647:
541:, a close relative to the axolotl, displays both paedomorphosis and peramorphosis. The larva can develop in either direction. Population density, food, and the amount of water may have an effect on the expression of heterochrony. A study conducted on the mole salamander in 1987 found it evident that a higher percentage of individuals became paedomorphic when there was a low larval population density in a constant water level as opposed to a high larval population density in drying water. This had an implication that led to hypotheses that selective pressures imposed by the environment, such as predation and loss of resources, were instrumental to the cause of these trends. These ideas were reinforced by other studies, such as peramorphosis in the
464:). Axolotls reach full sexual maturity while retaining their fins and gills (in other words, still in the juvenile form of their ancestors). They will remain in aquatic environments in this truncated developmental form, rather than moving onto land as other sexually mature salamander species. This is thought to be a form of hypomorphosis (earlier ending of development) that is both hormonally and genetically driven. The entire metamorphosis that would allow the salamander to transition into the adult form is essentially blocked by both of these drivers.
676:, brain and head growth starts at about the same developmental stage and grow at a rate similar to that of humans, but growth stops soon after birth, whereas humans continue brain and head growth several years after birth. This particular type of heterochrony, hypermorphosis, involves a delay in the offset of a developmental process, or what is the same, the presence of an early developmental process in later stages of development. Humans have some 30 different
103:
482:) would have a short face, large eyes, a thin palate, narrow jugal bone, tall and thin postorbitals, restricted adductors, and a short and bulbous braincase. As an organism such as this aged, they would change greatly in their cranial morphology to develop a robust skull with larger, overlapping bones. Birds, however, retain this juvenile morphology. Evidence from molecular experiments suggests both
449:, the retention of juvenile traits into the adult form as a result of retardation of somatic development, or of progenesis, the acceleration of developmental processes such that the juvenile form becomes a sexually mature adult. This means that in progenesis, germ cell growth is accelerated relative to normal or in neoteny; while somatic cell growth is normal in progenesis, but retarded in neoteny.
304:
504:
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160:, another concept he originated) or time (heterochrony), as exceptions to his rule. He thus intended the term to mean a change in the timing of the embryonic development of one organ with respect to the rest of the same animal, whereas it is now used, following the work of the British evolutionary embryologist
490:
have facilitated paedomorphosis in birds. These signalling pathways are known to play roles in facial patterning in other vertebrate species. This retention of the juvenile ancestral state has driven other changes in the anatomy that result in a light, highly kinetic (moveable) skull composed of many
401:
close species, for example a group of different bird species whose legs differ in their average length. These comparisons are complex because there are no universal ontogenetic timemarkers. The method of event pairing attempts to overcome this by comparing the relative timing of two events at a time.
452:
Neoteny retards the development of the organism into an adult, and has been described as "eternal childhood". In this form of heterochrony, the developmental stage of childhood is itself extended, and certain developmental processes that normally take place only during childhood (such as accelerated
295:
There are three major mechanisms of heterochrony, each of which can change in either of two directions, giving six types of perturbations, which can be combined in various ways. These ultimately result in extended, shifted, or truncated development of a particular process, such as the action of a
155:
at one stage. This, in his view, necessarily compressed the earlier developmental stages, representing the ancestors, into a shorter time, meaning accelerated development. The ideal for
Haeckel would be when the development of every part of an organism was thus accelerated, but he recognised that
529:
size, and longer lifespan. Their relatives that inhabit continental environments are much smaller. Insular rodents have evolved these features to accommodate the abundance of food and resources they have on their islands. These factors are part of a complex phenomenon termed Island syndrome or
300:, relative to the ancestral condition or to other conspecifics, depending on whether inter- or intraspecific heterochrony is the focus. Identifying which of the six perturbations is occurring is critical in identifying the actual underlying mechanism driving peramorphosis or paedomorphosis.
406:
changes. It is cumbersome to use because the number of event pair characters increases with the square of the number of events compared. Event pairing can however be automated, for instance with the PARSIMOV script. A recent method, continuous analysis, rests on a simple standardization of
549:, or the lifespan of the species in question. When a species has a relatively short lifespan, natural selection favors evolution of paedomorphosis (e.g. Axolotl: 7–10 years). Conversely, in long lifespans natural selection favors evolution of peramorphosis (e.g. Irish Elk: 20–22 years).
2114:
Bhullar, Bhart-Anjan S.; Morris, Zachary S.; Sefton, Elizabeth M.; et al. (2015-07-01). "A molecular mechanism for the origin of a key evolutionary innovation, the bird beak and palate, revealed by an integrative approach to major transitions in vertebrate history".
383:
gain their long necks by a different heterochrony, extending the development of their cervical vertebrae; they retain the usual mammalian number of these vertebrae, seven. This number appears to be constrained by the use of neck somites to form the mammalian
475:
from which they evolved. Extant birds have large eyes and brains relative to the rest of the skull; a condition seen in adult birds that represents (broadly speaking) the juvenile stage of a dinosaur. A juvenile avian ancestor (as typified by
379:(body segments), which relies on an oscillator. The oscillator clock runs some four times faster in snake than in mouse embryos, initially creating very thin somites. These expand to adopt a typical vertebrate shape, elongating the body.
1089:
Reilly, Stephen M. (February 1987). "Ontogeny of the hyobranchial apparatus in the salamanders
Ambystoma talpoideum (Ambystomatidae) and Notophthalmus viridescens (Salamandridae): The ecological morphology of two neotenic strategies".
688:
The term "heterokairy" was proposed in 2003 by John Spicer and Warren
Burggren to distinguish plasticity in timing of the onset of developmental events at the level of an individual (heterokairy) or population (heterochrony).
388:
muscle; the result is that the embryonic neck is divided into three modules, the middle one (C3 to C5) serving the diaphragm. The assumption is that disrupting this would kill the embryo rather than giving it more vertebrae.
