Neoteny

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Neoteny ( /niˈɒtəni/ ), [1] [2] [3] [4] also called juvenilization, [5] is the delaying or slowing of the physiological (or somatic) development of an organism, typically an animal. Neoteny is found in modern humans. [6] In progenesis (also called paedogenesis), sexual development is accelerated. [7]

Contents

Both neoteny and progenesis result in paedomorphism (or paedomorphosis), a type of heterochrony. [8] It is the retention in adults of traits previously seen only in the young. Such retention is important in evolutionary biology, domestication and evolutionary developmental biology.

Some authors define paedomorphism as the retention of larval traits, as seen in salamanders. [9] [10] [11]

History and etymology

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 (red) extend development (peramorphosis); postdisplacement, hypomorphosis, and deceleration (blue) all truncate it (paedomorphosis). Heterochrony.svg
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 (red) extend development (peramorphosis); postdisplacement, hypomorphosis, and deceleration (blue) all truncate it (paedomorphosis).

The origins of the concept of neoteny have been traced to the Bible (as argued by Ashley Montagu) and to the poet William Wordsworth's "The Child is the father of the Man" (as argued by Barry Bogin). The term itself was invented in 1885 by Julius Kollmann as he described the axolotl's maturation while remaining in a tadpole-like aquatic stage complete with gills, unlike other adult amphibians like frogs and toads. [12]

The word neoteny is borrowed from the German Neotenie, the latter constructed by Kollmann from the Greek νέος (neos, "young") and τείνειν (teínein, "to stretch, to extend"). The adjective is either "neotenic" or "neotenous". [13] For the opposite of "neotenic", different authorities use either "gerontomorphic" [14] [15] or "peramorphic". [16] Bogin points out that Kollmann had intended the meaning to be "retaining youth", but had evidently confused the Greek teínein with the Latin tenere, which had the meaning he wanted, "to retain", so that the new word would mean "the retaining of youth (into adulthood)". [12]

In 1926, Louis Bolk described neoteny as the major process in humanization. [12] In his 1977 book Ontogeny and Phylogeny , [17] Stephen Jay Gould noted that Bolk's account constituted an attempted justification for "scientific" racism and sexism, but acknowledged that Bolk had been right in the core idea that humans differ from other primates in becoming sexually mature in an infantile stage of body development. [12]

In humans

Neoteny in humans is the slowing or delaying of body development, compared to non-human primates, resulting in features such as a large head, a flat face, and relatively short arms. These neotenic changes may have been brought about by sexual selection in human evolution. In turn, they may have permitted the development of human capacities such as emotional communication. However, humans also have relatively large noses and long legs, both peramorphic (not neotenic) traits. Some evolutionary theorists have proposed that neoteny was a key feature in human evolution. [18] Gould argued that the "evolutionary story" of humans is one where we have been "retaining to adulthood the originally juvenile features of our ancestors". [19] J. B. S. Haldane mirrors Gould's hypothesis by stating a "major evolutionary trend in human beings" is "greater prolongation of childhood and retardation of maturity." [5] Delbert D. Thiessen said that "neoteny becomes more apparent as early primates evolved into later forms" and that primates have been "evolving toward flat face." [20] However, in light of some groups using neoteny-based arguments to support racism, Gould also argued "that the whole enterprise of ranking groups by degree of neoteny is fundamentally unjustified" (Gould, 1996, pg. 150). [21] Doug Jones argued that human evolution's trend toward neoteny may have been caused by sexual selection in human evolution for neotenous facial traits in women by men with the resulting neoteny in male faces being a "by-product" of sexual selection for neotenous female faces. [22]

In domestic animals

Neoteny is seen in domesticated animals such as dogs and mice. [23] This is because there are more resources available, less competition for those resources, and with the lowered competition the animals expend less energy obtaining those resources. This allows them to mature and reproduce more quickly than their wild counterparts. [23] The environment that domesticated animals are raised in determines whether or not neoteny is present in those animals. Evolutionary neoteny can arise in a species when those conditions occur, and a species becomes sexually mature ahead of its "normal development". Another explanation for the neoteny in domesticated animals can be the selection for certain behavioral characteristics. Behavior is linked to genetics which therefore means that when a behavioral trait is selected for, a physical trait may also be selected for due to mechanisms like linkage disequilibrium. Often, juvenile behaviors are selected for in order to more easily domesticate a species; aggressiveness in certain species comes with adulthood when there is a need to compete for resources. If there is no need for competition, then there is no need for aggression. Selecting for juvenile behavioral characteristics can lead to neoteny in physical characteristics because, for example, with the reduced need for behaviors like aggression, there is no need for developed traits that would help in that area. Traits that may become neotenized due to decreased aggression may be a shorter muzzle and smaller general size among the domesticated individuals. Some common neotenous physical traits in domesticated animals (mainly dogs, pigs, ferrets, cats, and even foxes) include floppy ears, changes in the reproductive cycle, curly tails, piebald coloration, fewer or shortened vertebra, large eyes, rounded forehead, large ears, and shortened muzzle. [24] [25]

