Heterochrony

In evolutionary developmental biology, heterochrony is a developmental change in the timing or rate of events, leading to changes in size and shape of organs and features over evolutionary time scales. It is contrasted with heterotopy, a change in spatial positioning of some process in the embryo, which can also create morphological innovation. Heterochrony can be divided into intraspecific heterochrony that explains variation within a species, and interspecific heterochrony that explains developmental variation phylogenetically, in the timing or rate of events of a descendent species with respect to an ancestral species.[2]

These changes all affect the start, end, rate, or timespan of a particular developmental process.[3] The concept of heterochrony was introduced by Ernst Haeckel in 1875,[4][5] and given its modern sense by Gavin de Beer in 1930.

Girafeskoure
Giraffes acquired their long necks through heterochrony, extending the growth of the seven neck vertebrae by extending the development of bone growth in the embryo, not by adding more bones.[1]

History

Haeckel vs von Baer
Ernst Haeckel supposed that embryonic development recapitulated an animal's phylogeny, and introduced heterochrony as an exception for individual organs. Modern biology agrees instead with Karl Ernst von Baer's view that development itself varies, such as by changing the timing of different processes, to cause a branching phylogeny.[6]

The concept of heterochrony was introduced by the German zoologist Ernst Haeckel in 1875, where he used it to define deviations from recapitulation theory, which held that "ontogeny recapitulates phylogeny".[4] As Stephen Jay Gould pointed out, Haeckel's term is now used in a sense contrary to his coinage. He assumed that embryonic development (ontogeny) of "higher" animals recapitulated their ancestral development (phylogeny). 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 embryologist Gavin de Beer in 1930, to mean a change with respect to the development of the same organ in the animal's ancestors.[7][8]

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.[9]

De Beer anticipated evolutionary developmental biology in his 1930 book Embryos and Ancestors,[10] showing that evolution could occur by heterochrony, such as in paedomorphosis, the retention of juvenile features in the adult.[11][5] De Beer argued that this enabled rapid evolutionary change, too brief to be recorded in the fossil record, and in effect explaining why apparent gaps were likely.[12]

Mechanisms

Heterochrony
Diagram of the six types of shift in heterochrony, a change in the timing or rate of any process in embryonic development. Predisplacement, hypermorphosis, and acceleration extend development (peramorphosis, in red); postdisplacement, hypomorphosis, and deceleration all truncate it (paedomorphosis, in blue). These may be combined, e.g. to shift some aspect of development earlier.

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.[13] Reilly et al 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).[2]

Interspecific heterochrony means differences in the rate or timing of a descendent species relative to its ancestor. This can result in either paedomophosis (truncating the ancestral ontogeny), peramorphosis (extending past the ancestral ontogeny), or isomorphosis (reaching the same ancestral state via a different mechanism).[2]

There are three major mechanisms of heterochrony,[14][15][16][17] each of which can change in either of two directions, giving six types of perturbations, which can be combined in various ways.[18] These ultimately result in extended, shifted, or truncated development of a particular process, such as the action of a single toolkit gene,[19] 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.[2]

Okapi Giraffe Neck
Despite greatly differing neck lengths, giraffes (right) have no more cervical vertebrae, just 7, than their fellow giraffids, okapi (left). With the number constrained, the development of the vertebrae is extended, allowing them to grow longer.
  • 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.[20] Giraffes gain 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 mammalian diaphragm muscle; 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.[21]

Detection

Heterochrony can be identified by comparing phylogenetically close 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.[22] This method detects event heterochronies, as opposed to allometric changes. 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.[23] A recent method, continuous analysis, rests on a simple standardization of ontogenetic time or sequences, on squared change parsimony and phylogenetic independent contrasts.[24]

Effects

Paedomorphosis

AxolotlBE
Axolotls retain gills and fins as adults; these are juvenile features in most amphibians.