216:, showing that evolution could occur by heterochrony, such as in paedomorphosis, the retention of juvenile features in the adult. De Beer argued that this enabled rapid evolutionary change, too brief to be recorded in the
453:
brain growth in humans), is also extended throughout this period. Neoteny has been implicated as a developmental cause for a number of behavior changes, as a result of increased brain plasticity and extended childhood.
2657:
Penin, Xavier; Berge, Christine; Baylac, Michel (May 2002). "Ontogenetic study of the skull in modern humans and the common chimpanzees: neotenic hypothesis reconsidered with a tridimensional
Procrustes analysis".
632:
Garstang's theory is certainly an attractive one, and it was much in favour for many years ... Unfortunately, recent DNA evidence has swung the pendulum in favour of Darwin's original theory. If the
187:
from such a larva. The proposal implied (if it were correct) a shared phylogeny of tunicates and vertebrates, and that heterochrony was a principal mechanism of evolutionary change.
371:. Where a typical vertebrate like a mouse has only around 60 vertebrae, snakes have between around 150 to 400, giving them extremely long spinal columns and enabling their sinuous
232:
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
646:
636:
constitute a recent re-enactment of an ancient
Garstang scenario, they should find closer kinship with some modern sea squirts than with others. Alas, this is not so.
2621:
Mitteroecker, P.; Gunz, P.; Bernhard, M.; Schaefer, K.; Bookstein, F. L. (June 2004). "Comparison of cranial ontogenetic trajectories among great apes and humans".
1845:
2284:
Raia, Pasquale; Guarino, Fabio M.; Turano, Mimmo; Gianluca Polese; Daniela Rippa; Francesco
Carotenuto; Daria M. Monti; Manuela Cardi; Domenico Fulgione (2010).
495:
overlapping bones. This is believed to have facilitated the evolution of cranial kinesis in birds which has played a critical role in their ecological success.
3310:
1511:
Germain, D.; Laurin, M. (2009). "Evolution of ossification sequences in salamanders and urodele origins assessed through event-pairing and new methods".
518:. From the fossil record, its antlers spanned up to 12 feet (3.7 m) wide, which is about a third larger than the antlers of its close relative, the
628:, and is still held by some modern biologists. However, according to others, closer genetic investigation rather seems to support Darwin's old opinion:
2471:
Richardson, Michael K.; Oelschlager, Helmut H. A. (2002). "Time, pattern, and heterochrony: a study of hyperphalangy in the dolphin embryo flipper".
86:
These changes all affect the start, end, rate or time span of a particular developmental process. The concept of heterochrony was introduced by
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Another example of peramorphosis is seen in insular (island) rodents. Their characteristics include gigantism, wider cheek and teeth, reduced
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in comparison to the chimpanzee, retaining larger heads, smaller jaws and noses, and shorter limbs, features found in juvenile chimpanzees.
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1937:
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2002:
Bhullar, Bhart-Anjan S.; Marugán-Lobón, Jesús; Racimo, Fernando; et al. (2012-05-27). "Birds have paedomorphic dinosaur skulls".
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2075:"How to Make a Bird Skull: Major Transitions in the Evolution of the Avian Cranium, Paedomorphosis, and the Beak as a Surrogate Hand"
1963:"How to Make a Bird Skull: Major Transitions in the Evolution of the Avian Cranium, Paedomorphosis, and the Beak as a Surrogate Hand"
79:
innovation. Heterochrony can be divided into intraspecific heterochrony, variation within a species, and interspecific heterochrony,
67:
compared to its ancestors or other organisms. This leads to changes in the size, shape, characteristics and even presence of certain
2791:
2834:
2829:
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Spicer, J. I.; Burggren, W. W. (2003). "Development of physiological regulatory systems: altering the timing of crucial events".
408:
136:
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Zelditch, Miriam L.; Fink, William L. (2015). "Heterochrony and heterotopy: stability and innovation in the evolution of form".
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both evolved from animals whose adult form was similar to (frog) tadpoles and the 'tadpole larvae' of tunicates. According to
117:'s view that development itself varies, such as by changing the timing of different processes, to cause a branching phylogeny.
3300:
254:
means changes in the rate or timing of development within a species. For example, some individuals of the salamander species
113:
an animal's phylogeny, and introduced heterochrony as an exception for individual organs. Modern biology agrees instead with
3225:
2390:"Neoteny and progenesis as two heterochronic processes involved in paedomorphosis in Triturus alpestris (Amphibia: Caudata)"
3076:
964:
699:
1774:
2514:
Emlen, Douglas J.; Nijhout, H. Frederik (2000). "The
Development and Evolution of Exaggerated Morphologies in Insects".
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means differences in the rate or timing of a descendant species relative to its ancestor. This can result in either
3235:
3101:
2933:
2447:
2343:
Semlitsch, Raymond D. (1987). "Paedomorphosis in
Ambystoma talpoideum: effects of density, food, and pond drying".
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Heterochrony is responsible for a wide variety of effects such as the lengthening of the fingers by adding extra
359:: The rate of a process can accelerate, extending its development, or decelerate (as in neoteny), truncating it.
319:(left). With the number constrained, the development of the vertebrae is extended, allowing them to grow longer.
483:
2567:
1206:
Evolution and
Development: report of the Dahlem Workshop on Evolution and Development, Berlin 1981, May 10–15
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delay the metamorphosis of the skull. Reilly and colleagues argue we can define these variant individuals as
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of development. It seeks to explain each step in the creation of an adult organism from an undifferentiated
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1058:"An integrative approach to heterochrony: the distinction between interspecific and intraspecific phenomena"
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in 1930, to mean a change with respect to the development of the same organ in the animal's ancestors.
