Heterochrony
![](https://upload.wikimedia.org/wikipedia/commons/thumb/6/6c/Aniversity.jpg/290px-Aniversity.jpg)
Inevolutionary developmental biology,heterochronyis any genetically controlled difference in the timing, rate, or duration of adevelopmental processin anorganismcompared to its ancestors or other organisms. This leads to changes in the size, shape, characteristics and even presence of certainorgansand features. It is contrasted withheterotopy,a change in spatial positioning of some process in the embryo, which can also createmorphologicalinnovation. Heterochrony can be divided into intraspecific heterochrony, variation within a species, and interspecific heterochrony,phylogeneticvariation, i.e. variation of a descendant species with respect to an ancestral species.
These changes all affect the start, end, rate or time span of a particular developmental process. The concept of heterochrony was introduced byErnst Haeckelin 1875 and given its modern sense byGavin de Beerin 1930.
History
[edit]![](https://upload.wikimedia.org/wikipedia/commons/thumb/0/0a/Haeckel_vs_von_Baer.svg/330px-Haeckel_vs_von_Baer.svg.png)
The concept of heterochrony was introduced by the German zoologistErnst Haeckelin 1875, where he used it to define deviations fromrecapitulation theory,which held that "ontogeny recapitulates phylogeny".[3][2]AsStephen Jay Gouldpointed out, Haeckel's term is now used in a sense contrary to his coinage; Haeckel had assumed thatembryonic development(ontogeny) of "higher" animals recapitulated their ancestral development (phylogeny), as when mammal embryos have structures on the neck that resemble fishgillsat one stage. This, in his view, necessarily compressed the earlier developmental stages, representing the ancestors, into a shorter time, meaning accelerated development. The ideal for Haeckel would be when the development of every part of an organism was thus accelerated, but he recognised that some organs could develop with displacements in position (heterotopy,another concept he originated) or time (heterochrony), as exceptions to his rule. He thus intended the term to mean a change in the timing of the embryonic development of one organ with respect to the rest of the same animal, whereas it is now used, following the work of the British evolutionary embryologistGavin de Beerin 1930, to mean a change with respect to the development of the same organ in the animal's ancestors.[4][5]
In 1928, the English embryologistWalter Garstangshowed thattunicatelarvae shared structures such as thenotochordwith adultvertebrates,and suggested that the vertebrates arose bypaedomorphosis (neoteny)from such a larva. The proposal implied (if it were correct) a shared phylogeny of tunicates and vertebrates, and that heterochrony was a principal mechanism of evolutionary change.[6]
Modernevolutionary developmental biology(evo-devo) studies themolecular geneticsof development. It seeks to explain each step in the creation of an adult organism from an undifferentiatedzygotein terms of the control ofexpression of one geneafter another. Further, it relates such patterns of control of development tophylogeny.De Beer to some extent anticipated such late 20th-century science in his 1930 bookEmbryos and Ancestors,[7]showing that evolution could occur by heterochrony, such as in paedomorphosis, the retention of juvenile features in the adult.[8][2]De Beer argued that this enabled rapid evolutionary change, too brief to be recorded in thefossil record,and in effect explaining why apparent gaps were likely.[9]
Mechanisms
[edit]![](https://upload.wikimedia.org/wikipedia/commons/thumb/e/ee/Heterochrony.svg/370px-Heterochrony.svg.png)
Heterochrony can be divided into intraspecific and interspecific types.
Intraspecific heterochronymeans changes in the rate or timing of development within a species. For example, some individuals of the salamander speciesAmbystoma talpoideumdelay the metamorphosis of the skull.[11]Reilly and colleagues argue we can define these variant individuals aspaedotypic(with truncated development relative to the ancestral condition),peratypic(with extended development relative to the ancestral condition), orisotypic(reaching the same ancestral shape, but via a different mechanism).[10]
Interspecific heterochronymeans differences in the rate or timing of a descendant species relative to its ancestor. This can result in eitherpaedomophosis(truncating the ancestral ontogeny),peramorphosis(extending past the ancestral ontogeny), orisomorphosis(reaching the same ancestral state via a different mechanism).[10]
There are three major mechanisms of heterochrony,[12][13][14][15]each of which can change in either of two directions, giving six types of perturbations, which can be combined in various ways.[16]These ultimately result in extended, shifted, or truncated development of a particular process, such as the action of a singletoolkit gene,[17]relative to the ancestral condition or to other conspecifics, depending on whether inter- or intraspecific heterochrony is the focus. Identifying which of the six perturbations is occurring is critical in identifying the actual underlying mechanism driving peramorphosis or paedomorphosis.[10]
![](https://upload.wikimedia.org/wikipedia/commons/thumb/a/a9/Okapi_Giraffe_Neck.png/170px-Okapi_Giraffe_Neck.png)
- Onset:A developmental process can either begin earlier,pre-displacement,extending its development, or later,post-displacement,truncating it.
