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Neoteny
View on WikipediaNeoteny (/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 in modern humans is more significant than in other primates.[6] In progenesis or paedogenesis, sexual development is accelerated.[7]
Both neoteny and progenesis result in paedomorphism[8] (as having the form typical of children) or paedomorphosis[9] (changing towards forms typical of children), a type of heterochrony.[10] 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.[11][12][13]
History and etymology
[edit]
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.[14][15]
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".[16] For the opposite of "neotenic", different authorities use either "gerontomorphic"[17][18] or "peramorphic".[19] 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)".[15]
In 1926, Louis Bolk described neoteny as the major process in humanization.[20][15] In his 1977 book Ontogeny and Phylogeny,[21] 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.[15]
In humans
[edit]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.[22] J. B. S. Haldane states 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."[23] 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.[24]
In domestic animals
[edit]Neoteny is seen in domesticated animals such as dogs and mice.[25] 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.[25] 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.[26][27][28]

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."[29] 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.[30] 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.[29]
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.[31] By 2011, the findings by the same researcher were simply "Dogs are not paedomorphic wolves."[32]
In other animals
[edit]
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.[33][34] 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.[35]
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.[36] 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.[36] 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.[37]
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.[38] 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.[38] 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.[36]
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.[33]
Bonobos share many physical characteristics with humans, including neotenous skulls.[39] 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.[39]
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.[37] Some cricket species shed their wings in adulthood;[40] in the genus Ozopemon, males (thought to be the first example of neoteny in beetles) are significantly smaller than females due to inbreeding.[41] In the termite Kalotermes flavicollis, neoteny is seen in molting females.[42]
In other species, such as the northwestern salamander (Ambystoma gracile), environmental conditions – high altitude, in this case – cause neoteny.[43] Neoteny is also found in a few species of the crustacean family Ischnomesidae, which live in deep ocean water.[44]
Neoteny is an ancient, pervasive phenomenon. In urodeles, many extant taxa are neotenic,[45] and both morphological [46] and histological data suggest that the Middle Jurassic taxon Marmorerpeton was neotenic.[47]
Subcellular neoteny
[edit]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.[48]
See also
[edit]References
[edit]- ^ "neoteny". Dictionary.com Unabridged (Online). n.d. Retrieved 21 April 2019.
- ^ "neoteny". The American Heritage Dictionary of the English Language (5th ed.). HarperCollins. Retrieved 21 April 2019.
- ^ "neoteny". Lexico US English Dictionary. Oxford University Press. Archived from the original on 22 March 2020.
- ^ "neoteny". Merriam-Webster.com Dictionary. Merriam-Webster. Retrieved 21 April 2019.
- ^ a b Montagu, A. (1989). Growing Young. Bergin & Garvey: CT.
- ^ Choi, Charles Q. (1 July 2009). "Being More Infantile May Have Led to Bigger Brains". Scientific American.
- ^ Volkenstein, M. V. 1994. Physical Approaches to Biological Evolution. Springer-Verlag: Berlin, [1].
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- ^ Ridley, Mark (1985). Evolution. Blackwell.
- ^ Whiteman, H.H. (1994). "Evolution of facultative paedomorphosis". Quarterly Review of Biology. 69 (2): 205–221. doi:10.1086/418540. S2CID 83500486.
- ^ Schell, S. C. Handbook of Trematodes of North America North of Mexico, 1985, pg. 22
- ^ Ginetsinskaya, T.A. Trematodes, Their Life Cycles, Biology and Evolution. Leningrad, USSR: Nauka 1968. Translated in 1988, [2].
- ^ Kollmann, J. (1885). "Das Ueberwintern von europäischen Frosch- und Tritonlarven und die Umwandlung des mexikanischen Axolotl" [The overwintering of European frog- and triton larvae and the transformation of the Mexican axolotl]. Verhandlungen der Naturforschenden Gesellschaft in Basel (Proceedings of the Natural Science Society of Basel) (in German). 7: 387–398. 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.)
- ^ a b c d Bogin, Barry (1999). Patterns of Human Growth. Cambridge University Press. pp. 157–169. ISBN 978-0-521-56438-0.
- ^ Neoteny, The Free Dictionary. 2011. Accessed April 30, 2011.
- ^ 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.
- ^ Hall, B.K., Hallgrímsson, B. Monroe, W.S. (2008). Strickberger's evolution: the integration of genes, organisms and populations. Jones and Bartlett Publishers: Canada.
- ^ Bolk, Louis (1926). Das Problem der Menschwerdung : Vortrag gehalten am 15. April 1926 auf der XXV. Versammlung der anatomischen Gesellschaft zu Freiburg [The Problem of Humanization: Lecture held on 15 April 1926 at the 25th Congress of the Anatomical Society at Freiberg] (in German). Jena, Germany: Gustav Fischer.
- ^ Gould, Stephen Jay (1977). Ontogeny and Phylogeny. Cambridge, Massachusetts: Belknap (Harvard University Press). ISBN 978-0-674-63940-9.