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pointed out, Haeckel's term is now used in a sense contrary to his coinage; Haeckel had assumed that
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2528:
1726:"Aerobic Glycolysis in the Human Brain is Associated with Development and Neotenous Gene Expression"
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acquired their long necks through heterochrony, extending the development period of the seven neck
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1318:"Evo-Devo and an Expanding Evolutionary Synthesis: A Genetic Theory of Morphological Evolution"
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Peramorphosis is delayed maturation with extended periods of growth. An example is the extinct
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522:. The Irish elk had larger antlers due to extended development during their period of growth.
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skeleton with antlers spanning 2.7 metres (8.9 ft) and a mass of 40 kg (88 lb)
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Moen, Ron A.; John Pastor; Yosef Cohen (1999). "Antler growth and extinction of Irish elk".
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2019:
1974:
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Smith, Charles Kay (1990). "A model for understanding the evolution of mammalian behavior".
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Fink, William L. (July 1982). "The conceptual relationship between ontogeny and phylogeny".
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999:"Homology and heterochrony: the evolutionary embryologist Gavin Rylands de Beer (1899–1972)"
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2015:
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Bhullar, Bhart-Anjan S.; Hanson, Michael; Fabbri, Matteo; et al. (September 2016).
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variation, i.e. variation of a descendant species with respect to an ancestral species.
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75:, a change in spatial positioning of some process in the embryo, which can also create
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Comparative
Biochemistry and Physiology Part A: Molecular & Integrative Physiology
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210:. De Beer to some extent anticipated such late 20th-century science in his 1930 book
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Bhullar, Bhart-Anjan S.; Hanson, Michael; Fabbri, Matteo; et al. (2016-09-01).
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Goyal, Manu S.; Hawrylycz, Michael; Miller, Jeremy A.; et al. (January 2014).
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570:
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102:
80:
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471:. The skulls and beaks of living, adult birds retain the anatomy of the juvenile
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998:
812:
593:
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Jeffery, J. E.; Bininda-Emonds, O.R.P.; Coates, M.I.; Richardson, M.K. (2005).
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is any genetically controlled difference in the timing, rate, or duration of a
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after another. Further, it relates such patterns of control of development to
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157:
72:
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2202:
Bout, Ron G.; Zweers, Gart A (2001). "The role of cranial kinesis in birds".
1914:
1831:
1274:"Heterochrony and Allometry: Lessons from the Water Strider Genus Limnoporus"
17:
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2160:"A zone of frontonasal ectoderm regulates patterning and growth in the face"
1947:
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40:
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244:. These may be combined, e.g. to shift some aspect of development earlier.
228:
147:(ontogeny) of "higher" animals recapitulated their ancestral development (
3127:
3096:
2091:
2074:
1979:
1962:
1667:"Extraordinary neoteny of synaptic spines in the human prefrontal cortex"
1665:
Petanjek, Zdravko; Judaš, Miloš; Šimić, Goran; et al. (2011-08-09).
613:
609:
585:
542:
380:
172:
151:), as when mammal embryos have structures on the neck that resemble fish
64:
2443:
How the Snake Lost its Legs. Curious Tales from the Frontier of Evo-Devo
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How the Snake Lost its Legs. Curious Tales from the Frontier of Evo-Devo
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How the Snake Lost its Legs. Curious Tales from the Frontier of Evo-Devo
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932:
How the Snake Lost its Legs. Curious Tales from the Frontier of Evo-Devo
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Heterochrony can be divided into intraspecific and interspecific types.
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2671:
2374:
1773:
Coppinger, R.; Glendinning, J.; Torop, E.; et al. (January 1987).
1606:
Somel, Mehmet; Franz, Henriette; Yan, Zheng; et al. (2009-04-07).
1448:
758:
Hall, B. K. (2003). "Evo-Devo: evolutionary developmental mechanisms".
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650:
581:
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457:
446:
434:
425:
375:. Snake embryos achieve this by accelerating their system for creating
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36:
32:
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2159:
2128:
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Several heterochronies have been described in humans, relative to the
430:
307:
Despite greatly differing neck lengths, giraffes (right) have no more
2839:
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retain gills and fins as adults; these are juvenile features in most
376:
199:
44:
2366:
1056:
Reilly, Stephen M.; Wiley, E.O.; Meinhardt, Daniel J. (1997-01-01).
272:(reaching the same ancestral shape, but via a different mechanism).
268:(with extended development relative to the ancestral condition), or
127:
The concept of heterochrony was introduced by the German zoologist
1575:
The eternal child : how evolution has made children of us all
673:
645:
575:
519:
502:
429:
368:
316:
302:
264:(with truncated development relative to the ancestral condition),
227:
101:
31:
2241:. Sunderland, Massachusetts: Sinauer Associates. pp. 64–66.
2055:
The skull, vol 2: patterns of structural and systematic diversity
3137:
152:
2773:
1272:
Klingenberg, Christian Peter; Spence, John R. (December 1993).
407:
ontogenetic time or sequences, on squared change parsimony and
292:(reaching the same ancestral state via a different mechanism).
1775:"Degree of Behavioral Neoteny Differentiates Canid Polymorphs"
807:. Topics in Geobiology. Vol. 7. Springer. pp. 1–13.
1814:
Heterochrony in evolution : a multidisciplinary approach
803:(1988). "The Uses of Heterochrony". In McKinney, M.L. (ed.).
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220:, and in effect explaining why apparent gaps were likely.
2158:
Hu, Diane; Marcucio, Ralph S.; Helms, Jill A. (May 2003).
156:
some organs could develop with displacements in position (
1423:"Analyzing developmental sequences using sequences units"
608:
suggested the neotenous origin of the vertebrates from a
467:
Paedomorphosis by progenesis may play a critical role in
363:
A dramatic illustration of how acceleration can change a
402:
This method detects event heterochronies, as opposed to
238:; postdisplacement, hypomorphosis, and deceleration all
2394:
Proceedings of the Royal Society B: Biological Sciences
1472:"A new technique for identifying sequence heterochrony"
969:. Belknap Press of Harvard University Press. pp.