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.[25]

Neoteny retards the development of the organism into an adult, and has been described as "eternal childhood".[26] 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[27][28][29]), 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.[30]

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)[31] that is both hormonally[32][33] and genetically driven.[32] The entire metamorphosis that would allow the salamander to transition into the adult form is essentially blocked by both of these drivers.[34]

Paedomorphosis may play a critical role in avian cranial evolution.[35] The skulls and beaks of living, adult birds retain the anatomy of the juvenile theropod dinosaurs from which they evolved.[36] 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.[37] 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 juvenille morphology [38] Evidence from molecular experiments suggests both fibroblast growth factor 8 (FGF8) and members of the WNT signalling pathway have facilitated paedomorphosis in birds.[39] These signalling pathways are known to play roles in facial patterning in other vertebrate species.[40] 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.[38][41] This is believed to have facilitated the evolution of cranial kinesis in birds[38] which has played a critical role in their ecological success.[41]

Peramorphosis

Irish Elk front
Irish elk skeleton with antlers spanning 2.7 metres (8.9 ft) and a mass of 40 kg (88 lb)

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 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.[42][43]

Another example of peramorphosis is seen in insular (island) rodents. Their characteristics include gigantism, wider cheek and teeth, reduced litter size, 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.[44] With less predation and competition for resources, selection favored overdevelopment of these species. Reduced litter sizes enable overdevelopment of their bodies into larger ones.

Ascidia 005
A 1901 comparison of a frog tadpole (a vertebrate) and a tunicate larva; in 1928 Walter Garstang proposed that vertebrates derived from such a larva by neoteny.

The mole salamander, a close relative to the axolotl, displays both paedomorphosis and paramorphosis. 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.[45] 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.[46] 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).[44]

Across the animal kingdom

Heterochrony is responsible for a wide variety of effects[3] such as the lengthening of the fingers by adding extra phalanges in dolphins to form their flippers,[47] sexual dimorphism,[9] the neotenous origin of the vertebrates from a tunicate larva,[9] and the polymorphism seen between insect castes.[48]

Human development neoteny body and head proportions pedomorphy maturation aging growth
Neoteny in human development

In humans

Several heterochronies have been described in humans, relative to the chimpanzee. In chimpanzee fetuses, 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 different neotenies in comparison to the chimpanzee, retaining larger heads, smaller jaws and noses, and shorter limbs, features found in juvenile chimpanzees.[49][50]

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 or population.[51]

See also

References

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See also

Acceleration (disambiguation)

Acceleration, in physics, is the rate at which the velocity of a body changes over time.

Acceleration may also refer to:

Acceleration (biology), the speeding up of some part of embryonic development, a form of heterochrony

Acceleration (differential geometry), the rate of change of velocity of a curve with respect to a given linear connection

Acceleration (human), in developmental biology

Acceleration (law), a shortening of the time period in which something is to take place

Academic acceleration, the rapid advancement of students

Cardiotocographic acceleration, an apparent abrupt increase in fetal heart rate

Vehicular acceleration, usually controlled by a throttle such as an accelerator pedal in a car

The sensation of a change in speed

Series acceleration, in mathematics, a sequence transformation for improving the rate of convergence of a series

Acceleration (album)

Barameda

Barameda (Indigenous Australian language: "fish trap"is a genus of rhizodont lobe-finned fish which lived during the Tournasian stage near the start of the Carboniferous period in Australia. While many Paleozoic sarcopterygan fishes are identified by their fleshy lobe fins, fused skull cases and basal qualities, the primary identifier of most Barameda fossils comes from their large rooted fangs, usually 22 centimetres (8.7 in) in length, and where the order Rhizodontida and family Rhizodontidae gain their name. The largest member of this genus, Barameda decipiens, reached an estimated length of over 20 feet (6.1 m), rivaling another large rhizodont in size, Rhizodus. Species of Barameda were obligate carnivores, preying on freshwater invertebrates, early fish, and possibly early tetrapods to sustain its massive length.

Bradley C. Livezey

Bradley Curtis Livezey (June 15, 1954 – February 8, 2011) was an American ornithologist with scores of publications. His main research included the evolution of flightless birds, the systematics of birds, and the ecology and behaviour of steamer ducks.

