Animal body plans are conservative. Although genes were known that could substantially modify organismal phenotypes (such as Mendel’s short versus tall pea plants), it was widely assumed that the body parts of conspecific animals were structurally conservative during the evolutionary short term. However, little was known about the genetic underpinnings of organismal development (ontogeny), or how ontogenetic shifts might relate to evolutionary processes.
ontogeny; Hox genes
Animal body plans are conservative. Although genes were known that could substantially modify organismal phenotypes (such as Mendel’s short versus tall pea plants), it was widely assumed that the body parts of conspecific animals were structurally conservative during the evolutionary short term. However, little was known about the genetic underpinnings of organismal development (ontogeny), or how ontogenetic shifts might relate to evolutionary processes.
In 1915, Calvin Bridges (see Bridges and Morgan, 1923) uncovered the first example of a “homeotic” mutation, which he named bithorax (bx). All adult insects have three thoracic segments (T1, T2, and T3) each normally bearing a pair of legs, with T2 and T3 also supporting wings and flight organs called halteres, respectively. Fruit flies homozygous for Bridges’ bx mutation developed as if T3 had been transformed into T2, such that individuals had an extra pair of wings (for a total of four rather than the usual two). Other homeotic mutations soon were discovered that acted during development in such a way as to transform (for example) antennae into legs that sprouted from a fly’s head!
Today, we know that homeotic genes encode factors that regulate gene transcription and that they occur as tight collinear clusters of about a dozen loci (derived through serial gene duplications) within the nuclear genomes of invertebrate and vertebrate animals. During an organism’s development, these “Hox” genes govern somatic differentiation along the primary anterposterior body axis and they also play key regulatory roles in the construction of secondary body axes such as limbs. Thus, Hox genes are of exceptional importance in directing morphogenesis during ontogeny, and they also are presumed to underlie many of the alterations in animal body plans during the evolutionary process.
The discovery of homeotic genes left an interesting scientific legacy. On the one hand, it fed into the Mendelian–Biometrician controversy of the early 1900s (see Chapter 19) by raising the possibility that evolution sometimes proceeds by saltational jumps in phenotype, and it thereby also gave fodder to Richard Goldschmidt’s (1940) suggestion that “hopeful monsters” might play a significant evolutionary role. These latter notions are no longer popular today. On the more positive side of the ledger, the discovery of homeotic genes helped to lay the foundation for a related concept – now widely accepted – that changes in gene regulation generally underlie the evolutionary diversification of organismal phenotypes (see Chapter 41). Furthermore, the study of homeotic genes and numerous other categories of regulatory loci has become a solid cornerstone of much modern research in “evo-devo” (evolutionary developmental biology).
1. Bridges CB, Morgan TH. 1923. The third-chromosome group of mutant characters of Drosophila melanogaster. The Carnegie Institute, Washington, DC.
2. Goldschmidt R. The Material Basis of Evolution New Haven, CT: Yale University Press; 1940.
3. Carroll SB. Homeotic genes and the evolution of arthropods and chordates. Nature. 1995;376:479–485.
4. Carroll SB, Grenier JK, Weatherbee SD. From DNA to Diversity: Molecular Genetics and the Evolution of Animal Design Malden, MA: Blackwell; 2001.
5. Carroll SB. Endless Forms Most Beautiful: The New Science of Evo Devo and the Making of the Animal Kingdom New York, NY: Norton; 2005.
6. Hoffer A, Xiang J, Pick L. Variation and constraint in Hox gene evolution. Proc Natl Acad Sci USA. 2013;110:2211–2216.