1173:
Keller,Evelyn Fox; Lloyd, Elisabeth A., eds. (1992).
47:
to add length to the bones, not by adding more bones.
1899:. Gilbert, Lawrence Irwin. Appleton-Century-Crofts.
456:
Progenesis (or paedogenesis) can be observed in the
327:: A developmental process can either begin earlier,
131:
in 1875, where he used it to define deviations from
3258:
3187:
3115:
3069:
3062:
3026:
2978:
2942:
2875:
2812:
2286:"The blue lizard spandrel and the island syndrome"
1137:
2057:. University of Chicago Press. pp. 391–437.
1897:Metamorphosis a problem in developmental biology
1857:
1855:
1671:Proceedings of the National Academy of Sciences
1612:Proceedings of the National Academy of Sciences
630:
891:
889:
887:
760:International Journal of Developmental Biology
612:larva, in opposition to Darwin's opinion that
183:, and suggested that the vertebrates arose by
2785:
1051:
1049:
1047:
1045:
8:
1932:. University of Chicago Press. p. 324.
1608:"Transcriptional neoteny in the human brain"
898:"Heterochrony: the Evolution of Development"
753:
751:
749:
718:
716:
397:Heterochrony can be identified by comparing
288:(extending past the ancestral ontogeny), or
2279:
2277:
3066:
2792:
2778:
2770:
2068:
2066:
2064:
1844:: CS1 maint: location missing publisher (
785:Horder, Tim (April 2006). "Heterochrony".
235:extend development (peramorphosis, in red)
2660:American Journal of Physical Anthropology
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2413:
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1978:
1879:
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1700:
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1438:
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1062:Biological Journal of the Linnean Society
913:
345:, extending its development, or earlier,
1864:"Genie Control of Axolotl Metamorphosis"
2197:
2195:
712:
331:, extending its development, or later,
3282:Index of evolutionary biology articles
1837:
838:
828:
624:, Garstang's opinion was also held by
90:in 1875 and given its modern sense by
1179:. Harvard University Press. pp.
732:. Palgrave Macmillan. pp. 280–.
596:derived from such a larva by neoteny.
282:(truncating the ancestral ontogeny),
241:truncate it (paedomorphosis, in blue)
175:larvae shared structures such as the
7:
789:. Chichester: John Wiley & Sons.
569:, and the polymorphism seen between
445:Paedomorphosis can be the result of
109:supposed that embryonic development
71:and features. It is contrasted with
2079:Integrative and Comparative Biology
1967:Integrative and Comparative Biology
1812:McKinney, Michael L. (2013-11-21).
1144:. Cambridge, Mass.: Belknap Press.
3311:Evolutionary developmental biology
3092:Evolutionary developmental biology
1799:10.1111/j.1439-0310.1987.tb00645.x
1291:10.1111/j.1558-5646.1993.tb01273.x
1075:10.1111/j.1095-8312.1997.tb01487.x
409:phylogenetic independent contrasts
341:: A process can either end later,
192:evolutionary developmental biology
167:In 1928, the English embryologist
123:Evolutionary developmental biology
53:evolutionary developmental biology
25:
1816:. McKinney, Michael L. New York.
902:Evolution: Education and Outreach
3049:Evolution of sexual reproduction
2485:10.1046/j.1525-142X.2002.02032.x
1525:10.1111/j.1525-142X.2009.00318.x
1176:Keywords in Evolutionary Biology
137:ontogeny recapitulates phylogeny
1573:Clive., Bromhall (2004-01-01).
1007:Journal of Experimental Zoology
2820:Genotype–phenotype distinction
1208:. Springer. pp. 313–332.
1:
3306:Evolutionary biology concepts
3077:Regulation of gene expression
2538:10.1146/annurev.ento.45.1.661
2264:Evolutionary Ecology Research
2216:10.1016/s1095-6433(01)00470-6
1928:Wainwright, Peter C. (1994).
1862:Tompkins, Robert (May 1978).
896:McNamara, Kenneth J. (2012).
787:Encyclopedia of Life Sciences
3247:Endless Forms Most Beautiful
3027:Evolution of genetic systems
2835:Gene–environment correlation
2830:Gene–environment interaction
2635:10.1016/j.jhevol.2004.03.006
2388:Denoel, M.; P. Joly (2000).
580:A 1901 comparison of a frog
486:8 (FGF8) and members of the
311:, just 7, than their fellow
3226:Christiane Nüsslein-Volhard
2516:Annual Review of Entomology
1513:Evolution & Development
813:10.1007/978-1-4899-0795-0_1
202:in terms of the control of
3327:
3102:Hedgehog signaling pathway
2979:Developmental architecture
2448:Cambridge University Press
1742:10.1016/j.cmet.2013.11.020
1398:Cambridge University Press
1366:Cambridge University Press
1335:10.1016/j.cell.2008.06.030
937:Cambridge University Press
661:
600:
545:. Another reason could be
423:
276:Interspecific heterochrony
252:Intraspecific heterochrony
120:
3279:
2929:Transgressive segregation
2568:Weidenfeld & Nicolson
2473:Evolution and Development
2237:Futuyma, Douglas (2013).
1489:10.1080/10635150590923227
1251:10.1017/s0094837300006977
915:10.1007/s12052-012-0420-3
870:10.1017/S0094837300016195
805:Heterochrony in Evolution
553:Across the animal kingdom
2600:. Orion. p. Pt324.
2311:10.1186/1471-2148-10-289
2290:BMC Evolutionary Biology
1421:Velhagen, W. A. (1997).
565:to form their flippers,
484:fibroblast growth factor
185:paedomorphosis (neoteny)
3107:Notch signaling pathway
3082:Gene regulatory network
2965:Dual inheritance theory
2717:10.1078/0944-2006-00103
1895:Etkin, William (1968).
