neoteny

File:Heterochrony.svg, 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).]]

Julius Kollmann created the term "neoteny" in 1885 after 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.{{cite journal |last=Kollmann |first=J. |title=Das Ueberwintern von europäischen Frosch- und Tritonlarven und die Umwandlung des mexikanischen Axolotl |journal=Verhandlungen der Naturforschenden Gesellschaft in Basel (Proceedings of the Natural Science Society of Basel) |date=1885 |volume=7 |pages=387–398 |url=https://www.biodiversitylibrary.org/item/42693#page/397/mode/1up |trans-title=The overwintering of European frog- and triton larvae and the transformation of the Mexican axolotl |language=German}} From pp. 397–398: "Dann drängt sich die Frage auf, ob das Latenzstadium der Eier, das einerseits bei Fischen, Vögeln and Säugethieren in so höchst überraschenden Formen vorkommt, anderseits das Latenzstadium bei den Wirbellosen ¹) nicht eine Variante derselben Eigenschaft der Organismen sei, welche ich Neotenie genannt habe, und die auf irgend einer Entwichlungsstufe in Kraft treten kann." (Then the question arises whether on the one hand the latency stage of eggs — which occurs in such highly surprising forms in fish, birds and mammals — [and] on the other hand the latency stage in invertebrates ¹) be not a variant of the same property of the organisms, which I have called "neoteny" and which can come into force at any stage of development.){{cite book |last=Bogin |first=Barry |title=Patterns of Human Growth |url=https://books.google.com/books?id=ScfPjwF3BngC&pg=PA158 |year=1999 |publisher=Cambridge University Press |isbn=978-0-521-56438-0 |pages=157–169}}

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".[http://www.thefreedictionary.com/neoteny Neoteny], The Free Dictionary. 2011. Accessed April 30, 2011. For the opposite of "neotenic", different authorities use either "gerontomorphic"Henke, W. (2007). Handbook of paleoanthropology, Volume 1. Springer Books, NY.Hetherington, R. (2010). The Climate Connection: Climate Change and Modern Human Evolution. Cambridge University Press. or "peramorphic".Hall, B.K., Hallgrímsson, B. Monroe, W.S. (2008). Strickberger's evolution: the integration of genes, organisms and populations. Jones and Bartlett Publishers: Canada. 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)".

In 1926, Louis Bolk described neoteny as the major process in humanization.{{cite book |last=Bolk |first=Louis |title=Das Problem der Menschwerdung : Vortrag gehalten am 15. April 1926 auf der XXV. Versammlung der anatomischen Gesellschaft zu Freiburg |trans-title=The Problem of Humanization: Lecture held on 15 April 1926 at the 25th Congress of the Anatomical Society at Freiberg |date=1926 |publisher=Gustav Fischer |location=Jena, Germany |language=German}} In his 1977 book Ontogeny and Phylogeny,{{cite book |last1=Gould |first1=Stephen Jay |title=Ontogeny and Phylogeny |date=1977 |publisher=Belknap (Harvard University Press) |location=Cambridge, Massachusetts |isbn=978-0-674-63940-9 |url=https://archive.org/details/ontogenyphylogen00goul }} 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.

{{main|Neoteny 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. Some evolutionary theorists have proposed that neoteny was a key feature in human evolution.{{cite journal |last=Shea |first=Brian T. |title=Heterochrony in human evolution: The case for neoteny reconsidered |journal=American Journal of Physical Anthropology |date=1989 |volume=32 |issue=S10 |pages=69–101 |doi=10.1002/ajpa.1330320505}} J. B. S. Haldane states a "major evolutionary trend in human beings" is "greater prolongation of childhood and retardation of maturity." 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."Thiessen, D.D. (1997). Bittersweet destiny: the stormy evolution of human behavior. Transaction Publishers, N.J. 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.{{cite journal |last1=Jones |first1=D. |display-authors=etal |year=1995 |title=Sexual selection, physical attractiveness, and facial neoteny: Cross-cultural evidence and implications [and comments and reply] |url=https://digitalcommons.usu.edu/cgi/viewcontent.cgi?article=1601&context=fchd_facpub|journal=Current Anthropology |volume=36 |issue=5 |pages=723–748 |doi=10.1086/204427 |s2cid=52840802 |url-access=subscription }}

{{further|Domestication of animals}}

Neoteny is seen in domesticated animals such as dogs and mice.{{cite journal |last=Price |first=E. |year=1999 |title=Behavioral development in animals undergoing domestication |journal=Applied Animal Behaviour Science |volume=65 |issue=3 |pages=245–271 |doi=10.1016/S0168-1591(99)00087-8}} 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. 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 rabbits, 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.{{cite book |last1=Vonk |first1=Jennifer |last2=Shackelford |first2=Todd |chapter=Neoteny |title=Encyclopedia of Animal Cognition and Behavior |publisher=Springer |date=1 April 2022 |pages=4590–4592 |isbn=978-3-319-55064-0 }}Bertone, J. (2006). Equine geriatric medicine and surgery. Saunders, MI.{{cite journal |last=Trut |first=L. N. |year=1999 |title=Early canid domestication: the farm-fox experiment |journal=American Scientist |volume=87 |issue=2 |pages=160–169 |doi=10.1511/1999.2.160 |bibcode=1999AmSci..87.....T }}

