Heterochrony and Behavior

Terminology

A popular statement reads: “ontogeny recapitulates phylogeny.” This is known as Ernest Haeckel’s (1834-1919) biogenetic law, proposed to explain similarities between developing embryos and the adult morphology of their ancestors. For example, human embryos exhibit gill slits even though gills never become functional. Haeckel interpreted this trait as a remnant of the human’s ancient fish ancestors. According to recapitulation, phylogeny occurs because new developmental stages are added during ontogeny, but each generation must go through the same sequence of stages as their ancestors before reaching stages unique to their species. Haeckel called it the principle of terminal addition.

For decades, the study of the relationship between ontogeny and phylogeny remained in the background of evolutionary science, surrounded by controversy and clouded by a complicated terminology. However, progress in molecular biology and a standardization of terminology paved the way for an integration of development and evolution (McNamara, 1986). Recapitulation is one of several possible outcomes relating ontogeny and phylogeny. Thus, the biogenetic law offers only a partial description of the facts. Recapitulation was subsumed under the more general concept of heterochrony—evolutionary changes in the rate of development and in the relative time of appearance of traits from ancestors to descendant species. Thus, developmental rate is said to be accelerated or retarded in descendants, relative to the rate observed in their ancestors.

Figure 3.9 lists the basic outcomes of heterochrony. Although there is a tendency to apply labels such as “neotenic” or “hypermorphic” to an entire species (as in the phrase, “humans are neotenic”), heterochrony applies to traits. Traits can exhibit different rates of evolutionary change. This aspect of evolution, known as mosaic evolution, can be appreciated by comparing the human hands (which preserve the ancestral grasping morphology of primates) and feet (which have evolved adaptations for bipedal locomotion, losing the grasping function observed in other primates).

Examples of heterochrony are common in terms of morphology. Dwarfism involves similar morphology in ancestors and descendants, but smaller body size in the descendants, whereas gigantism is the opposite. Changes in body size with preservation of morphological differentiation can be achieved by the action of growth hormones. In African pygmies, whose

Figure 3.9 Summary and characteristics of the main processes of heterochrony. Heterochrony refers to changes in the timing of development of particular traits in descendant species (D), relative to their ancestors (A).

ancestors were larger in body size, the levels of growth hormone are similar to those of larger humans until they reach puberty. In adults, however, there is reduced expression of the genes for the growth hormone and for the growth-hormone receptor, thus resulting in a short stature (Bozzola et al., 2009).

In paedomorphosis, descendants reach sexual maturity at a stage corresponding to a juvenile stage in their ancestors. Paedomorphosis has been postulated to be responsible for the evolution of chordates from tunicate larvae (Garstand, 1928). As adults, tunicates do not resemble a chordate, living a sessile life attached to a rock at the bottom of the sea in shallow waters. As larvae, however, they are free swimmers and exhibit all four major chordate traits: notochord, dorsal nerve cord, gill slits, and postanal tail. Whereas it is possible that vertebrates arose from a tunicate larva that became sexually mature before metamorphosis converted it into a sessile adult, other theories of vertebrate origins have also been proposed (Satoh, Rokhsar, & Nishikawa, 2014).

Neoteny involves a similarity in the onset of development, coupled with a decrease in the rate of development and a delay in sexual maturity. For example, most salamanders pass through an aquatic larval stage and metamorphose into a terrestrial animal before sexual maturity. However, some species achieve sexual maturation while still in the aquatic stage— a sexually active larvae of large body size. The Mexican axolotl (Ambystoma mexicanum), a salamander that lives in cave ponds of fresh water, has external gills and a flattened tail, but becomes sexually mature and reproduces as a typical amphibian by external fertilization. Axolotls do not normally metamorphose into a terrestrial form, as most salamanders do, but metamorphosis can be induced in the laboratory by treatment with the thyroid hormone thyroxin. Similarly, the human brain grows at a high rate until the 22nd week of gestation in both humans and chimpanzees. However, the human brain continues to grow at similar rates afterward, whereas growth is slowed down in chimpanzees after this point (Sakai et al., 2012). Thus, even after birth, the human brain continues to grow at fetal rates.

Peramorplwsis involves a delay in the onset of sexual maturity. The relationship between brain size and body size can be viewed as an example of hypermorplwsis. Many lineages exhibit an evolutionary trend toward an increase in body size—known as Cope’s law. When natural selection favors larger body size in the descendant compared to the ancestor, organs also need to grow in size. As discussed in Chapter 6, there is a positive correlation between body size and brain size in vertebrates that shows the concerted action of growth hormones in the entire organism.