1692:10.1073/pnas.1105108108
1633:10.1073/pnas.0900544106
1440:10.1093/sysbio/46.1.204
1204:Alberch, Pedro (1982).
1104:10.1002/jmor.1051910210
929:Held, Lewis I. (2014).
469:avian cranial evolution
194:(evo-devo) studies the
3155:cis-regulatory element
3063:Control of development
2943:Non-genetic influences
2909:evolutionary landscape
2406:10.1098/rspb.2000.1168
1140:Ontogeny and phylogeny
966:Ontogeny and Phylogeny
700:Ontogeny and Phylogeny
654:
644:
597:
543:Puerto Rican tree frog
511:
488:WNT signalling pathway
442:
320:
245:
204:expression of one gene
118:
48:
3301:Developmental biology
3266:Nature versus nurture
3170:Cell surface receptor
3087:Evo-devo gene toolkit
2986:Developmental biology
2924:Polygenic inheritance
2850:Quantitative genetics
2750:Developmental biology
1092:Journal of Morphology
662:Further information:
649:
601:Garstang's hypothesis
584:(a vertebrate) and a
579:
506:
433:
306:
231:
213:Embryos and Ancestors
145:embryonic development
133:recapitulation theory
121:Further information:
105:
61:developmental process
35:
3175:Transcription factor
2890:Genetic assimilation
2877:Genetic architecture
2760:Evolutionary biology
2053:Zusi, R. L. (1993).
1881:10.1093/icb/18.2.313
1400:. pp. 126–127.
653:in human development
257:Ambystoma talpoideum
3271:Morphogenetic field
3188:Influential figures
2597:The Ancestor's Tale
2564:The Ancestor's tale
2400:(1451): 1481–1485.
2359:1987Ecol...68..994S
2302:2010BMCEE..10..289R
2024:10.1038/nature11146
2016:2012Natur.487..223B
1791:1987Ethol..75...89C
1683:2011PNAS..10813281P
1677:(32): 13281–13286.
1624:2009PNAS..106.5743S
1243:1982Pbio....8..254F
1028:10.1002/jez.b.21100
1020:2006JEZB..306..317B
462:Ambystoma mexicanum
135:, which held that "
115:Karl Ernst von Baer
27:Evolutionary change
2960:Genomic imprinting
2672:10.1002/ajpa.10044
2092:10.1093/icb/icw069
1980:10.1093/icb/icw069
1868:American Zoologist
1476:Systematic Biology
1427:Systematic Biology
1368:. pp. 81–84.
1134:Gould, Stephen Jay
961:Gould, Stephen Jay
729:Principles of Life
655:
598:
512:
473:theropod dinosaurs
443:
321:
309:cervical vertebrae
246:
196:molecular genetics
119:
49:
3288:
3287:
3221:Eric F. Wieschaus
3183:
3182:
3001:Pattern formation
2905:Fitness landscape
2577:978-0-7538-1996-8
2457:978-1-107-62139-8
2177:10.1242/dev.00397
2129:10.1111/evo.12684
2010:(7406): 223–226.
1618:(14): 5743–5748.
1556:Current Mammalogy
1407:978-1-107-62139-8
1375:978-1-107-62139-8
980:978-0-674-63940-9
946:978-1-107-62139-8
822:978-1-4899-0797-4
801:Gould, Stephen J.
739:978-1-4641-6298-5
664:Neoteny in humans
567:sexual dimorphism
333:post-displacement
141:Stephen Jay Gould
43:'s growth in the
16:(Redirected from
3318:
3231:William McGinnis
3200:Richard Lewontin
3195:C. H. Waddington
3067:
3044:Neutral networks
2794:
2787:
2780:
2771:
2737:
2736:
2698:
2692:
2691:
2654:
2648:
2646:
2618:
2612:
2611:
2592:Dawkins, Richard
2588:
2582:
2581:
2560:Dawkins, Richard
2556:
2550:
2549:
2531:
2511:
2505:
2504:
2468:
2462:
2461:
2434:
2428:
2427:
2417:
2385:
2379:
2378:
2340:
2334:
2333:
2323:
2313:
2281:
2272:
2271:
2259:
2253:
2252:
2234:
2228:
2227:
2199:
2190:
2189:
2179:
2170:(9): 1749–1758.
2155:
2149:
2148:
2123:(7): 1665–1677.
2111:
2105:
2104:
2094:
2070:
2059:
2058:
2050:
2044:
2043:
1999:
1993:
1992:
1982:
1958:
1952:
1951:
1925:
1919:
1918:
1892:
1886:
1885:
1883:
1859:
1850:
1849:
1843:
1835:
1809:
1803:
1802:
1770:
1764:
1763:
1753:
1721:
1715:
1714:
1704:
1694:
1662:
1656:
1655:
1645:
1635:
1603:
1597:
1596:
1570:
1564:
1563:
1551:
1545:
1544:
1508:
1502:
1501:
1491:
1467:
1461:
1460:
1442:
1418:
1412:
1411:
1386:
1380:
1379:
1354:
1348:
1347:
1337:
1314:Carroll, Sean B.
1310:
1304:
1303:
1293:
1284:(6): 1834–1853.
1269:
1263:
1262:
1226:
1220:
1219:
1201:
1195:
1194:
1170:
1164:
1163:
1143:
1130:
1124:
1123:
1086:
1080:
1079:
1077:
1053:
1040:
1039:
1003:
991:
985:
984:
957:
951:
950:
926:
920:
919:
917:
893:
882:
881:
853:
847:
846:
840:
836:
834:
826:
797:
791:
790:
782:
776:
775:
766:(7–8): 491–495.
755:
744:
743:
724:Hillis, David M.
720:
684:Related concepts
672:. In chimpanzee
642:
399:phylogenetically
353:, truncating it.
335:, truncating it.