File:Unnatural selection, 2 heads, one species.jpg 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." 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.Beck, A.M. & Katcher, A.H. (1996). Between Pets and People: The Importance of Companionship. West Lafayette, Indiana: Purdue University Press. {{ISBN|1-55753-077-7}} 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.McGreevy, P.D. & Nicholas, F.W. (1999). Some Practical Solutions to Welfare Problems in Dog Breeding. In Animal Welfare. 8: 329–341.

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.Drake, Abby Grace, "Evolution and development of the skull morphology of canids: An investigation of morphological integration and heterochrony" (January 1, 2004). Doctoral Dissertations Available from Proquest. Paper AAI3136721. [http://scholarworks.umass.edu/dissertations/AAI3136721 link] By 2011, the findings by the same researcher were simply "Dogs are not paedomorphic wolves."{{cite journal |last1=Drake |first1=Abby Grace |doi=10.1111/j.1525-142X.2011.00470.x |pmid=21410876 |title=Dispelling dog dogma: An investigation of heterochrony in dogs using 3D geometric morphometric analysis of skull shape |journal=Evolution & Development |year=2011 |volume=13 |issue=2 |pages=204–213 |s2cid=20893501}}

File:Axolotl ganz.jpg, 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 the frog Lithobates clamitans. Full neoteny is seen in Ambystoma mexicanum and some populations of Ambystoma tigrinum, which remain in larval form throughout their lives.{{cite journal |last=Swingle |first=W. |year=1922 |title=Experiments on the metamorphosis of neotenous amphibians |url=https://zenodo.org/record/1426890|journal=Journal of Experimental Zoology |volume=36 |issue=4 |pages=397–421 |doi=10.1002/jez.1400360402 |bibcode=1922JEZ....36..397S }}{{cite web |url=http://amphibiaweb.org/species/3850 |title=Ambystoma tigrinum |publisher=Amphibia Web}} Lithobates clamitans is partially neotenous; it delays maturation during the winter as fewer resources are available; it can find resources more easily in its 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 juvenile plumage into adulthood, losing it when they are fully mature.{{cite journal |last=Foster |first=M. |year=1987 |title=Delayed maturation, neoteny, and social system differences in two manakins of genus Chiroxyphia |url=https://zenodo.org/record/1235115|journal=Evolution |volume=41 |issue=3|pages=547–558 |doi=10.2307/2409256|pmid=28563802 |jstor=2409256 }}

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.{{cite journal |last1=Barbosa |first1=P. |display-authors=etal |year=1989 |title=Life-history traits of forest-inhabiting flightless Lepidoptera |journal=American Midland Naturalist |volume=122 |issue=2|pages=262–274 |jstor=2425912 |doi=10.2307/2425912}} 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. 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.

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.{{cite journal |last=Snyder |first=R. |year=1956 |title=Comparative Features of the Life Histories of Ambystoma gracile (Baird) from Populations at Low and High Altitudes |journal=Copeia |volume=1956 |issue=1|pages=41–50 |jstor=1439242 |doi=10.2307/1439242}} 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. 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.

Many species of salamander, and amphibians in general, exhibit environmental neoteny. Axolotl and olm are perennibranchiate 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.

Bonobos share many physical characteristics with humans, including neotenous skulls.{{cite journal |last1=Shea |first1=B. T. |year=1983 |title=Paedomorphosis and Neoteny in the Pygmy Chimpanzee |journal=Science |volume=222 |issue=4623 |pages=521–522 |jstor=1691380 |doi=10.1126/science.6623093 |pmid=6623093 |bibcode=1983Sci...222..521S }} 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.

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.{{cite journal |last1=Harrison |first1=R. |year=1980 |title=Dispersal polymorphisms in insects |journal=Annual Review of Ecology and Systematics |volume=11 |issue=1 |pages=95–118 |jstor=2096904 |doi=10.1146/annurev.es.11.110180.000523|bibcode=1980AnRES..11...95H }} Some cricket species shed their wings in adulthood;{{cite journal |last1=Harrison |first1=R. |year=1980 |title=Dispersal Polymorphisms in Insects |journal=Annual Review of Ecology and Systematics |volume=11 |issue=1 |pages=95–118 |jstor=2096904 |doi=10.1146/annurev.es.11.110180.000523|bibcode=1980AnRES..11...95H }} in the genus Ozopemon, males (thought to be the first example of neoteny in beetles) are significantly smaller than females due to inbreeding.{{cite journal |last1=Jordal |first1=B. H. |last2=Beaver |first2=R. A. |last3=Normark |first3=B. B. |last4=Farrell |first4=B. D. |year=2002 |title=Extraordinary sex ratios and the evolution of male neoteny in sib-mating Ozopemon beetles |journal=Biological Journal of the Linnean Society |volume=75 |issue=3|pages=353–360 |doi=10.1046/j.1095-8312.2002.00025.x |doi-access=free }} In the termite Kalotermes flavicollis, neoteny is seen in molting females.{{cite journal |last1=Soltani-Mazouni |first1=N. |last2=Bordereau |first2=C. |year=1987 |title=Changes in the cuticle, ovaries and colleterial glands during the pseudergate and neotenic molt in Kalotermes flavicollis (FABR.) (Isoptera : Kalotermitidae) |journal=International Journal of Insect Morphology and Embryology |volume=16 |issue=3–4|pages=221–225 |doi=10.1016/0020-7322(87)90022-5 }}

