Heterochrony
In
These changes all affect the start, end, rate or time span of a particular developmental process. The concept of heterochrony was introduced by Ernst Haeckel in 1875 and given its modern sense by Gavin de Beer in 1930.
History
![](http://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 zoologist
In 1928, the English embryologist Walter Garstang showed that tunicate larvae shared structures such as the notochord with adult vertebrates, and suggested that the vertebrates arose by paedomorphosis (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]
Modern
Mechanisms
![](http://upload.wikimedia.org/wikipedia/commons/thumb/e/ee/Heterochrony.svg/370px-Heterochrony.svg.png)
Heterochrony can be divided into intraspecific and interspecific types.
Intraspecific heterochrony means changes in the rate or timing of development within a species. For example, some individuals of the salamander species Ambystoma talpoideum delay the metamorphosis of the skull.[11] Reilly and colleagues argue we can define these variant individuals as paedotypic (with truncated development relative to the ancestral condition), peratypic (with extended development relative to the ancestral condition), or isotypic (reaching the same ancestral shape, but via a different mechanism).[10]
Interspecific heterochrony means differences in the rate or timing of a descendant species relative to its ancestor. This can result in either paedomophosis (truncating the ancestral ontogeny),
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 single toolkit 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]
![](http://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, hypomorphosis or progenesis, 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 a body plan is seen in snakes. 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 sinuous locomotion. Snake embryos achieve this by accelerating their system for creating somites (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]
Detection
Heterochrony can be identified by comparing
Effects
Paedomorphosis
Paedomorphosis can be the result of neoteny, 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 the axolotl (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 in avian cranial evolution.[33] The skulls and beaks of living, adult birds retain the anatomy of the juvenile theropod dinosaurs from 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 by Coelophysis) 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 both fibroblast growth factor 8 (FGF8) and members of the WNT signalling pathway have 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
![](http://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 extinct Irish 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, the moose. 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, reduced
The mole 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 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 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
Heterochrony is responsible for a wide variety of effects
Garstang's hypothesis
Walter Garstang suggested the neotenous origin of the vertebrates from a tunicate larva,[6] in opposition to Darwin's opinion that tunicates and vertebrates both evolved from animals whose adult form was similar to (frog) tadpoles and the 'tadpole larvae' of tunicates. According to Richard Dawkins,[48] Garstang's opinion was also held by Alister 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 the larvaceans constitute 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
![](http://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
Several heterochronies have been described in humans, relative to the
Related concepts
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
- Ontogeny and Phylogeny
References
- ^ ISBN 978-1-4641-6298-5.
- ^ PMID 14756324.
- ^ Horder, Tim (April 2006). "Heterochrony". Encyclopedia of Life Sciences. Chichester: John Wiley & Sons.
- )
- S2CID 89098289.
- ^ .
- ISBN 978-1-107-62139-8.
- ISBN 978-0-674-63940-9.
- PMID 16506229.
- ^ .
- S2CID 49315190.
- OCLC 2508336.
- ISBN 978-0674503120.
- ISBN 978-0387113319.
- S2CID 84119618.
- PMID 28567993.
- PMID 18614008.
- ISBN 978-1-107-62139-8.
- ISBN 978-1-107-62139-8.
- PMID 11975352.
- PMID 16012094.
- S2CID 22629275.
- ^ Smith, Charles Kay (1990). "A model for understanding the evolution of mammalian behavior". Current Mammalogy. 2: 335–374.
- OCLC 59288040.
- PMID 19307592.
- PMID 21788513.
- PMID 24411938.
- .
- )
- ^ .
- OCLC 682061358.
- OCLC 29357502.
- PMID 27371392.
- S2CID 4370675.
- ^ Zusi, R. L. (1993). The skull, vol 2: patterns of structural and systematic diversity. University of Chicago Press. pp. 391–437.
- ^ PMID 27371392.
- S2CID 205124061.
- PMID 12642481.
- ^ PMID 11733177.
- ISBN 978-1605351155.
- ^ Moen, Ron A.; John Pastor; Yosef Cohen (1999). "Antler growth and extinction of Irish elk". Evolutionary Ecology Research. 1 (2): 235–249.
- ^ PMID 20854657.
- JSTOR 1938370.
- PMID 10983835.
- ISBN 978-1-107-62139-8.
- S2CID 15429067.
- PMID 10761593.
- ISBN 978-0-7538-1996-8.
- ISBN 978-0752873213.
- PMID 15183670.
- S2CID 15566858.
- S2CID 13558790.
See also
- Developmental biology
- Embryogenesis
- Evolutionary biology
- Phylogeny