329:pre-displacement
243:
237:
21:
3326:
3325:
3321:
3320:
3319:
3317:
3316:
3315:
3291:
3290:
3289:
3284:
3275:
3254:
3241:Sean B. Carroll
3179:
3111:
3058:
3022:
2974:
2955:Maternal effect
2938:
2871:
2808:
2798:
2746:
2741:
2740:
2700:
2699:
2695:
2656:
2655:
2651:
2647:
2620:
2619:
2615:
2608:
2590:
2589:
2585:
2578:
2558:
2557:
2553:
2529:10.1.1.323.5456
2513:
2512:
2508:
2470:
2469:
2465:
2458:
2450:. p. 152.
2436:
2435:
2431:
2387:
2386:
2382:
2367:10.2307/1938370
2353:(4): 992–1002.
2342:
2341:
2337:
2283:
2282:
2275:
2261:
2260:
2256:
2249:
2236:
2235:
2231:
2201:
2200:
2193:
2157:
2156:
2152:
2113:
2112:
2108:
2072:
2071:
2062:
2052:
2051:
2047:
2001:
2000:
1996:
1960:
1959:
1955:
1940:
1939:978-0-226869957
1927:
1926:
1922:
1907:
1894:
1893:
1889:
1861:
1860:
1853:
1836:
1824:
1811:
1810:
1806:
1772:
1771:
1767:
1730:Cell Metabolism
1723:
1722:
1718:
1664:
1663:
1659:
1605:
1604:
1600:
1585:
1584:978-0-091894429
1572:
1571:
1567:
1553:
1552:
1548:
1510:
1509:
1505:
1469:
1468:
1464:
1420:
1419:
1415:
1408:
1388:
1387:
1383:
1376:
1356:
1355:
1351:
1312:
1311:
1307:
1271:
1270:
1266:
1228:
1227:
1223:
1216:
1203:
1202:
1198:
1191:
1172:
1171:
1167:
1152:
1132:
1131:
1127:
1088:
1087:
1083:
1055:
1054:
1043:
1001:
993:
992:
988:
981:
959:
958:
954:
947:
928:
927:
923:
895:
894:
885:
855:
854:
850:
837:
827:
823:
799:
798:
794:
784:
783:
779:
757:
756:
747:
740:
722:
721:
714:
709:
695:
686:
666:
660:
643:
641:Richard Dawkins
640:
622:Richard Dawkins
606:Walter Garstang
603:
590:Walter Garstang
588:larva; in 1928
555:
547:generation time
539:mole salamander
501:
428:
422:
417:
395:
239:
233:
226:
169:Walter Garstang
125:
100:
28:
23:
22:
15:
12:
11:
5:
3324:
3322:
3314:
3313:
3308:
3303:
3293:
3292:
3286:
3285:
3280:
3277:
3276:
3274:
3273:
3268:
3262:
3260:
3256:
3255:
3253:
3252:
3251:
3250:
3238:
3233:
3228:
3223:
3218:
3217:
3216:
3205:François Jacob
3202:
3197:
3191:
3189:
3185:
3184:
3181:
3180:
3178:
3177:
3172:
3167:
3162:
3157:
3152:
3147:
3142:
3141:
3140:
3130:
3125:
3119:
3117:
3113:
3112:
3110:
3109:
3104:
3099:
3094:
3089:
3084:
3079:
3073:
3071:
3064:
3060:
3059:
3057:
3056:
3051:
3046:
3041:
3036:
3030:
3028:
3024:
3023:
3021:
3020:
3015:
3010:
3005:
3004:
3003:
2998:
2988:
2982:
2980:
2976:
2975:
2973:
2972:
2967:
2962:
2957:
2952:
2946:
2944:
2940:
2939:
2937:
2936:
2934:Sequence space
2931:
2926:
2921:
2916:
2911:
2902:
2897:
2892:
2887:
2881:
2879:
2873:
2872:
2870:
2869:
2864:
2863:
2862:
2852:
2847:
2842:
2837:
2832:
2827:
2822:
2816:
2814:
2810:
2809:
2799:
2797:
2796:
2789:
2782:
2774:
2768:
2767:
2762:
2757:
2752:
2745:
2742:
2739:
2738:
2693:
2649:
2613:
2607:978-0752873213
2606:
2583:
2576:
2551:
2522:(1): 661–708.
2506:
2479:(6): 435–444.
2463:
2456:
2438:Held, Lewis I.
2429:
2380:
2335:
2273:
2254:
2248:978-1605351155
2247:
2229:
2210:(1): 197–205.
2191:
2150:
2106:
2085:(3): 389–403.
2060:
2045:
1994:
1973:(3): 389–403.
1953:
1938:
1920:
1906:978-1461332466
1905:
1887:
1874:(2): 313–319.
1851:
1823:978-1489907950
1822:
1804:
1765:
1716:
1657:
1598:
1583:
1565:
1546:
1519:(2): 170–190.
1503:
1482:(2): 230–240.
1462:
1433:(1): 204–210.
1413:
1406:
1390:Held, Lewis I.
1381:
1374:
1358:Held, Lewis I.
1349:
1305:
1264:
1237:(3): 254–264.
1221:
1215:978-0387113319
1214:
1196:
1190:978-0674503120
1189:
1165:
1151:978-0674639416
1150:
1125:
1098:(2): 205–214.
1081:
1068:(1): 119–143.
1041:
1014:(4): 317–328.
986:
979:
952:
945:
939:. p. 67.
921:
908:(2): 203–218.
883:
864:(2): 241–254.