In other species, such as the northwestern salamander (Ambystoma gracile), environmental conditions{{snd}}high altitude, in this case{{snd}}cause neoteny.{{cite journal |last1=Eagleson |first1=G. |last2=McKeown |first2=B. |year=1978 |title=Changes in thyroid activity of Ambystoma gracile (Baird) during different larval, transforming, and postmetamorphic phases |journal=Canadian Journal of Zoology |volume=56 |issue=6|pages=1377–1381 |doi= 10.1139/z78-190|bibcode=1978CaJZ...56.1377E }} Neoteny is also found in a few species of the crustacean family Ischnomesidae, which live in deep ocean water.{{cite journal |last1=Brokeland |first1=W. |last2=Brandt |first2=A. |year=2004 |title=Two new species of Ischnomesidae (Crustacea: Isopoda) from the Southern Ocean displaying neoteny |journal=Deep-Sea Research Part II |volume=51 |issue=14–16|pages=1769–1785 |doi=10.1016/j.dsr2.2004.06.034 |bibcode=2004DSRII..51.1769B }}

Neoteny is an ancient, pervasive phenomenon. In urodeles, many extant taxa are neotenic,{{cite journal |last1=Wiens |first1=John J. |last2=Bonett |first2=Ronald M. |last3=Chippindale |first3=Paul T. |last4=Anderson |first4=Frank (Andy) |title=Ontogeny Discombobulates Phylogeny: Paedomorphosis and Higher-Level Salamander Relationships |journal=Systematic Biology |date=1 February 2005 |volume=54 |issue=1 |pages=91–110 |doi=10.1080/10635150590906037 |pmid=15805013 |url=https://doi.org/10.1080/10635150590906037}} and both morphological {{cite journal |last1=Evans |first1=Susan E. |last2=Milner |first2=Andrew R. |last3=Mussett |first3=Frances |title=The earliest known Salamanders (Amphibia, Caudata):A record from the Middle Jurassic of England |journal=Geobios |date=1 January 1988 |volume=21 |issue=5 |pages=539–552 |doi=10.1016/S0016-6995(88)80069-X |bibcode=1988Geobi..21..539E |url=https://doi.org/10.1016/S0016-6995(88)80069-X |issn=0016-6995|url-access=subscription }} and histological data suggest that the Middle Jurassic taxon Marmorerpeton was neotenic.{{cite journal |last1=de Buffrénil |first1=Vivian |last2=Canoville |first2=Aurore |last3=Evans |first3=Susan E. |last4=Laurin |first4=Michel |title=Histological study of karaurids, the oldest known (stem) urodeles |journal=Historical Biology |date=2 January 2015 |volume=27 |issue=1 |pages=109–114 |doi=10.1080/08912963.2013.869800 |bibcode=2015HBio...27..109D |url=http://dx.doi.org/10.1080/08912963.2013.869800|url-access=subscription }}

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.{{Citation |last1=Avidor-Reiss |first1=Tomer |last2=Turner |first2=Katerina |title=The Evolution of Centriole Structure: Heterochrony, Neoteny, and Hypermorphosis |date=2019 |url=https://doi.org/10.1007/978-3-030-23173-6_1 |work=The Golgi Apparatus and Centriole: Functions, Interactions and Role in Disease |pages=3–15 |editor-last=Kloc |editor-first=Malgorzata |access-date=12 October 2023 |series=Results and Problems in Cell Differentiation |place=Cham |publisher=Springer International |doi=10.1007/978-3-030-23173-6_1 |isbn=978-3-030-23173-6 |pmc=7576685 |pmid=31435789 |volume=67 }}

• Ageing
• Cuteness
• Kawaii
• Larviform female
• Moe (slang)
• Neotenic complex syndrome
• Neotenin

{{Reflist|30em}}

• Bergstorm, Carl T. & Dugatkin, Lee Alan (2012). Evolution, W.W. Norton {{ISBN|039391349X}}

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Category:Developmental biology

Category:Evolutionary biology

Category:Taxonomy (biology)