Neoteny and reduction in skull size - grey wolf and chihuahua skulls Unnatural selection, 2 heads, one species.jpg
Neoteny and reduction in skull size – grey wolf and chihuahua skulls

When the role of dogs expanded from just being working dogs to also being companions, humans started selective breeding dogs for morphological neoteny, and this selective breeding for "neoteny or paedomorphism" "strengthened the human-canine bond." [26] Humans bred dogs to have more "juvenile physical traits" as adults, such as short snouts and wide-set eyes which are associated with puppies because people usually consider these traits to be more attractive. Some breeds of dogs with short snouts and broad heads such as the Komondor, Saint Bernard and Maremma Sheepdog are more morphologically neotenous than other breeds of dogs. [27] Cavalier King Charles spaniels are an example of selection for neoteny because they exhibit large eyes, pendant-shaped ears and compact feet, giving them a morphology similar to puppies as adults. [26]

In 2004, a study that used 310 wolf skulls and over 700 dog skulls representing 100 breeds concluded that the evolution of dog skulls can generally not be described by heterochronic processes such as neoteny, although some pedomorphic dog breeds have skulls that resemble the skulls of juvenile wolves. [28] By 2011, the findings by the same researcher were simply "Dogs are not paedomorphic wolves." [29]

In other species

The axolotl is a neotenous salamander, often retaining gills throughout its life. Axolotl ganz.jpg
The axolotl is a neotenous salamander, often retaining gills throughout its life.

Neoteny has been observed in many other species. It is important to note the difference between partial and full neoteny when looking at other species, to distinguish between juvenile traits which are advantageous in the short term and traits which are beneficial throughout the organism's life; this might provide insight into the cause of neoteny in a species. Partial neoteny is the retention of the larval form beyond the usual age of maturation, with possible sexual development (progenesis) and eventual maturation into the adult form; this is seen in Lithobates clamitans . Full neoteny is seen in Ambystoma mexicanum and some populations of Ambystoma tigrinum , which remain in larval form throughout their lives. [30] [31] Lithobates clamitans is partially neotenous; it delays maturation during winter season because fewer resources are available, and it can find existing resources more easily in larval form. This encompasses both of the main causes of neoteny; the energy required to survive in the winter as a newly-formed adult is too great, so the organism exhibits neotenous characteristics until it can better survive as an adult. Ambystoma tigrinum retains its neoteny for a similar reason; however, the retention is permanent due to the lack of available resources throughout its lifetime. This is another example of an environmental cause of neoteny. Several avian species, such as the manakins Chiroxiphia linearis and Chiroxiphia caudata , exhibit partial neoteny. The males of both species retain juvenal plumage into adulthood, losing it when they are fully mature. [32] In some bird species, the retention of juvenile plumage is linked to the molting time in each species. To ensure no overlap between molting and mating times, the birds may exhibit partial neoteny in plumage; males do not attain their bright, adult plumage before the females are prepared to mate. Neoteny is present because there is no need for the males to molt early, and trying to mate with immature females would be energy-inefficient.

Neoteny is commonly seen in flightless insects, such as the females of the order Strepsiptera. Flightlessness in insects has evolved separately a number of times; factors which may have contributed to the separate evolution of flightlessness are high altitude, geographic isolation (islands), and low temperatures. [33] Under these environmental conditions, dispersal would be disadvantageous; heat is lost more rapidly through wings in colder climates. The females of certain insect groups become sexually mature without metamorphosis, and some do not develop wings. Flightlessness in some female insects has been linked to higher fecundity. [33] Aphids are an example of insects which may never develop wings, depending on their environment. If resources are abundant on a host plant, there is no need to grow wings and disperse. If resources become diminished, their offspring may develop wings to disperse to other host plants. [34]

Two environments which favor neoteny are high altitudes and cool temperatures, because neotenous individuals have more fitness than individuals which metamorphose into an adult form. The energy required for metamorphosis detracts from individual fitness, and neotenous individuals can utilize available resources more easily. [35] This trend is seen in a comparison of salamander species at lower and higher altitudes; in a cool, high-altitude environment, neotenous individuals survive more and are more fecund than those which metamorphose into adult form. [35] Insects in cooler environments tend to exhibit neoteny in flight because wings have a high surface area and lose heat quickly; it is disadvantageous for insects to metamorphose into adults. [33]

