Animal development: evolutionary perspective

The idea of a relationship between individual development, or ontogeny, and the evolutionary history of a race, or phylogeny, is an old one. The concept received much attention in the nineteenth century and is often associated with the names of Karl Ernst von Baer (1792-1876) and Ernst Haeckel (1834-1919), two prominent German biologists who offered differing perspectives on embryology and evolution. Haeckel coined the catchphrase and dominant paradigm: Ontogeny recapitulates (or repeats) phylogeny. Since Haeckel’s time, however, the relations between ontogeny and phylogeny have been portrayed in a variety of ways, including the reverse notion that phylogeny is the succession of ontogenies. Research in the 1970s and 1980s on the parallels between ontogeny and phylogeny focused on the change of timing in developmental events as a mechanism for recapitulation and on the developmental-genetic basis of evolutionary change.

Concepts of Biogenetic Law in the Nineteenth Century

During the early nineteenth century, two different concepts of parallels between development and evolution arose. The German J. F. Meckel (1781-1833) and the Frenchman Étienne Serres (1786-1868) believed that a higher animal in its embryonic development recapitulates the adult structures of animals below it on a scale of being. Baer, on the other hand, argued that no higher animal repeats an earlier adult stage, but rather, the embryo proceeds from undifferentiated homogeneity to differentiated heterogeneity, from the general to the specific. Von Baer published his famous and influential four laws in 1828: The more general characters of a large group of animals appear earlier in their embryos than the more special characters; from the most general forms, the less general are developed; every embryo of a given animal, instead of passing through the other forms, becomes separated from them; the embryo of a higher form never resembles any other form, only its embryo.

By the late nineteenth century, the notion of recapitulation and Baer’s laws of embryonic similarity were recast in evolutionary terms. Haeckel, and others, established the biogenetic law: That is, ontogeny recapitulates the adult stages of phylogeny. It was, in a sense, an updated version of the Serres-Meckel law but differed in that the notion was valid not only for a chain of being but also for many divergent lines of descent; ancestors had evolved into complex forms and were now considered to be modified by descent. More specifically, Haeckel thought of ontogeny as a short and quick recapitulation of phylogeny caused by the physiological functions of heredity and adaptation. During its individual development, he wrote, the organic individual repeats the most important changes in form through which its forefathers passed during the slow and long course of their paleontological development. The adult stages of ancestors are repeated during the development of descendants but crowded back into earlier stages of ontogeny. Ontogeny is the abbreviated version of phylogeny. These repeated stages reflect the history of the race. Haeckel considered phylogeny to be the mechanical cause of ontogeny.

The classic example of recapitulation is the stage of development in an unhatched bird or unborn mammal when gill slits are present. Haeckel argued that gill slits in this stage represented gill slits of the adult stage of ancestral fish, which in birds and mammals were pressed back into early stages of development. This theory differed from von Baer’s notion that the gill slit in the human embryo and in the adult fish represented the same stage in development. Recapitulationists explained the gill slits’ change from a large adult ancestor to a small embryo in two ways—terminal addition, in which stages are added to the end of an ancestral ontogeny, and condensation, in which development is accelerated as ancestral features are pushed back to earlier stages of the embryo. Haeckel also coined another term, heterochrony, which he used to denote a displacement in time of the appearance of one organ in ontogeny before another, thus disrupting the recapitulation of phylogeny in ontogeny. Haeckel was not, however, interested primarily in mechanisms or in embryology for its own sake but rather for the information it could provide for developing evolutionary histories.

Recapitulation in the Twentieth Century

With the rise of mechanistic experimental embryology and with the establishment of Mendelian genetics in the early twentieth century, the biogenetic law was largely repudiated by biologists. Descriptive embryology was out of fashion, and the existence of genes made the two correlate laws to recapitulation—terminal addition and condensation—untenable. One of the most influential modifications for later work on the subject was broached in a paper by Walter Garstang (1868-1949) in 1922, in which he reformulated the theory of recapitulation and refurbished the concept of heterochrony. Garstang argued that phylogeny does not control ontogeny but rather makes a record of the former: That is, phylogeny is a result of ontogeny. He suggested that adaptive changes in a larval stage coupled with shifts in the timing of development (heterochrony) could result in radical shifts in adult morphology.

