Heterochrony

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Giraffes acquired their long necks through heterochrony, extending the development period of the seven neck vertebrae's growth in the embryo to add length to the bones, not by adding more bones. Aniversity.jpg
Giraffes acquired their long necks through heterochrony, extending the development period of the seven neck vertebrae's growth in the embryo to add length to the bones, not by adding more bones.

In evolutionary developmental biology, heterochrony is any genetically controlled difference in the timing, rate, or duration of a developmental process in an organism compared to its ancestors or other organisms. This leads to changes in the size, shape, characteristics and even presence of certain organs and features. It is contrasted with heterotopy, a change in spatial positioning of some process in the embryo, which can also create morphological innovation. Heterochrony can be divided into intraspecific heterochrony, variation within a species, and interspecific heterochrony, phylogenetic variation, i.e. variation of a descendant species with respect to an ancestral species.

Contents

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

History

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

The concept of heterochrony was introduced by the German zoologist Ernst Haeckel in 1875, where he used it to define deviations from recapitulation theory, which held that "ontogeny recapitulates phylogeny". [3] [2] As Stephen Jay Gould pointed out, Haeckel's term is now used in a sense contrary to his coinage; Haeckel had assumed that embryonic development (ontogeny) of "higher" animals recapitulated their ancestral development (phylogeny), as when mammal embryos have structures on the neck that resemble fish gills 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 some organs could develop with displacements in position (heterotopy, another concept he originated) or time (heterochrony), as exceptions to his rule. He thus intended the term to mean a change in the timing of the embryonic development of one organ with respect to the rest of the same animal, whereas it is now used, following the work of the British evolutionary embryologist Gavin de Beer in 1930, to mean a change with respect to the development of the same organ in the animal's ancestors. [4] [5]

In 1928, the English embryologist Walter Garstang showed that tunicate larvae shared structures such as the notochord with adult vertebrates, and suggested that the vertebrates arose by paedomorphosis (neoteny) from such a larva. The proposal implied (if it were correct) a shared phylogeny of tunicates and vertebrates, and that heterochrony was a principal mechanism of evolutionary change. [6]

Modern evolutionary developmental biology (evo-devo) studies the molecular genetics of development. It seeks to explain each step in the creation of an adult organism from an undifferentiated zygote in terms of the control of expression of one gene after another. Further, it relates such patterns of control of development to phylogeny. De Beer to some extent anticipated such late 20th-century science in his 1930 book Embryos and Ancestors , [7] showing that evolution could occur by heterochrony, such as in paedomorphosis, the retention of juvenile features in the adult. [8] [2] De Beer argued that this enabled rapid evolutionary change, too brief to be recorded in the fossil record, and in effect explaining why apparent gaps were likely. [9]

Mechanisms

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

Heterochrony can be divided into intraspecific and interspecific types.

Intraspecific heterochrony means changes in the rate or timing of development within a species. For example, some individuals of the salamander species Ambystoma talpoideum delay the metamorphosis of the skull. [11] Reilly and colleagues argue we can define these variant individuals as paedotypic (with truncated development relative to the ancestral condition), peratypic (with extended development relative to the ancestral condition), or isotypic (reaching the same ancestral shape, but via a different mechanism). [10]

Interspecific heterochrony means differences in the rate or timing of a descendant species relative to its ancestor. This can result in either paedomophosis (truncating the ancestral ontogeny), peramorphosis (extending past the ancestral ontogeny), or isomorphosis (reaching the same ancestral state via a different mechanism). [10]

There are three major mechanisms of heterochrony, [12] [13] [14] [15] each of which can change in either of two directions, giving six types of perturbations, which can be combined in various ways. [16] These ultimately result in extended, shifted, or truncated development of a particular process, such as the action of a single toolkit gene, [17] 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. [10]

Despite greatly differing neck lengths, giraffes (right) have no more cervical vertebrae, just 7, than their fellow giraffids, okapi (left). With the number constrained, the development of the vertebrae is extended, allowing them to grow longer. Okapi Giraffe Neck.png
Despite greatly differing neck lengths, giraffes (right) have no more cervical vertebrae, just 7, than their fellow giraffids, okapi (left). With the number constrained, the development of the vertebrae is extended, allowing them to grow longer.