- ^ Shea, Brian T. (1989). "Heterochrony in human evolution: The case for neoteny reconsidered". American Journal of Physical Anthropology. 32 (S10): 69–101. doi:10.1002/ajpa.1330320505.
- ^ Thiessen, D.D. (1997). Bittersweet destiny: the stormy evolution of human behavior. Transaction Publishers, N.J.
- ^ Jones, D.; et al. (1995). "Sexual selection, physical attractiveness, and facial neoteny: Cross-cultural evidence and implications [and comments and reply]". Current Anthropology. 36 (5): 723–748. doi:10.1086/204427. S2CID 52840802.
- ^ a b Price, E. (1999). "Behavioral development in animals undergoing domestication". Applied Animal Behaviour Science. 65 (3): 245–271. doi:10.1016/S0168-1591(99)00087-8.
- ^ Vonk, Jennifer; Shackelford, Todd (1 April 2022). "Neoteny". Encyclopedia of Animal Cognition and Behavior. Springer. pp. 4590–4592. ISBN 978-3-319-55064-0.
- ^ Bertone, J. (2006). Equine geriatric medicine and surgery. Saunders, MI.
- ^ Trut, L. N. (1999). "Early canid domestication: the farm-fox experiment". American Scientist. 87 (2): 160–169. Bibcode:1999AmSci..87.....T. doi:10.1511/1999.2.160.
- ^ a b McGreevy, P.D. & Nicholas, F.W. (1999). Some Practical Solutions to Welfare Problems in Dog Breeding. In Animal Welfare. 8: 329–341.
- ^ 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
- ^ 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. link
- ^ Drake, Abby Grace (2011). "Dispelling dog dogma: An investigation of heterochrony in dogs using 3D geometric morphometric analysis of skull shape". Evolution & Development. 13 (2): 204–213. doi:10.1111/j.1525-142X.2011.00470.x. PMID 21410876. S2CID 20893501.
- ^ a b Swingle, W. (1922). "Experiments on the metamorphosis of neotenous amphibians". Journal of Experimental Zoology. 36 (4): 397–421. Bibcode:1922JEZ....36..397S. doi:10.1002/jez.1400360402.
- ^ "Ambystoma tigrinum". Amphibia Web.
- ^ Foster, M. (1987). "Delayed maturation, neoteny, and social system differences in two manakins of genus Chiroxyphia". Evolution. 41 (3): 547–558. doi:10.2307/2409256. JSTOR 2409256. PMID 28563802.
- ^ a b c Barbosa, P.; et al. (1989). "Life-history traits of forest-inhabiting flightless Lepidoptera". American Midland Naturalist. 122 (2): 262–274. doi:10.2307/2425912. JSTOR 2425912.
- ^ a b Harrison, R. (1980). "Dispersal polymorphisms in insects". Annual Review of Ecology and Systematics. 11 (1): 95–118. Bibcode:1980AnRES..11...95H. doi:10.1146/annurev.es.11.110180.000523. JSTOR 2096904.
- ^ a b Snyder, R. (1956). "Comparative Features of the Life Histories of Ambystoma gracile (Baird) from Populations at Low and High Altitudes". Copeia. 1956 (1): 41–50. doi:10.2307/1439242. JSTOR 1439242.
- ^ a b Shea, B. T. (1983). "Paedomorphosis and Neoteny in the Pygmy Chimpanzee". Science. 222 (4623): 521–522. Bibcode:1983Sci...222..521S. doi:10.1126/science.6623093. JSTOR 1691380. PMID 6623093.
- ^ Harrison, R. (1980). "Dispersal Polymorphisms in Insects". Annual Review of Ecology and Systematics. 11 (1): 95–118. Bibcode:1980AnRES..11...95H. doi:10.1146/annurev.es.11.110180.000523. JSTOR 2096904.
- ^ Jordal, B. H.; Beaver, R. A.; Normark, B. B.; Farrell, B. D. (2002). "Extraordinary sex ratios and the evolution of male neoteny in sib-mating Ozopemon beetles". Biological Journal of the Linnean Society. 75 (3): 353–360. doi:10.1046/j.1095-8312.2002.00025.x.
- ^ Soltani-Mazouni, N.; Bordereau, C. (1987). "Changes in the cuticle, ovaries and colleterial glands during the pseudergate and neotenic molt in Kalotermes flavicollis (FABR.) (Isoptera : Kalotermitidae)". International Journal of Insect Morphology and Embryology. 16 (3–4): 221–225. doi:10.1016/0020-7322(87)90022-5.
- ^ Eagleson, G.; McKeown, B. (1978). "Changes in thyroid activity of Ambystoma gracile (Baird) during different larval, transforming, and postmetamorphic phases". Canadian Journal of Zoology. 56 (6): 1377–1381. Bibcode:1978CaJZ...56.1377E. doi:10.1139/z78-190.