848:
821:
792:
777:
745:
738:
711:
710:
708:
705:
704:
703:
694:
691:
685:
682:
659:
656:
638:
602:
599:
592:proposed that
554:
551:
500:
497:
424:Main article:
421:
420:Paedomorphosis
418:
416:
413:
394:
391:
361:
360:
354:
343:hypermorphosis
336:
225:
222:
99:
96:
26:
24:
14:
13:
10:
9:
6:
4:
3:
2:
3323:
3312:
3309:
3307:
3304:
3302:
3299:
3298:
3296:
3283:
3278:
3272:
3269:
3267:
3264:
3263:
3261:
3257:
3249:
3248:
3244:
3243:
3242:
3239:
3237:
3234:
3232:
3229:
3227:
3224:
3222:
3219:
3215:
3212:
3211:
3210:
3209:Jacques Monod
3206:
3203:
3201:
3198:
3196:
3193:
3192:
3190:
3186:
3176:
3173:
3171:
3168:
3166:
3163:
3161:
3158:
3156:
3153:
3151:
3148:
3146:
3143:
3139:
3136:
3135:
3134:
3131:
3129:
3126:
3124:
3123:Homeotic gene
3121:
3120:
3118:
3114:
3108:
3105:
3103:
3100:
3098:
3095:
3093:
3090:
3088:
3085:
3083:
3080:
3078:
3075:
3074:
3072:
3068:
3065:
3061:
3055:
3052:
3050:
3047:
3045:
3042:
3040:
3037:
3035:
3032:
3031:
3029:
3025:
3019:
3016:
3014:
3011:
3009:
3006:
3002:
2999:
2997:
2994:
2993:
2992:
2991:Morphogenesis
2989:
2987:
2984:
2983:
2981:
2977:
2971:
2968:
2966:
2963:
2961:
2958:
2956:
2953:
2951:
2948:
2947:
2945:
2941:
2935:
2932:
2930:
2927:
2925:
2922:
2920:
2917:
2915:
2912:
2910:
2906:
2903:
2901:
2898:
2896:
2893:
2891:
2888:
2886:
2883:
2882:
2880:
2878:
2874:
2868:
2865:
2861:
2858:
2857:
2856:
2853:
2851:
2848:
2846:
2843:
2841:
2838:
2836:
2833:
2831:
2828:
2826:
2825:Reaction norm
2823:
2821:
2818:
2817:
2815:
2811:
2807:
2803:
2795:
2790:
2788:
2783:
2781:
2776:
2775:
2772:
2766:
2763:
2761:
2758:
2756:
2755:Embryogenesis
2753:
2751:
2748:
2747:
2743:
2734:
2730:
2726:
2722:
2718:
2714:
2710:
2706:
2705:
2697:
2694:
2689:
2685:
2681:
2677:
2673:
2669:
2665:
2661:
2653:
2650:
2644:
2640:
2636:
2632:
2629:(6): 679–97.
2628:
2624:
2617:
2614:
2609:
2603:
2599:
2598:
2593:
2587:
2584:
2579:
2573:
2569:
2565:
2561:
2555:
2552:
2547:
2543:
2539:
2535:
2530:
2525:
2521:
2517:
2510:
2507:
2502:
2498:
2494:
2490:
2486:
2482:
2478:
2474:
2467:
2464:
2459:
2453:
2449:
2445:
2444:
2439:
2433:
2430:
2425:
2421:
2416:
2411:
2407:
2403:
2399:
2395:
2391:
2384:
2381:
2376:
2372:
2368:
2364:
2360:
2356:
2352:
2348:
2347:
2339:
2336:
2331:
2327:
2322:
2317:
2312:
2307:
2303:
2299:
2295:
2291:
2287:
2280:
2278:
2274:
2270:(2): 235–249.
2269:
2265:
2258:
2255:
2250:
2244:
2240:
2233:
2230:
2225:
2221:
2217:
2213:
2209:
2205:
2198:
2196:
2192:
2187:
2183:
2178:
2173:
2169:
2165:
2161:
2154:
2151:
2146:
2142:
2138:
2134:
2130:
2126:
2122:
2118:
2110:
2107:
2102:
2098:
2093:
2088:
2084:
2080:
2076:
2069:
2067:
2065:
2061:
2056:
2049:
2046:
2041:
2037:
2033:
2029:
2025:
2021:
2017:
2013:
2009:
2005:
1998:
1995:
1990:
1986:
1981:
1976:
1972:
1968:
1964:
1957:
1954:
1949:
1945:
1941:
1935:
1931:
1924:
1921:
1916:
1912:
1908:
1902:
1898:
1891:
1888:
1882:
1877:
1873:
1869:
1865:
1858:
1856:
1852:
1847:
1841:
1833:
1829:
1825:
1819:
1815:
1808:
1805:
1800:
1796:
1792:
1788:
1785:(2): 89–108.
1784:
1780:
1776:
1769:
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623:
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571:insect castes
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532:Foster's rule
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218:fossil record
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162:Gavin de Beer
159:
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129:Ernst Haeckel
124:
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112:
111:recapitulated
108:
107:Ernst Haeckel
104:
97:
95:
93:
92:Gavin de Beer
89:
88:Ernst Haeckel
84:
82:
78:
77:morphological
74:
70:
66:
62:
58:
54:
46:
42:
38:
34:
30:
19:
18:Heterochronic
3245:
3138:eyeless gene
3034:Evolvability
3008:Segmentation
2885:Canalisation
2855:Heterochrony
2854:
2845:Heritability
2813:Key concepts
2711:(2): 91–99.
2708:
2702:
2696:
2666:(1): 50–62.
2663:
2659:
2652:
2626:
2623:J. Hum. Evol
2622:
2616:
2596:
2586:
2563:
2554:
2519:
2515:
2509:
2476:
2472:
2466:
2442:
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2397:
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2350:
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2338:
2293:
2289:
2267:
2263:
2257:
2238:
2232:
2207:
2203:
2167:
2163:
2153:
2120:
2116:
2109:
2082:
2078:
2054:
2048:
2007:
2003:
1997:
1970:
1966:
1956:
1929:
1923:
1896:
1890:
1871:
1867:
1813:
1807:
1782:
1778:
1768:
1736:(1): 49–57.