Cranial evolutionary allometry

Cranial evolutionary allometry (CREA) is a scientific theory regarding trends in the shape of mammalian skulls during the course of evolution in accordance with body size (i.e., allometry). Specifically, the theory posits that there is a propensity among closely related mammalian groups for the skulls of the smaller species to be short and those of the larger species to be long. This propensity appears to hold true for placental as well as non-placental mammals, and is highly robust. Examples of groups which exhibit this characteristic include antelopes, fruit bats, mongooses, squirrels and kangaroos as well as felids.It is believed that the reason for this trend has to do with size-related constraints on the formation and development of the mammalian skull. Facial length is one of the best known examples of heterochrony.

David B. Weishampel

Professor David Bruce Weishampel (born November 16, 1952) is an American palaeontologist in the Center for Functional Anatomy and Evolution at Johns Hopkins University School of Medicine. Weishampel received his Ph.D. in Geology from the University of Pennsylvania in 1981. His research focuses include dinosaur systematics, European dinosaurs of the Late Cretaceous, jaw mechanics and herbivory, cladistics and heterochrony and the history of evolutionary biology. Weishampel's best known published work is The Dinosauria University of California Press; 2nd edition (December 1, 2004). He consulted for Jurassic Park and is a good friend of Steven Spielberg. He has received an Academy Scientific and Technical Award.

Elpistostegalia

Elpistostegalia or Panderichthyida is an order of prehistoric lobe-finned fishes which lived during the Late Devonian period (about 385 to 374 million years ago). They represent the advanced tetrapodomorph stock, the fishes more closely related to tetrapods than the osteolepiform fishes. The earliest elpistostegalians, combining fishlike and tetrapod-like characters, are sometimes called fishapods, a phrase coined for the advanced elpistostegalian Tiktaalik.

Gavin de Beer

Sir Gavin Rylands de Beer (1 November 1899 – 21 June 1972) was a British evolutionary embryologist, known for his work on heterochrony as recorded in his 1930 book Embryos and Ancestors. He was director of the Natural History Museum, London, president of the Linnean Society of London, and a winner of the Royal Society's Darwin Medal for his studies on evolution.

Heterotopy

Heterotopy is an evolutionary change in the spatial arrangement of an animal's embryonic development, complementary to heterochrony, a change to the rate or timing of a development process. It was first identified by Ernst Haeckel in 1866 and has remained less well studied than heterochrony.

Incisoscutum

Incisoscutum is a genus of arthrodire placoderm from the Late Frasnian Gogo Reef, from Late Devonian Australia. The genus contains two species I. ritchiei, named after Dr. Alex Ritchie, a palaeoichthyologist and senior fellow of the Australian Museum, and I. sarahae, named after Sarah Long, daughter of its discoverer and describer, Dr. John A. Long.

The genus is important in the study of early vertebrates as well-preserved fossilised embryos have been found in female specimens and ossified pelvic claspers found in males. This shows that viviparity and internal fertilisation was common amongst these primitive jawed vertebrates, which are outside the crown group Gnathostoma.

In a study of fossil remains, comparison of the ontogeny of fourteen dermal plates from Compagopiscis croucheri and the more derived species Incisoscutum ritchiei suggested that lengthwise growth occurs earlier in the ontogeny than growth in width, and that dissociated allometric heterochrony has been an important mechanism in the evolution of the arthrodires, which include placoderms.

These same fossil specimens also show that Incisoscutum was a predator, as muscle fibres from the tails of other placoderms have been found in the stomach regions.

Maotherium

Maotherium is a genus extinct symmetrodont mammal that was discovered in Early Cretaceous rocks in Liaoning Province, China, in 2003. Its scientific name means "Mao's beast" after the Chinese politician Mao Zedong. Maotherium belongs to an extinct group of Mesozoic mammals called symmetrodonts. Though little is known about this group, the symmetrodonts have several similarities - specifically their teeth. They have tall pointed, but simple molars in a triangular arrangement. Originally symmetrodonts were known since the 1920s. Now a vast majority have been restored, such as Zhangheotherium and Akidolestes, during the early 21st century. One of the fossils of Maotherium preserved the imprints of fur, like the mammals Eomaia and Sinodelphys.

A species described in 2009, Maotherium asiaticus, sheds light on the evolution of the mammalian middle ear. In modern mammals, the Meckel's cartilage appears during development but disappears before adulthood. In Maotherium asiaticus, that cartilage not only remained, but turned into bone.