Stephen Jay Gould (1941-2002) resurrected the long unpopular concept of recapitulation with his book Ontogeny and Phylogeny (1977). In addition to recounting the historical development of the idea of recapitulation, he made an original contribution to defining and explicating the mechanism (heterochrony) involved in producing parallels between ontogeny and phylogeny. He argued that heterochrony—“changes in the relative time of appearance and rate of development for characters already present in ancestors”—was of prime evolutionary importance. He reduced Gavin de Beer’s complex eight-mode analysis of heterochrony to two simplified processes: acceleration and retardation. Acceleration occurs if a character appears earlier in the ontogeny of a descendant than it did in an ancestor because of a speeding up of development. Conversely, retardation occurs if a character appears later in the ontogeny of a descendant than it did in an ancestor because of a slowing down of development. To demonstrate these concepts, Gould introduced a “clock model” to bring some standardization and quantification to the heterochrony concept.

He considered the primary evolutionary value of ontogeny and phylogeny to be in the immediate ecological advantages for slow or rapid maturation rather than in the long-term changes of form. Neoteny (the opposite of recapitulation) is the most important determinant of human evolution. Humans have evolved by retaining the young characters of their ancestors and have therefore achieved behavioral flexibility and their characteristic form. For example, there is a striking resemblance between some types of juvenile apes and adult humans; this similarity for the ape soon fades in its ontogeny as the jaw begins to protrude and the brain shrinks. Gould also insightfully predicted that an understanding of ontogeny and phylogeny would lead to a rapprochement between molecular and evolutionary biology.

By the 1980s, Rudolf Raff (1941-2019) and Thomas C. Kaufman found this rapprochement by synthesizing embryology with genetics and evolution, published in their work Embryos, Genes, and Evolution (1983). Their work focused on the developmental-genetic mechanisms that generate evolutionary change in morphology. They asserted that a genetic program governs ontogeny and that a small number of genes that function as switches between alternate states or pathways are the deciding factors in development. When these genetic switch systems are modified, evolutionary changes in morphology occur mechanistically. They argued further that regulatory genes—genes that control development by turning structural genes on and off—control the timing of development, make decisions about cell fates, and integrate structural gene expression to produce differentiated tissue. All this plays a considerable role in evolution.

Description Versus Experimentation

Both embryology and evolution have traditionally been descriptive sciences using methods of observation and comparison. By the end of the nineteenth century, a dichotomy had arisen between the naturalistic (descriptive) and the experimentalist tradition. The naturalists’ tradition viewed the organism as a whole, and morphological studies and observations of embryological development were central to their program. Experimentalists, on the other hand, focused on laboratory studies of isolated aspects of function. A mechanistic outlook was compatible with this experimental approach.

Modern embryology uses both descriptive and experimental methods. Descriptive embryology uses topographic, histological (tissue analysis), cytological (cell analysis), and electron microscope techniques supplemented by morphometric (the measurement of form) analysis. Embryos are visualized using either plastic models of developmental stages, schematic drawings, or computer simulations. Cell lineage drawings are also used with the comparative method for phylogenies.

Experimental embryology, on the other hand, uses more invasive methods of manipulating the organism. During this field of study’s early period, scientists subjected amphibian embryos to various changes to their normal path of development; they were chopped into pieces, transplanted, exposed to chemicals, and spun in centrifuges. Later, fate maps came into use to determine the future development of regions in the embryo. It was found that small patches of cells on the surface of the embryo could be stained, without damaging the cell, by applying small pieces of agar soaked in a vital dye. One could then follow the stained cells to their eventual position in the gastrula.

Interdisciplinary Studies

Evolutionary theory primarily uses paleontology (study of the fossil record) to study the evolutionary history of species, yet Gould also used quantification (the clock model, for example), statistics, and ecology to understand the parallels between ontogeny and phylogeny. Most scientists interested in the relationships between ontogeny and phylogeny chiefly use comparative and theoretical methods. They, for example, compare structures in different animal groups or compare the adult structures of an animal with the young stage of another. If similarities exist, are the lineages similar? Are the stages in ontogenetic development similar to those of the development of the whole species?

Yet, the study of relationships between ontogeny and phylogeny is an interdisciplinary subject. Not only are methods from embryology and evolutionary theory of help but also, increasingly, techniques are applied from molecular genetics. Haeckel’s method was primarily a descriptive historical one, and he collected myriad descriptive studies of different animals. Although scientists in those days had relatively simple microscopes, they left meticulous and detailed accounts.

A fusion of embryology, evolution, and genetics involves combining different methods from each of the respective disciplines for the study of the relationship between ontogeny and phylogeny. The unifying approach has been causal-analytical, in the sense that biologists have been examining mechanisms that produce parallels between ontogeny and phylogeny, as well as the developmental-genetic basis for evolutionary change. The methods are either technical or theoretical. Technical methods include the electron microscope, histological, cytological, and experimental analyses; the theoretical methods include comparison, historical analysis, observations, statistics, and computer simulation.

