservation of the hunchback promoter in Diptera.

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Acknowledgements

Discussions with M. Labouesse and comments on the manuscript from J.-M. Gibert and the three anonymous reviewers are gratefully acknowledged. Work in the author's laboratory is funded by The Wellcome Trust.

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Authors and Affiliations

  1. Department of Zoology, University of Cambridge, Downing Street, Cambridge, CB2 3EJ, UK

    Pat Simpson

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  1. Pat Simpson
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DATABASES

LocusLink

AbdB

achaete-scute

Antp

bab

bcd

caudal

chordin

Deformed

Dpp

dsx

eve

Giant

Hb

hedgehog

Kruppel

ovo

Orthodenticle

Rb

RbAp48

short gastrulation

Ubx

zen

WormBase

cye-1

lin-39

Glossary

SATELLITE SPECIES

Species that are sufficiently closely related to the well-known model species that the underlying genetic regulation of homologous cellular processes can be compared.

DIPTERA

The true flies, an order of insects with a single pair of wings.

ANLAGE

A group of cells that are destined to become a specific structure or tissue in the adult, but have not yet differentiated.

CYCLORRAPHOUS FLIES

Highly derived Diptera in which pupal development and metamorphosis take place in a puparium, a modified form of the last larval cuticle.

TRICHOME

A thin, cuticular, non-sensory process that is secreted by an individual cell.

MONOMORPHIC SPECIES

A species in which males and females are structurally identical for the trait that is under consideration.

FATE MAP

The description of the cell divisions from fertilized egg to adult, which are linked to the eventual anatomical position of the cell in the animal and the differentiated state, or fate, of the cell.

BLAST CELL

An undifferentiated precursor cell.

EQUIVALENCE GROUP

A group of cells with the same developmental or genetic potential. Any subsequent differences between them generally result from extrinsic signals.

COMPLEMENT

Two alleles that each give a mutant phenotype when homozygous, are said to complement if they give a wild-type phenotype when combined in the same individual.

GENE CONVERSION

The non-reciprocal transfer of genetic information between homologous genes, as a consequence of mismatch repair after heteroduplex formation.

PRIMARY PAIR-RULE GENES

Pair-rule genes are expressed in alternating stripes and function to allocate cells to the different segments of the body. The primary pair-rule genes respond to several upstream factors by means of complex modular promoters.

GENETIC DRIFT

The random fluctuations in allele frequencies over time that are due to chance alone.

STABILIZING SELECTION

Selection that favours intermediate phenotypes over extreme phenotypes.

CANALIZATION

The buffering or stabilization of developmental pathways against mutational or environmental perturbations, by several genetic factors.

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Simpson, P. Evolution of development in closely related species of flies and worms. Nat Rev Genet 3, 907 (2002). https://doi.org/10.1038/nrg947

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