1733:
1729:
1719:
1674:
1670:
1660:
1615:
1611:
1601:
1574:
1568:
1559:
1555:
1549:
1516:
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1506:
1479:
1475:
1465:
1430:
1426:
1416:
1393:
1384:
1361:
1352:
1328:(1): 25–36.
1325:
1321:
1308:
1281:
1277:
1267:
1234:
1231:Paleobiology
1230:
1224:
1205:
1199:
1175:
1168:
1139:
1128:
1095:
1091:
1084:
1065:
1061:
1011:
1005:
989:
965:
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931:
924:
905:
901:
861:
858:Paleobiology
857:
851:
804:
795:
786:
780:
763:
759:
728:
726:(May 2011).
698:
687:
667:
631:
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477:
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451:
444:
396:
362:
356:
350:
346:
342:
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332:
328:
324:
298:toolkit gene
294:
290:isomorphosis
289:
283:
279:
275:
274:
269:
265:
261:
255:
251:
250:
247:
240:
234:
211:
189:
171:showed that
166:
126:
85:
81:phylogenetic
57:heterochrony
56:
50:
29:
3236:Mike Levine
3145:Distal-less
2970:Polyphenism
2950:Epigenetics
2802:development
2164:Development
839:|work=
618:vertebrates
594:vertebrates
479:Coelophysis
367:is seen in
181:vertebrates
179:with adult
3295:Categories
3214:Lac operon
3039:Robustness
3018:Modularity
3013:Metamerism
2919:Plasticity
2914:Pleiotropy
2867:Heterotopy
2296:(1): 289.
1562:: 335–374.
707:References
670:chimpanzee
634:larvaceans
491:small, non
439:amphibians
404:allometric
373:locomotion
351:progenesis
262:paedotypic
224:Mechanisms
158:heterotopy
73:heterotopy
3165:Morphogen
3150:Engrailed
3133:Pax genes
3054:Tinkering
2900:Epistasis
2895:Dominance
2806:phenotype
2765:Phylogeny
2524:CiteSeerX
2239:Evolution
2145:205124061
2117:Evolution
1915:682061358
1840:cite book
1832:883381554
1577:. Ebury.
1278:Evolution
841:ignored (
831:cite book
678:neotenies
658:In humans
614:tunicates
559:phalanges
516:Irish elk
508:Irish elk
393:Detection
386:diaphragm
365:body plan
313:giraffids
266:peratypic
208:phylogeny
177:notochord
149:phylogeny
94:in 1930.
41:vertebrae
3128:Hox gene
3116:Elements
3097:Homeobox
2744:See also
2733:13558790
2725:16351894
2688:15566858
2680:11953945
2643:15183670
2594:(2004).
2562:(2005).
2546:10761593
2501:15429067
2493:12492144
2440:(2014).
2424:10983835
2330:20854657
2224:11733177
2186:12642481
2137:25964090
2101:27371392
2032:22722850
1989:27371392
1948:29357502
1779:Ethology
1760:24411938
1711:21788513
1652:19307592
1593:59288040
1541:22629275
1533:19245549
1498:16012094
1457:11975352
1392:(2014).
1360:(2014).
1344:18614008
1316:(2008).
1300:28567993
1259:84119618
1136:(1977).
1120:49315190
1112:29921111
1036:16506229
997:(2006).
963:(1977).
878:89098289
772:14756324
693:See also
639:—
610:tunicate
586:tunicate
563:dolphins
435:Axolotls
381:Giraffes
270:isotypic
173:tunicate
65:organism
37:Giraffes
3259:Debates
3070:Systems
2996:Eyespot
2860:Neoteny
2704:Zoology
2415:1690691
2375:1938370
2355:Bibcode
2346:Ecology
2321:2949876
2298:Bibcode
2040:4370675
2012:Bibcode
1787:Bibcode
1751:4389678
1702:3156171
1679:Bibcode
1643:2659716
1620:Bibcode
1449:2413644
1239:Bibcode
1181:158–167
1160:2508336
1016:Bibcode
971:221–222
674:fetuses
651:Neoteny
582:tadpole
458:axolotl
447:neoteny
426:Neoteny
415:Effects
377:somites
296:single
190:Modern
98:History
3160:Ligand
2840:Operon
2731:
2723:
2686:
2678:
2641:
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2526:
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2004:Nature
1987:
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770:
736:
527:litter
369:snakes
339:Offset
200:zygote
139:". As
69:organs
63:in an
45:embryo
2729:S2CID
2684:S2CID
2497:S2CID
2371:JSTOR
2141:S2CID
2036:S2CID
1537:S2CID
1445:JSTOR
1255:S2CID
1116:S2CID
1002:(PDF)
874:S2CID
520:moose
325:Onset
317:okapi
153:gills
2800:The
2721:PMID
2676:PMID
2639:PMID
2602:ISBN
2572:ISBN
2542:PMID
2489:PMID
2452:ISBN
2420:PMID
2326:PMID
2243:ISBN
2220:PMID
2182:PMID
2133:PMID
2097:PMID
2028:PMID
1985:PMID
1944:OCLC
1934:ISBN
1911:OCLC
1901:ISBN
1846:link
1828:OCLC
1818:ISBN
1756:PMID
1707:PMID
1648:PMID
1589:OCLC
1579:ISBN
1529:PMID
1494:PMID
1453:PMID
1402:ISBN
1370:ISBN
1340:PMID
1322:Cell
1296:PMID
1210:ISBN
1185:ISBN
1156:OCLC
1146:ISBN
1108:PMID
1032:PMID
1012:306B
975:ISBN
941:ISBN
843:help
817:ISBN
768:PMID
734:ISBN
616:and
537:The
357:Rate
2804:of
2713:doi
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2668:doi
2664:118
2631:doi
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2306:doi
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2008:487
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