Heterochrony can be separated into two different types: paedomorphosis (literally “child-shape”) and peramorphosis (literally “beyond-shape”). A descendant organism, whether it be a descendant individual within a population or a geologically younger species, when compared with its ancestor, can show either “less” or “more” growth. Paedomorphosis is the type of heterochrony where there is less growth during ontogeny in a descendant form, compared with its ancestor. The name reflects the fact that descendant adults resemble the juvenile condition of the ancestor. In the other form of heterochrony, the descendant undergoes more development and is said to show peramorphosis. Frequently, though certainly not inevitably, paedomorphic forms may be smaller than their ancestor, while peramorphic forms tend to be larger. Paedomorphosis and peramorphosis are not evolutionary processes in themselves but are descriptive terms that describe the appearance of the descendant morphology. They are the morphological (and sometimes behavioral) end result of the operation of a variety of heterochronic processes.
Paedomorphosis and peramorphosis can each be produced by three different, complementary processes: variations in time of cessation of growth, variation in time of commencement of growth, and change in rate of growth (Alberch et al. 1979; McNamara 1986a). Paedomorphosis occurs if the period of growth of the descendant form is stopped prematurely—progenesis (hypomorphosis of Reilly et al. 1997); if onset of growth is delayed—postdisplacement; or if the rate of growth is less in the descendant than in the ancestor—neoteny (deceleration of Reilly et al. 1997) (Figs. 2 and 3). Progenesis will affect the entire organism if premature cessation of growth is caused by the earlier onset of sexual maturity. Like neoteny and postdisplacement, it may, though, also target specific morphological features.
Peramorphosis occurs if the period of growth in the descendant is extended (hypermorphosis), if the onset of growth occurs earlier in the descendant than in the ancestor (predisplacement), or if the growth rate is increased (acceleration). Hypermorphosis, like progenesis, can affect the whole organism when the onset of sexual maturity is delayed, because fast juvenile growth rates will persist for a longer period. Alternatively, hypermorphosis can target just certain traits. Acceleration and predisplacement will affect only specific features, not the entire organism.
While this categorization of heterochrony into these six basic processes appears to have much utility, it has been argued that this presupposes a uniformity of morphological change during ontogeny, which may not always be the case (Rice 1997). It is often possible to compartmentalize ontogeny into discrete growth phases, such as embryonic, infantile, and juvenile growth in mammals, or discrete growth instars in arthropods. Each of these phases can have its own ontogenetic trajectory, which might be at variance with other growth phases. Each can be subjected to its own heterochronic variation, involving extensions or contractions of these phases, or discrete variation in growth rates. This type of intra-ontogenetic heterochrony is called sequential heterochrony (McNamara 2002).
The terminology of heterochrony can be used to describe the appearance of discrete structures formed during ontogeny, such as the number of vertebrae or digits (so-called “meristic” characters) that develop during ontogeny. It can also be applied to the subsequent changes in shape of these structures during growth. These have been termed mitotic and growth heterochrony, respectively (McKinney and McNamara 1991). In many organisms, mitotic heterochrony, particularly that induced by pre- and postdisplacement, can play a very significant role during very early developmental stages. This is due to variations between ancestors and descendants in the timing of onset of development of major morphological features. Neoteny and acceleration, in other words reduced and accelerated growth rates, respectively, will be especially common during later ontogenetic development.
The relationship between size and shape is known as allometry and arises from differential growth rates between different parts of the body or in different axes on the same structure. For instance, as a bone grows, it may become relatively longer and thinner because growth is occurring at a faster rate along one axis than another. Should the relative size and shape of a structure remain the same throughout ontogeny, relative to the organism’s overall body size, growth is described as isometric. Although very few organisms grow isometrically (Klingenberg 1998), some individual traits, such as vertebrate skeletal elements, can be isometric. Usually, though, a structure such as a bone will change shape and size relative to the size and shape of the whole organism during ontogeny. If the bone increases in relative size, growth is said to occur by positive allometry. However, if there is a relative reduction in size, growth is said to show negative allometry.
There is a close relationship between allometry and heterochrony because heterochrony involves changes not only in time but also in shape and size. The consequence of changing growth rates (acceleration and neoteny) is to cause such allometric changes. Extensions or contractions of the period of growth--in other words, hypermorphosis or progenesis--have the effect of accentuating or reducing the effects of allometric changes. Consequently, those organisms that undergo pronounced allometric change during growth are more likely to generate very different descendant adult morphologies if rates or durations of growth have changed.
For example, when the skull of the domestic dog, Canis familiaris, is compared with that of the domestic cat, Felis domestica, the dog skull can be seen to undergo pronounced positive allometric change during ontogeny, particularly by strong growth of the muzzle (Fig. 4). By artificially changing growth rates and timing, a wide range of breeds that vary substantially in cranial morphology have been produced. For instance, tiny dogs like chihuahuas or King Charles spaniels are very paedomorphic, but large Irish wolfhounds are peramorphic (Fig. 5). In contrast, the extent of allometric change is minimal in the domestic cat, so that breeds do not differ greatly in morphology (Wayne 1986). In the natural world, the same effect occurs. Those organisms that produce a wider range of variation because of greater ontogenetic allometric change produce more raw material for natural selection, leading to the evolution of a wide range of descendants.
It may be trifle hard to imagine but your fluffy little Pekingese dog peering at you with doting eyes is really a wolf. This is because, as one of the numerous breeds of domestic dog (many unwittingly selected for by humans for particular heterochronic traits), it “evolved” from a wolf. All the traits present in the first known domestic dogs, which date back to at least 30,000 years (Germonpré et al. 2009), occur in puppies of wolves: shortened muzzles; steeper, wider foreheads; and smaller body size (Fig. 6). Thus, domestic dogs are essentially paedomorphic wolves (Morey 1994). But Mesolithic man was unlikely to have been selecting for these traits. He was more likely to have been selecting aspects of juvenile wolf behavior. Such more amenable juvenile behavior is more likely to have put wolf pups in contact with humans. Socialization in dogs is best developed when they are between three and 12 weeks old, at a time when primary bonds are formed. Those that fail to bond with humans are likely to have been driven away or killed.