Many species of salamander, and amphibians in general, exhibit environmental neoteny. Axolotl and olm are salamander species which retain their juvenile aquatic form throughout adulthood, examples of full neoteny. Gills are a common juvenile characteristic in amphibians which are kept after maturation; examples are the tiger salamander and rough-skinned newt, both of which retain gills into adulthood. [30]

Bonobos share many physical characteristics with humans, including neotenous skulls. [36] The shape of their skull does not change into adulthood (only increasing in size), due to sexual dimorphism and an evolutionary change in the timing of development. [36] Juveniles became sexually mature before their bodies had fully developed as adults and, due to a selective advantage, the skull's neotenic structure remained.[ citation needed ]

In some groups, such as the insect families Gerridae, Delphacidae and Carabidae, energy costs result in neoteny; many species in these families have small, neotenous wings or none at all. [34] Some cricket species shed their wings in adulthood; [37] in the genus Ozopemon , males (thought to be the first example of neoteny in beetles) are significantly smaller than females due to inbreeding. [38] In the termite Kalotermes flavicollis , neoteny is seen in molting females. [39]

In other species, such as the northwestern salamander (Ambystoma gracile), environmental conditions high altitude, in this case cause neoteny. [40] Neoteny is also found in a few species of the crustacean family Ischnomesidae, which live in deep ocean water. [41]

Subcellular neoteny

Neoteny is usually used to describe animal development; however, neoteny is also seen in the cell organelles. It was suggested that subcellular neoteny could explain why sperm cells have atypical centrioles. One of the two sperm centrioles of fruit fly exhibit the retention of “juvenile” centriole structure, which can be described as centriolar “neoteny”. This neotenic, atypical centriole is known as the Proximal Centriole-Like. Typical centrioles form via a step by step process in which a cartwheel forms, then develops to become a procentriole, and further matures into a centriole. The neotenic centriole of fruit fly resembles an early procentriole. [42]

See also

Related Research Articles

Metamorphosis Profound change in body structure during the postembryonic development of an organism

Metamorphosis is a biological process by which an animal physically develops after birth or hatching, involving a conspicuous and relatively abrupt change in the animal's body structure through cell growth and differentiation. Some insects, fish, amphibians, mollusks, crustaceans, cnidarians, echinoderms, and tunicates undergo metamorphosis, which is often accompanied by a change of nutrition source or behavior. Animals can be divided into species that undergo complete metamorphosis ("holometaboly"), incomplete metamorphosis ("hemimetaboly"), or no metamorphosis ("ametaboly").

Salamander Order of amphibians (Urodela)

Salamanders are a group of amphibians typically characterized by a lizard-like appearance, with slender bodies, blunt snouts, short limbs projecting at right angles to the body, and the presence of a tail in both larvae and adults. All 10 present-day salamander families are grouped together under the order Urodela. Salamander diversity is highest in the Northern Hemisphere and most species are found in the Holarctic realm, with some species present in the Neotropical realm.

Larva Juvenile form of distinct animals before metamorphosis

A larva is a distinct juvenile form many animals undergo before metamorphosis into adults. Animals with indirect development such as insects, amphibians, or cnidarians typically have a larval phase of their life cycle.

Axolotl Species of amphibian (salamander)

The axolotl, Ambystoma mexicanum, also known as the Mexican walking fish, is a neotenic salamander related to the tiger salamander. Although colloquially known as a "walking fish", the axolotl is not a fish but an amphibian. The species was originally found in several lakes, such as Lake Xochimilco underlying Mexico City. Axolotls are unusual among amphibians in that they reach adulthood without undergoing metamorphosis. Instead of developing lungs and taking to the land, adults remain aquatic and gilled.

Mole salamander

The mole salamanders are a group of advanced salamanders endemic to North America. The group has become famous due to the presence of the axolotl, widely used in research due to its paedomorphosis, and the tiger salamander which is the official amphibian of many states, and often sold as a pet.

Sexual maturity is the capability of an organism to reproduce. It may be considered synonymous with adulthood, but, in humans, puberty encompasses the process of sexual maturation and adulthood is based on cultural definitions.

Cuteness Subjective physical trait

Cuteness is a subjective term describing a type of attractiveness commonly associated with youth and appearance, as well as a scientific concept and analytical model in ethology, first introduced by Konrad Lorenz. Lorenz proposed the concept of baby schema (Kindchenschema), a set of facial and body features, that make a creature appear "cute" and activate ("release") in others the motivation to care for it. Cuteness may be ascribed to people as well as things that are regarded as attractive or charming.

