Getting beyond the population genetics/developmental biology split: A New Evolutionary Synthesis

In 1922, Walter Garstang declared that ontogeny (an individual's development) does not recapitulate phylogeny (evolutionary history); rather, it creates phylogeny. Evolution is generated by heritable changes in development. "The first bird," said Garstang, "was hatched from a reptile's egg." Thus, when we say that the contemporary one-toed horse evolved from a five-toed ancestor, we are saying that heritable changes occurred in the differentiation of the limb mesoderm into chondrocytes during embryogenesis in the horse lineage. Evolution, said Richard Goldschmidt (1940), is the result of heritable changes in development, and this is as true for whether a fly has two or three bristles on its back as for whether an appendage is to become a fin or a limb.

This view of evolution as the result of hereditary changes affecting development was largely lost during the 1940s, when the Modern Synthesis of population genetics and evolutionary biology formed a new framework for research in evolutionary biology. The Modern Synthesis has been one of the greatest intellectual achievements of biology. By merging the traditions of Darwin and Mendel, evolution within a species could be explained: Diversity within a population arose from the random production of mutations, and the environment acted to select the most fit phenotypes. Those individuals most capable of reproducing would transmit the genes that gave them their advantage. Such genes included, for example, those encoding enzymes with higher rates of synthesis and globins with greater oxygen-carrying capacity. It was assumed that the same kinds of changes (genetic or chromosomal mutations) that caused evolution within a species also caused the evolution of new species. There would need to be an accumulation of these mutations, and a mechanism of reproductive isolation to enable them to accumulate in new combinations, if a new phenotype was to be produced.

Not only could the Modern Synthesis explain evolution within a species remarkably well, it also explained medically relevant questions such as why certain alleles that seem deleterious (the hemoglobin gene variant that can result in sickle cell anemia, for example) might be selected for in certain populations. The population genetic approach to evolution was summed up by one of its foremost practitioners and theorists, Theodosius Dobzhansky, when he declared, "Evolution is a change in the genetic composition of populations. The study of the mechanisms of evolution falls within the province of population genetics" (Dobzhansky 1951).

When the Modern Synthesis was formulated, developmental biology and developmental genetics were not established sciences. As the Synthesis became strengthened by systematics, plant biology, and paleontology, there was little that developmental biology could add. The questions raised in evolutionary biology could be answered without recourse to developmental biology, and the developmental approach became excluded from the Modern Synthesis (Hamburger 1980; Gottlieb 1992; Dietrich 1995; Gilbert et al. 1996). It was thought that population genetics could explain evolution, so morphology and development were seen to play little role in modern evolutionary theory (Adams 1991). In other words, macroevolution (the large morphological changes seen between species, classes, and phyla) could be explained by the mechanisms of microevolution, which is evolution within a species and can be described as "differential adaptive values of genotypes or deviations from random mating or both these factors acting together" (Torrey and Feduccia 1979).

However, the population genetic model of evolution contained some major assumptions that have now been called into question.

Gradualism. The supposition that all evolutionary changes occur gradually was debated by Darwin and his friends. Thomas Huxley, for instance, accepted evolution, but he felt that Darwin had burdened his theory with an unnecessary assumption of gradualism. A century later, Eldredge and Gould (1972), Stanley (1979), and others postulated punctuated equilibrium as an alternative to the gradualism that characterized the Modern Synthesis. According to this theory, species were characterized by their morphological stability. Evolutionary changes tended to be rapid, not gradual. At the same time, molecular studies (King and Wilson 1975) showed that 99% of the DNA of humans and chimpanzees was identical, demonstrating that a small change in DNA could cause large and important morphological changes. New findings in paleontology and molecular biology prompted scientists to consider seriously the view that mutations in regulatory genes can create large changes in morphology in a relatively short time.

Extrapolation of microevolution to macroevolution. The idea that accumulations of small mutations result in changes leading to higher taxa has also been criticized. Goldschmidt (1940) began his book The Material Basis of Evolution by asking the population genetic evolutionary biologists to try to explain the evolution of hair in mammals, feathers in birds, and the poison apparatus of snakes. Interestingly, both Goldschmidt and Waddington saw homeotic mutations as the kind of genetic change that could change one structure into another and possibly create new structures or new combinations of structures. These mutations would not be in the structural genes, but in the regulatory genes.

Lack of genetic similarity in disparate organisms. We have come a long way from when Ernst Mayr (1966) could state, concerning macroevolution: "Much that has been learned about gene physiology makes it evident that the search for homologous genes is quite futile except in very close relatives." Indeed, when one considers the Hox genes, the signal transduction pathways, and the families of paracrine factors, adhesion molecules, and transcription factors, the opposite has been seen to be the case. Adult organisms may have dissimilar structures, but the genes instructing the formation of these structures are extremely similar.