- ^ Brokeland, W.; Brandt, A. (2004). "Two new species of Ischnomesidae (Crustacea: Isopoda) from the Southern Ocean displaying neoteny". Deep-Sea Research Part II. 51 (14–16): 1769–1785. Bibcode:2004DSRII..51.1769B. doi:10.1016/j.dsr2.2004.06.034.
- ^ Wiens, John J.; Bonett, Ronald M.; Chippindale, Paul T.; Anderson, Frank (Andy) (1 February 2005). "Ontogeny Discombobulates Phylogeny: Paedomorphosis and Higher-Level Salamander Relationships". Systematic Biology. 54 (1): 91–110. doi:10.1080/10635150590906037. PMID 15805013.
- ^ Evans, Susan E.; Milner, Andrew R.; Mussett, Frances (1 January 1988). "The earliest known Salamanders (Amphibia, Caudata):A record from the Middle Jurassic of England". Geobios. 21 (5): 539–552. Bibcode:1988Geobi..21..539E. doi:10.1016/S0016-6995(88)80069-X. ISSN 0016-6995.
- ^ de Buffrénil, Vivian; Canoville, Aurore; Evans, Susan E.; Laurin, Michel (2 January 2015). "Histological study of karaurids, the oldest known (stem) urodeles". Historical Biology. 27 (1): 109–114. Bibcode:2015HBio...27..109D. doi:10.1080/08912963.2013.869800.
- ^ Avidor-Reiss, Tomer; Turner, Katerina (2019), Kloc, Malgorzata (ed.), "The Evolution of Centriole Structure: Heterochrony, Neoteny, and Hypermorphosis", The Golgi Apparatus and Centriole: Functions, Interactions and Role in Disease, Results and Problems in Cell Differentiation, vol. 67, Cham: Springer International, pp. 3–15, doi:10.1007/978-3-030-23173-6_1, ISBN 978-3-030-23173-6, PMC 7576685, PMID 31435789, retrieved 12 October 2023
Further reading
[edit]- Bergstorm, Carl T. & Dugatkin, Lee Alan (2012). Evolution, W.W. Norton ISBN 039391349X
Neoteny
View on GrokipediaDefinition and Conceptual Foundations
Precise Biological Definition
Neoteny constitutes a distinct category of heterochrony, defined as an evolutionary shift involving a reduction in the rate of somatic development relative to the ancestral condition, while reproductive maturation proceeds at a comparable or unaltered pace. Heterochrony itself encompasses any genetically controlled alteration in the timing, rate, or duration of developmental events compared to an ancestor, often manifesting as changes in growth trajectories that yield morphological novelty.[7] In neoteny, this deceleration specifically targets non-reproductive somatic traits, such as skeletal or organ maturation, leading to the retention of juvenile or larval features—e.g., proportions, pigmentation, or appendages—within sexually mature adults.[7][5] This process differs from progenesis, the other primary mechanism producing paedomorphosis (the broader phenotypic outcome of juvenilized adulthood), wherein overall development is truncated by an acceleration of sexual maturation, affecting the entire organism rather than selectively slowing somatic growth. Neoteny's selective impact on growth rates enables modular evolutionary changes, where specific body regions or traits retain ancestral juvenile forms without compromising reproductive timing, as evidenced in quantitative analyses of developmental trajectories in vertebrates.[7] Genetic underpinnings, such as regulatory shifts in hormone-sensitive pathways, underpin this rate disparity, though neoteny is observable phenotypically without necessitating molecular dissection.[5] The term originates from classical studies distinguishing neoteny's rate-based mechanism from timing offsets like paedogenesis, emphasizing causal realism in developmental evolution: somatic retardation preserves adaptive juvenile morphologies under selection pressures favoring early reproduction.[7] Empirical validation comes from comparative ontogenies, where neotenic lineages exhibit extended larval-like phases, quantifiable via allometric scaling of trait sizes against age or size proxies.[7] This definition holds across taxa, from amphibians displaying facultative neoteny under environmental cues to domesticated mammals, underscoring its role in adaptive paedomorphosis without implying uniform juvenilization across all traits.[5]Distinctions from Related Phenomena
![Diagram illustrating heterochrony processes including neoteny][float-right] Heterochrony refers to evolutionary changes in the timing, rate, or duration of developmental events, serving as a broad framework encompassing neoteny as one specific mechanism.[7] Neoteny specifically involves a retardation in the rate of somatic development relative to sexual maturation, allowing juvenile morphological traits—such as large heads, short limbs, and reduced sexual dimorphism—to persist into adulthood without altering the timing of reproductive maturity.[8] This contrasts with progenesis, another heterochronic process, where somatic development is truncated due to accelerated sexual maturation, resulting in paedomorphic adults that achieve reproductive capability earlier but with incomplete ontogeny.[9] Paedomorphosis describes the phenotypic outcome of retaining ancestral juvenile traits in descendant adults, achievable through either neoteny or progenesis, but it is not synonymous with neoteny itself.[10] In neoteny, the extended somatic juvenility arises from a slower developmental tempo, as observed in species like the axolotl (Ambystoma mexicanum), where metamorphosis is delayed indefinitely while gonadal development proceeds.[8] Progenesis, by comparison, shortens the overall lifespan of developmental phases, often linked to ecological pressures favoring rapid reproduction, such as in certain salamanders where paedomorphic forms mature sexually in larval habitats without somatic advancement.[11] Neoteny must also be differentiated from peramorphosis, the opposing heterochronic category involving extended or accelerated development beyond ancestral adult forms, such as through hypermorphosis (prolonged growth) or acceleration (faster somatic rates).[7] While neoteny and related paedomorphic processes reduce morphological complexity by conserving early ontogenetic stages, peramorphic shifts, like those in some mammalian cranial evolution, extend development to produce novel adult traits.[10] These distinctions highlight neoteny's role in evolutionary paedomorphosis via rate hypomorphosis, distinct from truncation-based mechanisms, with empirical support from comparative studies in amphibians showing divergent life-history outcomes: neoteny often sustains longer lifespans, whereas progenesis correlates with abbreviated generation times.[8][9]Evolutionary Significance