- Offset:A process can either end later,hypermorphosis,extending its development, or earlier,hypomorphosisorprogenesis,truncating it.
- Rate:The rate of a process can accelerate, extending its development, or decelerate (as in neoteny), truncating it.
A dramatic illustration of how acceleration can change abody planis seen insnakes.Where a typical vertebrate like a mouse has only around 60 vertebrae, snakes have between around 150 to 400, giving them extremely long spinal columns and enabling their sinuouslocomotion.Snake embryos achieve this by accelerating their system for creatingsomites(body segments), which relies on an oscillator. The oscillator clock runs some four times faster in snake than in mouse embryos, initially creating very thin somites. These expand to adopt a typical vertebrate shape, elongating the body.[18] Giraffesgain their long necks by a different heterochrony, extending the development of their cervical vertebrae; they retain the usual mammalian number of these vertebrae, seven.[1]This number appears to be constrained by the use of neck somites to form the mammaliandiaphragmmuscle; the result is that the embryonic neck is divided into three modules, the middle one (C3 to C5) serving the diaphragm. The assumption is that disrupting this would kill the embryo rather than giving it more vertebrae.[19]
Detection
[edit]Heterochrony can be identified by comparingphylogeneticallyclose species, for example a group of different bird species whose legs differ in their average length. These comparisons are complex because there are no universal ontogenetic timemarkers. The method of event pairing attempts to overcome this by comparing the relative timing of two events at a time.[20]This method detects event heterochronies, as opposed toallometricchanges. It is cumbersome to use because the number of event pair characters increases with the square of the number of events compared. Event pairing can however be automated, for instance with the PARSIMOV script.[21]A recent method, continuous analysis, rests on a simple standardization of ontogenetic time or sequences, on squared change parsimony andphylogenetic independent contrasts.[22]
Effects
[edit]Paedomorphosis
[edit]![](https://upload.wikimedia.org/wikipedia/commons/thumb/f/f6/AxolotlBE.jpg/220px-AxolotlBE.jpg)
Paedomorphosis can be the result ofneoteny,the retention of juvenile traits into the adult form as a result of retardation of somatic development, or of progenesis, the acceleration of developmental processes such that the juvenile form becomes a sexually mature adult. This means that in progenesis, germ cell growth is accelerated relative to normal or in neoteny; while somatic cell growth is normal in progenesis, but retarded in neoteny.[23]
Neoteny retards the development of the organism into an adult, and has been described as "eternal childhood".[24]In this form of heterochrony, the developmental stage of childhood is itself extended, and certain developmental processes that normally take place only during childhood (such as accelerated brain growth in humans[25][26][27]), is also extended throughout this period. Neoteny has been implicated as a developmental cause for a number of behavior changes, as a result of increased brain plasticity and extended childhood.[28]
Progenesis (or paedogenesis) can be observed in theaxolotl(Ambystoma mexicanum). Axolotls reach full sexual maturity while retaining their fins and gills (in other words, still in the juvenile form of their ancestors). They will remain in aquatic environments in this truncated developmental form, rather than moving onto land as other sexually mature salamander species. This is thought to be a form of hypomorphosis (earlier ending of development)[29]that is both hormonally[30][31]and genetically driven.[30]The entire metamorphosis that would allow the salamander to transition into the adult form is essentially blocked by both of these drivers.[32]
Paedomorphosis by progenesis may play a critical role inavian cranial evolution.[33]The skulls and beaks of living, adult birds retain the anatomy of the juveniletheropod dinosaursfrom which they evolved.[34]Extant birds have large eyes and brains relative to the rest of the skull; a condition seen in adult birds that represents (broadly speaking) the juvenile stage of a dinosaur.[35]A juvenile avian ancestor (as typified byCoelophysis) would have a short face, large eyes, a thin palate, narrow jugal bone, tall and thin postorbitals, restricted adductors, and a short and bulbous braincase. As an organism such as this aged, they would change greatly in their cranial morphology to develop a robust skull with larger, overlapping bones. Birds, however, retain this juvenile morphology.[36]Evidence from molecular experiments suggests bothfibroblast growth factor8 (FGF8) and members of theWNT signalling pathwayhave facilitated paedomorphosis in birds.[37]These signalling pathways are known to play roles in facial patterning in other vertebrate species.[38]This retention of the juvenile ancestral state has driven other changes in the anatomy that result in a light, highly kinetic (moveable) skull composed of many small, non-overlapping bones.[36][39]This is believed to have facilitated the evolution of cranial kinesis in birds[36]which has played a critical role in their ecological success.[39]