A dramatic illustration of how acceleration can change a body plan is seen in snakes. Where a typical vertebrate like a mouse has only around 60 vertebrae, snakes have between around 150 to 400, giving them extremely long spinal columns and enabling their sinuous locomotion. Snake embryos achieve this by accelerating their system for creating somites (body segments), which relies on an oscillator. The oscillator clock runs some four times faster in snake than in mouse embryos, initially creating very thin somites. These expand to adopt a typical vertebrate shape, elongating the body. [18] Giraffes gain their long necks by a different heterochrony, extending the development of their cervical vertebrae; they retain the usual mammalian number of these vertebrae, seven. [1] This number appears to be constrained by the use of neck somites to form the mammalian diaphragm muscle; the result is that the embryonic neck is divided into three modules, the middle one (C3 to C5) serving the diaphragm. The assumption is that disrupting this would kill the embryo rather than giving it more vertebrae. [19]

Detection

Heterochrony can be identified by comparing phylogenetically close species, for example a group of different bird species whose legs differ in their average length. These comparisons are complex because there are no universal ontogenetic timemarkers. The method of event pairing attempts to overcome this by comparing the relative timing of two events at a time. [20] This method detects event heterochronies, as opposed to allometric changes. It is cumbersome to use because the number of event pair characters increases with the square of the number of events compared. Event pairing can however be automated, for instance with the PARSIMOV script. [21] A recent method, continuous analysis, rests on a simple standardization of ontogenetic time or sequences, on squared change parsimony and phylogenetic independent contrasts. [22]

Effects

Paedomorphosis

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

Paedomorphosis can be the result of neoteny, the retention of juvenile traits into the adult form as a result of retardation of somatic development, or of progenesis, the acceleration of developmental processes such that the juvenile form becomes a sexually mature adult. 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. [23]

Neoteny retards the development of the organism into an adult, and has been described as "eternal childhood". [24] In this form of heterochrony, the developmental stage of childhood is itself extended, and certain developmental processes that normally take place only during childhood (such as accelerated brain growth in humans [25] [26] [27] ), 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. [28]

Progenesis (or paedogenesis) can be observed in the axolotl (Ambystoma mexicanum). Axolotls reach full sexual maturity while retaining their fins and gills (in other words, still in the juvenile form of their ancestors). They will remain in aquatic environments in this truncated developmental form, rather than moving onto land as other sexually mature salamander species. This is thought to be a form of hypomorphosis (earlier ending of development) [29] that is both hormonally [30] [31] and genetically driven. [30] The entire metamorphosis that would allow the salamander to transition into the adult form is essentially blocked by both of these drivers. [32]

Paedomorphosis by progenesis may play a critical role in avian cranial evolution. [33] The skulls and beaks of living, adult birds retain the anatomy of the juvenile theropod dinosaurs from which they evolved. [34] 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. [35] A juvenile avian ancestor (as typified by Coelophysis ) would have a short face, large eyes, a thin palate, narrow jugal bone, tall and thin postorbitals, restricted adductors, and a short and bulbous braincase. As an organism such as this aged, they would change greatly in their cranial morphology to develop a robust skull with larger, overlapping bones. Birds, however, retain this juvenile morphology. [36] Evidence from molecular experiments suggests both fibroblast growth factor 8 (FGF8) and members of the WNT signalling pathway have facilitated paedomorphosis in birds. [37] These signalling pathways are known to play roles in facial patterning in other vertebrate species. [38] This retention of the juvenile ancestral state has driven other changes in the anatomy that result in a light, highly kinetic (moveable) skull composed of many small, non-overlapping bones. [36] [39] This is believed to have facilitated the evolution of cranial kinesis in birds [36] which has played a critical role in their ecological success. [39]

Peramorphosis

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

Peramorphosis is delayed maturation with extended periods of growth. An example is the extinct Irish elk. From the fossil record, its antlers spanned up to 12 feet (3.7 m) wide, which is about a third larger than the antlers of its close relative, the moose. The Irish elk had larger antlers due to extended development during their period of growth. [40] [41]

Another example of peramorphosis is seen in insular (island) rodents. Their characteristics include gigantism, wider cheek and teeth, reduced litter size, and longer lifespan. Their relatives that inhabit continental environments are much smaller. Insular rodents have evolved these features to accommodate the abundance of food and resources they have on their islands. These factors are part of a complex phenomenon termed Island syndrome or Foster's rule. [42]

The mole salamander, 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. [43] 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. [44] These ideas were reinforced by other studies, such as peramorphosis in the Puerto Rican tree frog. Another reason could be generation time, or the lifespan of the species in question. When a species has a relatively short lifespan, natural selection favors evolution of paedomorphosis (e.g. Axolotl: 7–10 years). Conversely, in long lifespans natural selection favors evolution of peramorphosis (e.g. Irish Elk: 20–22 years). [42]

Across the animal kingdom

Heterochrony is responsible for a wide variety of effects [45] such as the lengthening of the fingers by adding extra phalanges in dolphins to form their flippers, [46] sexual dimorphism, [6] and the polymorphism seen between insect castes. [47]