Neoteny represents a key heterochronic mechanism in evolution, characterized by the prolongation of somatic development relative to reproductive maturation, resulting in paedomorphic adult forms that retain larval or juvenile traits. This process facilitates evolutionary novelty by decoupling morphological maturation from gonadal development, allowing organisms to achieve sexual maturity without completing ontogenetic trajectories that might be maladaptive in specific environments.[12] In salamanders of the genus Ambystoma, for instance, neoteny has evolved independently multiple times, enabling facultative shifts between metamorphic and paedomorphic life histories that enhance survival in stable aquatic habitats where terrestrial metamorphosis imposes high energetic costs.[3] The adaptive value of neoteny lies in its promotion of developmental plasticity, which can buffer against environmental variability and open novel ecological niches. By retaining traits such as gills or reduced ossification, neotenic forms avoid the risks of metamorphosis, such as desiccation or predation during transition, thereby increasing lifetime reproductive success in predator-poor or resource-limited settings.[3] Empirical studies on Ambystoma species demonstrate that neotenic populations often exhibit higher densities in permanent water bodies, with genetic underpinnings involving thyroid hormone signaling pathways that regulate metamorphosis suppression.[3] This plasticity not only sustains populations in marginal habitats but also serves as a precursor for speciation, as isolated neotenic lineages accumulate distinct adaptations over generations.[12] Evolutionarily, neoteny contrasts with peramorphic processes by favoring peramorphosis through retardation rather than acceleration, potentially accelerating diversification rates in lineages prone to heterochrony. In insects like Lycidae beetles, multiple ancient origins of neoteny underscore its recurrent utility in generating morphological disparity via simple shifts in developmental timing, independent of major genomic reorganizations.[12] While neoteny's prevalence across amphibians, insects, and mammals suggests broad selective advantages—such as enhanced learning capacity or reduced somatic investment—its fixation depends on ecological contexts where juvenile traits confer fitness benefits without compromising fertility.[11] Causal analyses indicate that neoteny thrives in environments with low extrinsic mortality and abundant juvenile resources, aligning with life-history theory predictions for delayed maturation strategies.[3]Historical Development
Etymology and Early Observations
The term "neoteny" was coined in 1884 by German anatomist Julius Kollmann, derived from the Greek neos ("young") and teinein ("to stretch" or "hold"), denoting the prolongation of juvenile traits into sexual maturity.[13][14] Kollmann introduced the concept while examining the axolotl (Ambystoma mexicanum), a salamander that attains reproductive capability in its larval form, complete with external gills and aquatic adaptations, bypassing typical metamorphosis to a terrestrial adult stage.[3] This observation highlighted neoteny as a distinct heterochronic process, where somatic development lags behind gonadal maturation.[3] Earlier recognition of similar phenomena predated the term, with naturalists documenting persistent larval traits in amphibians. In 1875, August Weismann interpreted such cases as atavistic reversions to ancestral gill-breathing aquatic forms, suggesting neoteny reflected a return to primitive conditions rather than a novel evolutionary adaptation.[15] Observations of neotenic salamanders, including Ambystoma species, revealed facultative neoteny, where individuals could metamorphose under certain environmental cues like iodine availability, but often remained paedomorphic in stable aquatic habitats.[3] These findings, primarily from Mexican and North American populations, underscored neoteny's prevalence in urodeles, influencing subsequent evolutionary theories on developmental plasticity.[3]Key Theoretical Contributions
Julius Kollmann coined the term "neoteny" in 1885 to denote the retention of larval or juvenile traits into sexual maturity, particularly as observed in salamanders like the axolotl, where aquatic gill-bearing forms reproduce without undergoing metamorphosis to terrestrial adulthood.[3] This concept built on earlier observations of paedogenesis but emphasized the evolutionary potential of delayed somatic maturation relative to reproductive timing.[3] In 1926, Dutch anatomist Louis Bolk advanced neoteny into a broader explanatory framework known as the fetalization or retardation theory, positing that human evolution involved a systematic slowing of developmental rates compared to other primates, resulting in the persistence of fetal characteristics—such as a globular skull, reduced facial prognathism, and brain expansion—into adulthood.[16] Bolk argued this retardation affected multiple organ systems, linking neoteny not only to morphology but to extended dependency and plasticity, though later critiques noted inconsistencies in comparing human and ape ontogenies across disparate traits.[16] Julian Huxley refined the theoretical scope of neoteny in 1927 by integrating it into the study of heterochrony—shifts in developmental timing—as a mechanism of evolutionary change, distinguishing neoteny specifically as the retardation of somatic (body) development while gonadal maturation proceeds on schedule, in contrast to progenesis, where somatic growth is truncated to achieve early reproduction with juvenile form.