Peramorphosis
[edit]![](https://upload.wikimedia.org/wikipedia/commons/thumb/5/5d/Irish_Elk_front.jpg/220px-Irish_Elk_front.jpg)
Peramorphosis is delayed maturation with extended periods of growth. An example is the extinctIrish elk.From the fossil record, its antlers spanned up to 12 feet (3.7 m) wide, which is about a third larger than the antlers of its close relative, themoose.The Irish elk had larger antlers due to extended development during their period of growth.[40][41]
Another example of peramorphosis is seen in insular (island) rodents. Their characteristics include gigantism, wider cheek and teeth, reducedlittersize, and longer lifespan. Their relatives that inhabit continental environments are much smaller. Insular rodents have evolved these features to accommodate the abundance of food and resources they have on their islands. These factors are part of a complex phenomenon termed Island syndrome orFoster's rule.[42]
Themole salamander,a close relative to the axolotl, displays both paedomorphosis and peramorphosis. The larva can develop in either direction. Population density, food, and the amount of water may 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.[43]This had an implication that led to hypotheses that selective pressures imposed by the environment, such as predation and loss of resources, were instrumental to the cause of these trends.[44]These ideas were reinforced by other studies, such as peramorphosis in thePuerto Rican tree frog.Another reason could begeneration time,or the lifespan of the species in question. When a species has a relatively short lifespan, natural selection favors evolution of paedomorphosis (e.g. Axolotl: 7–10 years). Conversely, in long lifespans natural selection favors evolution of peramorphosis (e.g. Irish Elk: 20–22 years).[42]
Across the animal kingdom
[edit]Heterochrony is responsible for a wide variety of effects[45]such as the lengthening of the fingers by adding extraphalangesindolphinsto form their flippers,[46]sexual dimorphism,[6]and the polymorphism seen betweeninsect castes.[47]
![](https://upload.wikimedia.org/wikipedia/commons/thumb/a/a0/Ascidia_005.png/220px-Ascidia_005.png)
Garstang's hypothesis
[edit]Walter Garstangsuggested the neotenous origin of the vertebrates from atunicatelarva,[6]in opposition to Darwin's opinion thattunicatesandvertebratesboth evolved from animals whose adult form was similar to (frog) tadpoles and the 'tadpole larvae' of tunicates. According toRichard Dawkins,[48]Garstang's opinion was also held byAlister Hardy,and is still held by some modern biologists. However, according to others, closer genetic investigation rather seems to support Darwin's old opinion:
Garstang's theory is certainly an attractive one, and it was much in favour for many years... Unfortunately, recent DNA evidence has swung the pendulum in favour of Darwin's original theory. If thelarvaceansconstitute a recent re-enactment of an ancient Garstang scenario, they should find closer kinship with some modern sea squirts than with others. Alas, this is not so.[49]
— Richard Dawkins
![](https://upload.wikimedia.org/wikipedia/commons/thumb/2/2a/Human_development_neoteny_body_and_head_proportions_pedomorphy_maturation_aging_growth.png/220px-Human_development_neoteny_body_and_head_proportions_pedomorphy_maturation_aging_growth.png)
In humans
[edit]Several heterochronies have been described in humans, relative to thechimpanzee.In chimpanzeefetuses,brain and head growth starts at about the same developmental stage and grow at a rate similar to that of humans, but growth stops soon after birth, whereas humans continue brain and head growth several years after birth. This particular type of heterochrony, hypermorphosis, 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. Humans have some 30 differentneoteniesin comparison to the chimpanzee, retaining larger heads, smaller jaws and noses, and shorter limbs, features found in juvenile chimpanzees.[50][51]
Related concepts
[edit]The term "heterokairy" was proposed in 2003 by John Spicer and Warren Burggren to distinguish plasticity in timing of the onset of developmental events at the level of an individual (heterokairy) or population (heterochrony).[52]
See also
[edit]References
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