In biology, heterochrony is defined as a developmental change in the timing or rate of events, leading to changes in size and shape. There are two main components, namely (i) the onset and offset of a particular process, and (ii) the rate at which the process operates. A developmental process in one species can only be described as heterochronic in relation to the same process in another species, considered the basal or ancestral state, which operates with different onset and/or offset times, and/or at different rates. The concept was first introduced by Ernst Haeckel in 1875.^[1]

An example can best illustrate the three dimensions of heterochrony.

• Predisplacement and postdisplacement: If a developmental process, such as the growth of a tail in the embryo of "species A", starts earlier and ends earlier than that of "species B", but the rate of growth is the same for both, the final result may basically be the same, although the tail of species A develops earlier than the one of species B. The earlier exhibits predisplacement, and the later species exhibits postdisplacement.^[2]
• Neoteny: if the rate of growth is increased, and the time between the start and end of development is decreased proportionally, the tail will end up the same size. The species with faster growth exhibits acceleration, and the species with slower exhibits neoteny.^[2]
• Hypermorphosis: if the end of development is delayed and the rate is unaffected, development progresses further, and the tail will be also larger. The species that develops further exhibits hypermorphosis, and the species that does not develop as far exhibits progenesis.^[2]

Detecting heterochronies[edit]

Some heterochronies are easily identifiable when comparing phylogenetically close species, for example a group of different bird species whose legs differ in their average length. However, in many cases, these comparisons are complex because there are no universal ontogenetic time markers. Because of this, the method of event pairing, consisting in comparing the relative timing of two events at a time, was developed.^[3] This method was designed to detect event heterochronies, as opposed to allometric changes. It is fairly cumbersome to use because the number of event pair characters increases with the square of the number of events compared. Thus, an automated algorithm was implemented into the PARSIMOV script.^[4] A more recent method, continuous analysis, rests on a simple standardization of ontogenetic time or sequences, on squared change parsimony and phylogenetic independent contrasts.^[5]

Humans[edit]

Several heterochronies have been described in humans, relative to the chimpanzee. For instance, in chimpanzee fetuses brain and head growth starts at about the same developmental stage and present a growth rate similar to that of humans, but end soon after birth. Humans, on the contrary, continue their brain and head growth several years after birth. This particular type of heterochrony is named hypermorphosis and involves a delay in the offset of a developmental process, or what is the same, the presence of an early developmental process in later stages of development. In addition, humans are known for presenting about 30 different neotenies in comparison to the chimpanzee.^[6]

In other species[edit]

Heterochrony is extensively referenced in biological literature, but inconsistency with its uses remains. This is due to lack of universal definition. To exacerbate the confusion, subcategories of heterochrony were and are currently being used differently. The term neoteny is one of three types of paedomorphosis, that was originally used by Kolman (1885) to describe the truncation of development in an organism. Later on, neoteny was used by De Beer (1930) to describe decreased growth in somatic character and accelerated growth in gonadal development. To alleviate the confusion for simplicity purposes, heterochrony in other species will be described in the form of paedomorphosis and peramorphosis. In addition, species will be described in comparison to similar species or relatives along its lineage.^[7]

Paedomorphosis can be observed when an organism/species mature (sexual maturation is most typical) while retaining juvenile traits. One species commonly studied is the Axolotl. The adult Axolotl looks very similar to its larval form. Some say it looks like a giant larva. Adult Axolotls are sexually mature, but retain their gills and fins. They remain in aquatic environments.^[8][9]In three species of bagworm moths, females become flightless when their wings become degenerate, reduced, or wingless due to apoptosis. The reduction in their wings begins in their late larval stage to pupal stage. A common misconception of insects is the importance of acquiring the ability of flight.^[10] From an evolutionary perspective, if there is no demand for flight, then natural selection will favor flightlessness.

Contrary to paedomorphosis, peramorphosis is delayed maturation and extended periods of growth. The extinct Irish elk is an example of peramorphosis. From the fossil record, its antlers spanned up to 12 feet wide, which is about a third larger than the antlers of its close relative, the moose. The Irish elk had larger antlers due to extended development during their period of growth. In addition, these huge antlers exemplify outweighed benefits of sexual selection by ecological selection. Due to the nutrient costs of maintaining these antlers combined with rapid climate change, the Irish elk could not adapt and evolve smaller antlers fast enough, which led to its extinction.^[11][12] Another example of peramorphosis is the insular (island) rodents. Their characteristics include gigantism, wider cheek and teeth, reduced litter size, and longer life span. Their relatives that inhabit continental environments are much smaller. These insular rodents have evolved gigantism, wider cheeks, and larger teeth to accommodate the abundance of larger food and resources they have on their islands. These factors are part of a complex phenomenon termed Island Syndrome.^[13] With less predation and competition for resources, selection favored overdevelopment of these species. Reduced litter sizes enable overdevelopment of their bodies into larger ones. In some species of frogs, such as the Puerto Rican tree frog, they skip their entire larval stage. These frogs hatch out of their eggs into froglets with limbs, severely reduced gills (or no gills), and gill slits. Their habitats include forests, gardens, under rocks, and logs, which are non-aquatic.^[14][15]

A trend commonly seen is that paedomorphic species have the tendency to inhabit or stay in aquatic environments and peramorphic species tend to inhabit terrestrial environments. The mole salamander, which is a close relative to the Axolotl, surprisingly displays both paedomorphosis and paramorphisis. The larva can develop in either direction, but not backwards. Some research supposes that population density, food, and the amount of water have an effect on the expression of heterochrony. A study conducted on the mole salamander in 1987 found it evident that a higher percentage of individuals became paedomorphic when there was a low larval population density in a constant water level as opposed to a high larval population density in drying water.^[16] This had an implication that led to hypotheses claiming that selective pressures imposed by the environment, such as predation and loss of resources, were instrumental to the cause of these trends.^[17] These ideas were reinforced by other studies, such as peramorphosis in the Puerto Rican Tree frog. Another reason could be generation time, or the lifespan of the species in question. When a species has a relatively short lifespan, natural selection will favor evolution of paedomorphosis (e.g. Axolotl: 7-10 years). On the flip side, in long lifespans natural selection will favor evolution of peramorphosis (e.g. Irish Elk: 20-22 years).^[18]

References[edit]

See also[edit]

• Developmental biology
• Embryogenesis
• Evolutionary biology
• Neoteny
• Phylogeny