[17] Huxley's framework highlighted how such dissociations could generate paedomorphic adults, providing a quantitative basis for modeling heterochronic evolution beyond qualitative descriptions.[17] Gavin de Beer, in his 1930 book Embryos and Ancestors, synthesized neoteny within a critique of strict recapitulation theory, proposing that evolutionary novelties often arise through paedomorphosis via neoteny, where ancestral juvenile stages become fixed in descendant adults, enabling mosaic evolution in which different body parts develop at independent rates.[18] De Beer's analysis of vertebrate embryos demonstrated how neoteny facilitates adaptive radiation by preserving plasticity and reducing specialization, influencing subsequent evo-devo research on developmental constraints.[18]Underlying Mechanisms
Genetic and Molecular Bases
Neoteny arises from genetic alterations that delay or truncate the expression of genes responsible for adult morphological and physiological traits, often involving regulatory elements that control developmental timing. These changes can manifest as mutations in transcription factors, hormone signaling pathways, or cis-regulatory sequences, leading to prolonged juvenile gene expression profiles. In vertebrates, such mechanisms frequently implicate heterochronic shifts in developmental programs, where juvenile states are stabilized through inhibitory feedback loops or reduced sensitivity to maturation signals.[19][4] In amphibians, particularly the axolotl (Ambystoma mexicanum), neoteny is genetically controlled by a single recessive allele that prevents metamorphosis, resulting in retention of larval gills and aquatic morphology into adulthood. This allele, dominant in related species like the tiger salamander for inducing metamorphosis, disrupts thyroid hormone-mediated signaling, which normally triggers tissue remodeling. Laboratory strains exhibit neoteny due to artificial selection, with genetic analyses revealing high inbreeding and fixation of neotenic traits independent of wild populations.[20][21] In mammals, including humans, molecular evidence points to neoteny in neural development through gene duplications and regulatory evolution. Human-specific paralogs SRGAP2B and SRGAP2C, arising from segmental duplications approximately 2-3 million years ago, inhibit the ancestral SRGAP2A protein, thereby reducing its suppression of SYNGAP1 and prolonging dendritic spine maturation. Proteomic studies across species confirm delayed synaptic protein maturation in humans compared to chimpanzees, correlating with extended periods of synaptic plasticity. Transcriptional analyses further show human prefrontal cortex retaining fetal-like gene expression patterns into postnatal stages, unlike faster-maturing non-human primates.[22][23][4] Broader molecular bases include heterochronic shifts in microRNAs or splicing factors that fine-tune gene expression timing, as seen in comparative genomic studies of paedomorphic traits. For instance, balancing of splicing regulators is required for human synaptic neoteny, where imbalances mimic neurodevelopmental disorders. These mechanisms underscore neoteny's role in evolutionary divergence, though direct causation remains inferred from comparative data rather than experimental recapitulation in most cases.[24][25]Developmental and Hormonal Processes
Neoteny arises from heterochronic developmental shifts that retard somatic maturation relative to gonadal development, resulting in the retention of larval or juvenile morphological, physiological, and behavioral traits in reproductively mature individuals.[20] This retardation can be facultative, allowing metamorphosis under certain environmental cues, or obligate, as seen in species like the axolotl (Ambystoma mexicanum).[3] In amphibians, hormonal control primarily involves the hypothalamus-pituitary-thyroid (HPT) axis, where insufficient thyroid hormone (TH) signaling maintains neoteny by blocking metamorphosis. Neotenic forms exhibit low endogenous TH titers throughout larval stages, failing to surge as in metamorphic conspecifics, due to defects in hypothalamic corticotropin-releasing hormone (CRH) stimulation of thyrotropin (TSH) or downstream responsiveness.[26] Exogenous administration of TH, such as thyroxine (T4) or triiodothyronine (T3), induces metamorphosis in facultatively neotenic species like the axolotl, confirming functional TH receptors (TRs) but highlighting upstream regulatory failures.[27] Quantitative trait loci (QTL), including met1, modulate TH sensitivity, implicating genes like nradd (involved in neural apoptosis) and pou1f1 (pituitary transcription factor) in neotenic differentiation.[26] Obligate neoteny in urodeles such as Necturus maculosus involves tissue-specific insensitivity to TH despite a functional HPT system, preventing somatic remodeling like gill resorption or limb elongation.[28] Metamorphosis induction requires not only TH but also TSH or hypothalamic stimulation, underscoring neoteny as a deviation in endocrine integration rather than TH absence alone.[28] In domesticated mammals, neotenic traits emerge from selection pressures favoring tameness, which retard overall developmental rates and correlate with adrenal hypofunction and lowered stress hormones like cortisol.[29] Experimental fox domestication demonstrates hormonal shifts, including reduced ACTH, contributing to paedomorphic features such as floppy ears and shortened muzzles, though direct TH mediation remains less established than in amphibians.[30] These processes suggest neoteny involves conserved heterochronic mechanisms modulated by endocrine timing, with amphibians providing the clearest hormonal models.[31]Manifestations in Animals