The population genetic model was formulated to explain natural selection. It is based on genetic differences in adult organisms competing for reproductive advantage. The developmental genetic model has been formulated to account for phylogeny-evolution above the species level. It is based on the similarities among regulatory genes that are active in embryos and larvae. We are still approaching evolution in the two ways that Darwin recognized. Both views involve descent with modification, and one can emphasize either the similarities or the differences between taxa. Thus, when confronted with the question of how the arthropod body plan arose, Hughes and Kaufman (2003) begin their study, "To answer this question by invoking natural selection is correct-but insufficient. The fangs of a centipede...and the claws of a lobster accord these organisms a fitness advantage. However, the crux of the mystery is this: From what developmental genetic changes did these novelties arise in the first place?"

There is emerging now a rapproachment between the population genetic accounts of evolution and the developmental genetic accounts of evolution. The population genetic approach has focused on variation within populations, while the developmental genetic approach has focused on variation between populations (Amundson 2001, 2005; Gilbert 2000). Similarly, population geneticists have been looking primarily at genes in adults competing for reproductive success, while developmental geneticists have been looking at genes involved in forming embryonic and larval organs. These differences are becoming blurred as both population geneticists and developmental geneticists begin looking at the regulatory genes that control development (see Arthur 1997; Macdonald and Goldstein 1999; Zeng et al. 1999; as well as the newer examples in the developmental biology textbook). The two approaches complement each other: While the population genetic approach focuses on the survival of the fittest, the developmental genetic approach to evolution is more concerned with the arrival of the fittest.

Evolutionary developmental biology is already beginning to provide answers to classic evolutionary genetic questions. Evolutionary biologists have long studied problems such as mimicry and industrial melanism. Now, the genes involved in these processes are being identified so that the mechanisms of underlying phenomena can be explained (Koch et al. 1998; Brakefield 1998; see also the work of described in Chapter 23). To explain evolution, both the population genetic and the developmental genetic accounts are required (Figure 1).

Figure 1 A newly emerging evolutionary synthesis. The classic approach to evolution has been that of population genetics. This approach emphasized variations within a species that enabled certain adult individuals to reproduce more frequently; thus, it could explain natural selection. The developmental approach looks at variation between populations, and it emphasizes the regulatory genes responsible for organ formation. It is better able to explain evolutionary novelty and constraint. Together, these two approaches constitute a more complete genetic approach to evolution.

Literature Cited

Amundson, R. 2001. Adaptation and development: On the lack of common ground. In E. Sober and S. Orzack (eds.), Adaptation and Optimality. Cambridge University Press, Cambridge, pp. 303-334.

Amundson, R. 2005. The Changing Role of the Embryo in Evolutionary Thought: The Roots of Evo-Devo. Cambridge University Press, NY.

Arthur, W. 1997. The Origin of Animal Body Plans: A Study in Evolutionary Developmental Biology. Cambridge University Press, New York.

Brakefield, P. M. 1998. The evolution-development interface and advances with the eyespot patterns of Bicyclus butterflies. Heredity 80: 265-272.

Dietrich, M. 1995. Richard Goldschmidt's "heresies" and the evolutionary synthesis. J. Hist. Biol. 28: 431-461.

Dobzhansky, Th. 1951. Genetics and the Origin of Species, 3rd Ed. Columbia University Press, New York.

Eldredge, N. and S. J. Gould. 1972. Punctuated equilibria: An alternative to phyletic gradualism. In T. J. M. Schopf (ed.), Models of Paleobiology. Freeman, Cooper & Co., San Francisco, pp. 82-115.

Garstang, W. 1922. The theory of recapitulation: A critical restatement of the biogenetic law. Zool. J. Linn. Soc. 35: 81-101.

Gilbert, S. F. 2000. Genes classical and genes developmental: The different uses of genes in evolutionary synthesis. In P. J. Beurton, R. Falk and H. J. Rheinberger (eds.), The Concept of the Gene in Development and Evolution. Cambridge University Press, Cambridge, pp. 178-192.

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Gottlieb, G. 1992. Individual Development and Evolution: The Genesis of Novel Behavior. Oxford University Press, New York.

Hamburger, V. 1980. Embryology and the Modern Synthesis in evolutionary theory. In E. Mayr and W. Provine (eds.), The Evolutionary Synthesis: Perspectives on the Unification of Biology. Cambridge University Press, New York, pp. 97-112.

Hughes, C. GG. and T. C. Kaufman. 2002. Hox genes and the evolution of the arthropod body plan. Evo. Dev. 4: 459-499.

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Koch, P. B., D. N. Keys, T. Rocheleau, K. Aronstein, M. Blackburn, S. B. Carroll and R. H. ffrench-Constant. 1998. Regulation of dopa decarboxylase expression during color pattern formation in wild-type and melanic tiger swallowtail butterflies. Development 125: 2303-2313.

Macdonald, S. J. and D. B. Goldstein. 1999. A quantitative genetic analysis of male sexual traits distinguishing the sibling species Drosophila simulans and D. sechellia. Genetics 153: 1683-1699.

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Zeng, Z. B., C. H. Kao and C. J. Basten. 1999. Estimating the genetic architecture of quantitative traits. Genet. Res. 74: 279-289.

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