Ramifications Beyond Science

The relationship between ontogeny and phylogeny is one of the most important ideas in biology and a central theme in evolutionary biology. It illuminates the evolution of ecological strategies, large-scale evolutionary change, and the biology of regulation. This scientific idea has also had far-reaching influences in areas such as anthropology, political theory, literature, child development, education, and psychology.

In the late nineteenth century, embryological development was a major part of evolutionary theory; however, that was not the case for much of the twentieth century. Although there was some interest in embryology and evolution from the 1920s to 1950s by Garstang, J. S. Huxley, de Beer, and Richard Goldschmidt, during the first three decades of the twentieth century, genetics and development were among the most important and active areas in biological thought, yet there were few attempts to integrate the two areas. It is this new synthesis of evolution, embryology, and genetics that has emerged as one of the most exciting frontiers in the life sciences.

Although knowledge to be gained from a synthesis of development and evolution seems not to have any immediate practical application, it can offer greater insights into mechanisms of evolution, and knowledge of evolution will give similar insights into mechanisms of development. A study of these relations and interactions also enlarges humankind’s understanding of the nature of the development of individuals and their relation to the larger historical panorama of the history of life.

Twenty-first-century researchers continue to contribute to the understanding of the evolution and development of animals. Some research contradicts previous findings, such as an RNA molecule, not a protein, as previously asserted, creates the colors, shapes, and patterns on butterfly wings. Other studies uncover ongoing evolutionary adaptations that help bridge information gaps in historical evolutionary data. For example, one study introduced guppies to an environment without predators and other guppies to an environment with a new predator, cichlids, to evaluate adaptive changes. In six to eight generations, the guppies that did not experience predation were larger, had fewer young, and matured more slowly. In contrast, those living among cichlids had more babies, were smaller, and matured more slowly.

Scientists at Oxford University used energy-dispersive X-ray spectroscopy and X-ray diffraction to investigate the fossil record’s gap between the first animals long believed to have existed (including by Darwin) and the earliest known fossils. Evidence indicated a preservation bias between specific species and tissues in various geological eras, allowing some life forms to be better documented. This confirmed that animals had not yet evolved in the Neoproterozoic era, as some research suggested, indicating that the maximum date of animal origin was around 789 million years ago.

Principal Terms

Acceleration: The appearance of an organ earlier in the development of a descendant than in the ancestor as a result of an acceleration of development

Heterochrony: Changes in developmental timing that produce parallels between ontogeny and phylogeny; changes in the relative time of appearance and rate of development for organs already present in ancestors

Neoteny: Either the retention of immature characteristics in the adult form or the sexual maturation of larval stages

Ontogeny: The successive stages during the development of an animal, primarily embryonic but also postnatal

Paedomorphosis: The appearance of youthful characters of ancestors in later ontogenetic stages of descendants

Phylogeny: A series of stages in the evolutionary history of species and lineages

Recapitulation: The repetition of phylogeny in ontogeny or of the ancestral adult stages in the embryonic stages of descendants

Retardation: The appearance of an organ later in the development of a descendant than in the ancestor as a result of a slowing of development

Bibliography

Bonner, J. T. Morphogenesis: An Essay on Development. Princeton University Press, 1952.

De Beer, Gavin. Embryos and Ancestors. Clarendon Press, 1951.

Gilbert, Scott F. Evolutionary Developmental Biology. Academic Press an Imprint of Elsevier, 2021.

Gilbert, Scott F. "Evolution and Development." Stanford Encyclopedia of Philosophy, 8 July 2020, plato.stanford.edu/entries/evolution-development. Accessed 5 July 2023.

Gould, Stephen Jay. “Ontogeny and Phylogeny—Revisited and Reunited.” BioEssays, vol. 14, no. 4, Apr. 1992, pp. 275-280.

Gould, Stephen Jay. Ontogeny and Phylogeny. Harvard University Press, 1977.

Kappeler, Peter M. Animal Behaviour: An Evolutionary Perspective. Springer, 2022.

"New Oxford Study Sheds Light on the Origin of Animals." University of Oxford, 28 June 2023, www.ox.ac.uk/news/2023-06-28-new-oxford-study-sheds-light-origin-animals. Accessed 20 Sept. 2024.

Raff, Rudolf A., and Thomas C. Kaufman. Embryos, Genes, and Evolution: The Developmental-Genetic Basis of Evolutionary Change. Macmillan, 1983.

Schwartz, Jeffrey H. Sudden Origins: Fossils, Genes, and the Emergence of Species. Wiley, 1999.