Neoteny in Amphibians and Aquatic Species
Neoteny in amphibians primarily occurs among salamanders (order Urodela), where it manifests as paedomorphosis—the retention of larval traits such as external gills, aquatic locomotion, and a flattened tail into sexual maturity, bypassing metamorphic transformation to terrestrial forms. This phenomenon is documented in nine of the ten salamander families, often as an alternative life history strategy to metamorphosis.[32] Paedomorphic salamanders exhibit delayed somatic development relative to reproductive maturation, enabling reproduction in stable aquatic habitats while avoiding the physiological costs and mortality risks associated with terrestrial transition.[33] The axolotl (Ambystoma mexicanum), endemic to Lake Xochimilco and surrounding waters in central Mexico, represents a prominent example of neoteny, with wild populations predominantly paedomorphic and retaining juvenile features like feathery external gills for branchial respiration, lidless eyes, and permeable skin throughout adulthood.[34] These salamanders reach sexual maturity at lengths of 15–45 cm without endogenous thyroid hormone surges sufficient for metamorphosis, though exogenous thyroxine administration can induce it experimentally, confirming the underlying hormonal mechanism.[35] Neoteny in axolotls is linked to permanent aquatic environments with low predation pressure from large fish, conferring advantages like enhanced regenerative capacity, as evidenced by their ability to regrow limbs, spinal cord, and even parts of the heart and brain.[36] However, habitat degradation has critically endangered wild axolotls, with populations declining over 90% since the 1980s due to pollution and introduced species.[21] Facultative neoteny, where individuals can either metamorphose or remain paedomorphic based on environmental cues, is observed in species like the tiger salamander (Ambystoma tigrinum and related Ambystoma complex), with neotenic forms predominant in high-elevation, fishless lakes where cooler temperatures and resource stability favor larval retention.[3] Evolutionary analyses indicate neoteny evolved multiple times in Ambystoma, often correlating with colonization of isolated aquatic niches at elevations above 2,000 meters, where metamorphosis yields lower fitness due to desiccation risks and energy demands.[3] Similarly, the mudpuppy (Necturus maculosus) exhibits obligate paedomorphosis, remaining fully aquatic with gilled larvae-like morphology across its range in eastern North American rivers and lakes.[32] In other amphibian groups, neoteny is rarer; for instance, paedomorphosis in the Ezo salamander (Hynobius retardatus) of Japan involves facultative retention of larval traits in specific pond habitats, documented since observations in the 20th century.[37] Among strictly aquatic species beyond amphibians, true neoteny is less common, though heterochronic shifts akin to paedomorphosis occur in some fish lineages, such as delayed maturation in certain cave-adapted populations, but these lack the pronounced larval-adult dissociation seen in salamanders.[38] Overall, amphibian neoteny underscores adaptive plasticity in life cycles, with genetic underpinnings involving thyroid pathway genes like thrb and environmental modulation via iodine availability.[34]Neoteny in Domesticated Mammals
Domesticated mammals frequently display neoteny as part of the domestication syndrome, where artificial selection for traits like tameness results in the retention of juvenile morphological, behavioral, and physiological features into adulthood. Common neotenic manifestations include shortened muzzles, floppy ears, reduced brain size, depigmented patches, smaller teeth, and prolonged juvenile playfulness or nonseasonal estrus cycles. These changes arise not from direct selection for morphology but as pleiotropic effects linked to reduced neural crest cell activity during development, which influences craniofacial structure, pigmentation, and adrenal function.[29] The Russian silver fox (Vulpes vulpes) experiment, initiated by Dmitry Belyaev in 1959, provides experimental evidence: foxes selected solely for reduced fear and aggression toward humans over 10-15 generations exhibited neotenic traits such as floppy ears, curled tails, piebald coats, and widened skulls resembling juveniles, with 18-35% of offspring classified as "elite tame" by the fourth generation. This rapid emergence—within 4-6 generations for some traits—demonstrated neoteny as a byproduct of tameness selection, with genetic analyses identifying QTLs associated with both behavior and morphology.[39][40] In dogs (Canis familiaris), neoteny is evident when compared to ancestral wolves (Canis lupus). Zoologist Desmond Morris observed in his 1969 book The Human Zoo that domesticated dogs are "rather juvenile versions of their wild counterparts," highlighting the retention of juvenile traits such as prolonged dependency and playfulness into adulthood, in contrast to adult wolves. Adult dogs retain pup-like proportions, including larger crania relative to body size, shorter snouts, pronounced forehead stops, and softer facial features that enhance expressiveness, diverging from wolves' more robust adult morphology. Brain size reduction averages 10-15% in dogs versus wolves, correlating with juvenile-like docility. Similar patterns occur in domesticated cats (Felis catus), with smaller brains (about 25% reduction from wildcats) and juvenile facial rounding; guinea pigs (Cavia porcellus), showing prolonged infancy and reduced aggression; and pigs (Sus domesticus), featuring floppy ears and curly tails absent in wild boars. Rats (Rattus norvegicus) selected for tameness likewise display neotenic white spotting and behavioral juvenility.[29][41]- Morphological traits: Floppy ears (dogs, foxes, pigs), shortened muzzles (dogs, cats, foxes), depigmentation (foxes, dogs, rats).