This event in evolution may be an example of heterochrony, a change in the timing of development.

Mapusaurus

Mapusaurus ("Earth lizard") was a giant carnosaurian, Carcharodontosaurid dinosaur from the early Late Cretaceous (late Cenomanian to early Turonian stage) of what is now Argentina and possibly Chile.

Metatrochophore

A metatrochophore (;) is a type of larva developed from the trochophore larva of a polychaete annelid.

Metatrochophores have a number of features trochophores lack, including eyespots and segments.

Neoteny

Neoteny (, or ), also called juvenilization, is the delaying or slowing of the physiological (or somatic) development of an organism, typically an animal. Neoteny is found in modern humans. In progenesis (also called paedogenesis), sexual development is accelerated.Both neoteny and progenesis result in paedomorphism (or paedomorphosis), a type of heterochrony. Some authors define paedomorphism as the retention of larval traits, as seen in salamanders.Both neoteny and progenesis cause the retention in adults of traits previously seen only in the young. Such retention is important in evolutionary biology, domestication and evolutionary developmental biology.

Ontogeny and Phylogeny (book)

Ontogeny and Phylogeny is a 1977 book on evolution by Stephen Jay Gould, in which the author explores the relationship between embryonic development (ontogeny) and biological evolution (phylogeny). Unlike his many popular books of essays, it was a technical book, and over the following decades it was influential in stimulating research into heterochrony, changes in the timing of embryonic development, which had been neglected since Ernst Haeckel's theory that ontogeny recapitulates phylogeny had been largely discredited.

René Zazzo

René Zazzo (27 October 1910 - September 1995) was a French psychologist and pedagogue.

The essence of Zazzo's research related to child psychology. He was one of the first people to study a group of problems relating to dyslexia and disability. Considering the development of children considered to be weak, Zazzo proposed the concept of "oligophrenic heterochrony" in order to show that this development, compared with that of normal children, occurred at various speeds, according to the particular psychobiological sector concerned. The majority of research which Zazzo produced between 1950 and 1980 centered on what he regarded as "the principal problem of psychology"—that of the identity: how does a person's psyche build itself? The fields in which he worked were various attempts to bring answers to this question.

Richard Goldschmidt

Richard Benedict Goldschmidt (April 12, 1878 – April 24, 1958) was a German-born American geneticist. He is considered the first to attempt to integrate genetics, development, and evolution. He pioneered understanding of reaction norms, genetic assimilation, dynamical genetics, sex determination, and heterochrony. Controversially, Goldschmidt advanced a model of macroevolution through macromutations popularly known as the "Hopeful Monster" hypothesis.Goldschmidt also described the nervous system of the nematode, a piece of work that influenced Sydney Brenner to study the wiring diagram of Caenorhabditis elegans, winning Brenner and his colleagues the Nobel Prize in 2002.

Ryuichi Matsuda

Ryuichi Matsuda (July 8, 1920 – June 19, 1986) was a Japanese entomologist.He obtained his PhD in entomology from Stanford University. He worked at the Biosystematics Research Institute of Canada.He wrote several works on the comparative morphology of insects. He is most well known for his controversial book Animal Evolution in Changing Environments (1987).He coined the term "pan-environmentalism" for his evolutionary theory which he saw as a fusion of Darwinism with neo-Lamarckism. He held that heterochrony is a main mechanism for evolutionary change and that novelty in evolution can be generated by genetic assimilation. His views were criticized by Arthur M. Shapiro for providing no solid evidence for his theory. Shapiro noted that "Matsuda himself accepts too much at face value and is prone to wish-fulfilling interpretation."Interest in Matsuda's research was revived by Brian K. Hall, Gerd B. Müller and others in the volume Environment, Development, and Evolution: Toward a Synthesis (2004) which was a tribute to his ideas.

Trochophore

A trochophore (; also spelled trocophore) is a type of free-swimming planktonic marine larva with several bands of cilia.

By moving their cilia rapidly, a water eddy is created. In this way they control the direction of their movement. Additionally, in this way they bring their food closer, in order to capture it more easily.

Key concepts
Genetic architecture
Non-genetic influences
Developmental architecture
Evolution of genetic systems
Control of development
Influential figures
Debates

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