Heterochrony Evolutionary change in the rates or durations of developmental events, leading to structural changes

In evolutionary developmental biology, heterochrony is any genetically controlled difference in the timing or duration of a developmental process in an organism compared to its ancestors or other organisms. This leads to changes in the size, shape, characteristics and even presence of certain organs and features. 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, variation within a species, and interspecific heterochrony, phylogenetic variation, i.e. variation of a descendant species with respect to an ancestral species.

Common mudpuppy Species of salamander

The common mudpuppy is a species of salamander in the genus Necturus. They live an entirely aquatic lifestyle in parts of North America in lakes, rivers, and ponds. They go through paedomorphosis and retain their external gills. Because skin and lung respiration alone is not sufficient for gas exchange, mudpuppies must rely on external gills as their primary means of gas exchange. They are usually a rusty brown color and can grow to an average length of 24 in (609.5 mm). Mudpuppies are nocturnal creatures, and come out during the day only if the water in which they live is murky. Their diet consists of almost anything they can get in their mouths, including insects, mollusks, and earthworms. Once a female mudpuppy reaches sexual maturity at six years of age, she can lay an average of 60 eggs. In the wild, the average lifespan of a mudpuppy is 11 years.

Taylors salamander

Taylor's salamander, Ambystoma taylori, is a species of salamander found only in Laguna Alchichica, a high-altitude crater lake to the southwest of Perote, Puebla, Mexico. It was first described in 1982 but had been known to science prior to that. It is a neotenic salamander, breeding while still in the larval state and not undergoing metamorphosis. The lake in which it lives is becoming increasingly saline and less suitable for the salamander, which is declining in numbers. The International Union for Conservation of Nature (IUCN) has rated it as being "critically endangered".

Gavin de Beer

Sir Gavin Rylands de Beer 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.

The Puerto Hondo stream salamander or Michoacan stream salamander, Ambystoma ordinarium, is a mole salamander from the Cordillera Volcánica within the Mexican state of Michoacán.

Yellow-peppered salamander

The yellow-peppered salamander also known as the salamandra de Champala and the yellow-headed salamander, is a species of mole salamander native to areas at an elevation of 4900 ft around Santa Cruz, Rancho Malveste and Tapalpa in Jalisco, Mexico.

<i>Ambystoma talpoideum</i>

Ambystoma talpoideum, the mole salamander, is a species of salamander found in much of the eastern and central United States, from Florida to Texas, north to Illinois, east to Kentucky, with isolated populations in Virginia and Indiana. Older sources often refer to this species as the tadpole salamander because some individuals remain in a neotenic state. This salamander lives among the leaf litter on the forest floor, migrating to ponds to breed.

<i>Ontogeny and Phylogeny</i> (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.

Self-domestication is the process of adaptation of wild animals to cohabiting with humans, without direct human selective breeding of the animals. Dogs and cats have undergone this kind of self-domestication. Self-domestication also refers to the evolution of hominids, particularly humans and bonobos, toward collaborative, docile behavior. As described by British biological anthropologist Richard Wrangham, self-domestication involves being in an environment that favors reduction in aggression, including interspecific and intraspecific antagonism, for survival. Spandrels, or evolutionary byproducts, also accompany self-domestication, including depigmentation, arrested development, and reduced sexual dimorphism.

<i>Apateon</i>

Apateon is an extinct genus of temnospondyl amphibian within the family Branchiosauridae.


Purebred breeders are dog breeders that intentionally breed purebred dogs specifically to continue the lineage of certain breed characteristics in dogs by mating selected canines.

Branchiosauridae

Branchiosauridae is an extinct family of small amphibamiform temnospondyls with external gills and an overall juvenile appearance. The family has been characterized by hundreds of well-preserved specimens from the Permo-Carboniferous of Middle Europe. Specimens represent well defined ontogenetic stages and thus the taxon has been described to display paedomorphy (perennibranchiate). However, more recent work has revealed branchiosaurid taxa that display metamorphosing trajectories. The name Branchiosauridae refers to the retention of gills.

Neoteny in humans

Neoteny in humans is the retention of juvenile features well into adulthood. This trend is greatly amplified in humans especially when compared to non-human primates. Adult humans more closely resemble the infants of gorillas and chimpanzees than the adults. Neotenic features of the head include the globular skull; thinness of skull bones; the reduction of the brow ridge; the large brain; the flattened and broadened face; the hairless face; hair on the head; larger eyes; ear shape; small nose; small teeth; and the small maxilla and mandible.

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Further reading