- Behavioral traits: Extended playfulness and reduced aggression (foxes, dogs, rats).
- Physiological traits: Smaller adrenal glands and nonseasonal reproduction (multiple species).[29]
Neoteny in Wild Mammals and Other Taxa
In wild mammals, neoteny manifests prominently in the naked mole-rat (Heterocephalus glaber), a eusocial subterranean rodent native to arid regions of East Africa, where adults retain juvenile-like developmental patterns contributing to exceptional longevity exceeding 30 years despite a small body size of approximately 35-40 grams.[43] This species exhibits delayed somatic maturation, with physiological processes such as hematopoiesis mirroring embryonic or juvenile states in other rodents; for instance, erythropoiesis occurs in both bone marrow and spleen, an extramedullary site predominant in fetal mammals but atypical in adults.[44] Neotenic features extend to neural development, where brain maturation proceeds slowly, preserving plasticity and correlating with resistance to age-related pathologies like neurodegeneration.[45] These traits are hypothesized to underpin the naked mole-rat's cancer resistance, hypoxia tolerance, and negligible senescence, adaptations suited to its colony-based, low-oxygen burrow environment where reproduction is restricted to few breeders, reducing selection pressure for rapid aging.[46] Unlike domesticated mammals, where neoteny often arises from artificial selection for tameness, the naked mole-rat's neoteny appears evolutionarily conserved, linked to eusociality in highly cooperative species, as evidenced by comparative genomic analyses showing retained juvenile gene expression profiles into adulthood.[43] [47] Examples of neoteny in wild non-mammalian taxa beyond amphibians are scarce and typically facultative rather than obligate. In certain reptilian lineages, such as some blind cave-dwelling species, paedomorphic traits like retained larval pigmentation or reduced ossification occur sporadically under environmental stress, but these do not constitute full neoteny as defined by retarded somatic development with reproductive maturity.[48] Avian taxa show no well-documented obligate neoteny in wild populations, though some flightless island endemics display paedomorphosis in skeletal proportions, potentially as a byproduct of insular dwarfism rather than heterochronic shifts. Overall, neoteny in wild taxa outside social mammals and amphibians remains underexplored, with most empirical data emphasizing its role in niche adaptations like extended juvenility for ecological persistence.[3]Neoteny in Human Biology and Evolution
Anatomical and Morphological Evidence
Humans retain several cranial features characteristic of juvenile great apes, including a globular skull shape, thin cranial vault bones, and a reduced supraorbital torus or brow ridge.[43] These traits contrast with the more prognathic, robust skulls of adult chimpanzees and gorillas, where facial projection and supraorbital development increase markedly during ontogeny.[49] Morphometric analyses of fossil hominins show a progressive reduction in facial prognathism and midfacial retraction in Homo sapiens compared to earlier species like Homo erectus, aligning adult human profiles more closely with juvenile australopithecine or ape forms.[50] The human face exhibits paedomorphic proportions, such as a broadened, flattened midface with vertically shortened dimensions, large relative eye orbits, and reduced nasal and maxillary prominence—features that persist into adulthood unlike in other primates, where somatic maturation elongates and projects the face.[51] Dental evidence supports this, with smaller, less robust dentition and delayed eruption patterns resembling those of immature primates, though absolute tooth size reduction may reflect dietary shifts rather than pure heterochronic retardation.[52] Skeletal morphology further indicates neotenic retention, including a gracile postcranial skeleton with reduced muscle attachments, elongated limbs relative to trunk length (particularly longer legs than arms), and an absence of structures like the baculum present in adult male primates.[43] Comparative ontogenetic studies reveal that while human shape changes mimic paedomorphosis through retarded growth trajectories in facial and cranial elements, braincase expansion involves peramorphic extension, achieving larger absolute volumes than ancestral juveniles.[49][51] This dissociation—retardation in somatic traits alongside extension in neural ones—underlies claims of neoteny in human evolution, though critics argue it represents mosaic heterochrony rather than uniform juvenilization.[5]Behavioral and Cognitive Correlates
Neotenic morphological features in adult humans, such as relatively large eyes, small noses, and rounded faces, serve as cues that psychologically trigger protective instincts, affection, and attraction, distinct from the biological process of neoteny itself but rooted in evolutionary adaptations for caregiving. This phenomenon, known as the baby schema or Kindchenschema, was conceptualized by Konrad Lorenz as a set of infantile traits that elicit nurturing responses, promoting social bonding and similar to reactions observed toward juveniles in other species like kittens or puppies.[53] Human neoteny manifests behaviorally through the retention of juvenile traits such as prolonged playfulness and exploratory tendencies into adulthood, distinguishing humans from other primates where such behaviors diminish sharply post-infancy.[54][55] Adult humans engage in play at rates exceeding those of adult great apes, facilitating social bonding, conflict resolution, and the rehearsal of complex skills, with rough-and-tumble play observed across cultures as a mechanism for physical and emotional regulation.[56][54] This extension correlates with neoteny's role in promoting affiliative and cooperative social structures, as evidenced by comparative primate studies showing reduced adult play in species with shorter developmental windows.[57] Cognitively, neoteny supports extended periods of neural plasticity and delayed maturation, enabling cumulative learning and abstract reasoning beyond what is typical in other mammals.[58] Synaptic density in human prefrontal cortex peaks between ages 8 and 10—60% higher than adult levels in visual areas and 50% in frontal regions—far later than in macaques, where peaks occur by 2–4 months, allowing prolonged synaptogenesis and refinement into the third decade.[59] This delay fosters enhanced working memory, planning, and social cognition, with transcriptional profiles revealing that 38% of analyzed brain genes in humans exhibit neotenic expression patterns, particularly in prefrontal cortex, compared to chimpanzees.[4] Empirical comparative data underscore these correlates: species with longer juvenile phases, including humans, show superior performance in problem-solving and social learning tasks, with human rearing periods extending cognitive development through safe, iterative exploration akin to juvenile states in other taxa.[57] Such traits likely contributed to human evolutionary success by amplifying adaptability, though they remain subject to environmental modulation, as seen in studies of adversity delaying prefrontal-amygdala connectivity maturation beyond typical timelines.[58][59]Empirical Measurements and Comparative Data
Empirical assessments of neoteny in humans often quantify craniofacial morphology through geometric morphometrics and ontogenetic scaling. Comparative studies of skull development reveal that adult human crania retain proportions resembling juvenile great apes, with reduced facial prognathism and a relatively larger neurocranium. For instance, in chimpanzees (Pan troglodytes), postnatal facial growth extends the muzzle forward, resulting in adult facial length comprising approximately 50-60% of total cranial length, whereas in humans, this ratio stabilizes earlier at around 30-40%, preserving a more globular, infantile vault shape.[60][61] Landmark-based analyses confirm that human adults occupy a distinct morphospace, offset from adult apes toward their juvenile forms along allometric trajectories, with shape differences emerging early in ontogeny due to divergent growth rates in the viscerocranium.[62] Brain size metrics further support neotenic patterns, as humans exhibit prolonged postnatal encephalization. At birth, human brain volume averages 350-400 cm³, representing less than 25% of adult size (≈1,350 cm³), the lowest relative value among primates; chimpanzees achieve ≈30-40% at birth (adult ≈400 cm³).[63][64] This delay correlates with extended cortical folding and gyrification, where human prefrontal regions mature over 20-25 years, compared to 10-15 years in apes.[65] Molecular data provide transcriptional evidence of neoteny, particularly in prefrontal cortex gene expression. Analysis of 7,958 genes across humans, chimpanzees, and rhesus macaques identified 299 heterochronic shifts among 3,075 comparable transcripts, with 38% (114 genes) indicating human neoteny—wherein adult human profiles resemble juvenile chimpanzee states more closely than adult chimpanzee ones (FDR=10%, P=2×10⁻⁴).[65][4] These neotenic genes, affecting ≈4% of the cortical transcriptome, enrich in gray matter regions and peak in divergence around age 10, underscoring slower maturation in humans relative to apes.[65]| Feature | Human Adult | Chimpanzee Adult | Juvenile Ape Similarity to Human Adult |
|---|---|---|---|
| Relative Brain Size at Birth (% adult) | <25% | ≈30-40% | N/A |
| Facial Length/Cranial Length Ratio | 30-40% | 50-60% | High (retains infantile proportions) |
| Heterochronic Genes (Neoteny %) | 38% of shifts | Baseline (0% reference) | Adult human ≈ juvenile chimp |
| </section_text> |