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

Garstang's hypothesis

Walter Garstang suggested the neotenous origin of the vertebrates from a tunicate larva, [6] in opposition to Darwin's opinion that tunicates and vertebrates both evolved from animals whose adult form was similar to (frog) tadpoles and the 'tadpole larvae' of tunicates. According to Richard Dawkins, [48] Garstang's opinion was also held by Alister Hardy, and is still held by some modern biologists. However, according to others, closer genetic investigation rather seems to support Darwin's old opinion:

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 larvaceans 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. [49]

— Richard Dawkins
Neoteny in human development Human development neoteny body and head proportions pedomorphy maturation aging growth.png
Neoteny in human development

In humans

Several heterochronies have been described in humans, relative to the chimpanzee. In chimpanzee fetuses, brain and head growth starts at about the same developmental stage and grow at a rate similar to that of humans, but growth stops soon after birth, whereas humans continue brain and head growth several years after birth. This particular type of heterochrony, hypermorphosis, involves a delay in the offset of a developmental process, or what is the same, the presence of an early developmental process in later stages of development. Humans have some 30 different neotenies in comparison to the chimpanzee, retaining larger heads, smaller jaws and noses, and shorter limbs, features found in juvenile chimpanzees. [50] [51]

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). [52]

See also

Related Research Articles

<span class="mw-page-title-main">Embryo drawing</span> Illustration of embryos in their developmental sequence

Embryo drawing is the illustration of embryos in their developmental sequence. In plants and animals, an embryo develops from a zygote, the single cell that results when an egg and sperm fuse during fertilization. In animals, the zygote divides repeatedly to form a ball of cells, which then forms a set of tissue layers that migrate and fold to form an early embryo. Images of embryos provide a means of comparing embryos of different ages, and species. To this day, embryo drawings are made in undergraduate developmental biology lessons.

Neoteny, also called juvenilization, is the delaying or slowing of the physiological, or somatic, development of an organism, typically an animal. Neoteny is found in modern humans compared to other primates. In progenesis or paedogenesis, sexual development is accelerated.

The theory of recapitulation, also called the biogenetic law or embryological parallelism—often expressed using Ernst Haeckel's phrase "ontogeny recapitulates phylogeny"—is a historical hypothesis that the development of the embryo of an animal, from fertilization to gestation or hatching (ontogeny), goes through stages resembling or representing successive adult stages in the evolution of the animal's remote ancestors (phylogeny). It was formulated in the 1820s by Étienne Serres based on the work of Johann Friedrich Meckel, after whom it is also known as Meckel–Serres law.

<span class="mw-page-title-main">Ontogeny</span> Origination and development of an organism

Ontogeny is the origination and development of an organism, usually from the time of fertilization of the egg to adult. The term can also be used to refer to the study of the entirety of an organism's lifespan.

<span class="mw-page-title-main">Evolutionary developmental biology</span> Comparison of organism developmental processes

Evolutionary developmental biology is a field of biological research that compares the developmental processes of different organisms to infer how developmental processes evolved.

<span class="mw-page-title-main">Atavism</span> Reappearance of a genetic trait once thought extinct

In biology, an atavism is a modification of a biological structure whereby an ancestral genetic trait reappears after having been lost through evolutionary change in previous generations. Atavisms can occur in several ways, one of which is when genes for previously existing phenotypic features are preserved in DNA, and these become expressed through a mutation that either knocks out the dominant genes for the new traits or makes the old traits dominate the new one. A number of traits can vary as a result of shortening of the fetal development of a trait (neoteny) or by prolongation of the same. In such a case, a shift in the time a trait is allowed to develop before it is fixed can bring forth an ancestral phenotype. Atavisms are often seen as evidence of evolution.

<span class="mw-page-title-main">Axolotl</span> Species of salamander

The axolotl is a paedomorphic salamander closely related to the tiger salamander. It is unusual among amphibians in that it reaches adulthood without undergoing metamorphosis. Instead of taking to the land, adults remain aquatic and gilled. The species was originally found in several lakes underlying what is now Mexico City, such as Lake Xochimilco and Lake Chalco. These lakes were drained by Spanish settlers after the conquest of the Aztec Empire, leading to the destruction of much of the axolotl's natural habitat.

<span class="mw-page-title-main">Amniote</span> Clade of tetrapods including reptiles, birds and mammals

Amniotes are tetrapod vertebrate animals belonging to the clade Amniota, a large group that comprises the vast majority of living terrestrial and semiaquatic vertebrates. Amniotes evolved from amphibian ancestors during the Carboniferous period and further diverged into two groups, namely the sauropsids and synapsids. They are distinguished from the other living tetrapod clade — the non-amniote lissamphibians — by the development of three extraembryonic membranes, thicker and keratinized skin, and costal respiration.

<span class="mw-page-title-main">Viviparity</span> Development of the embryo inside the mother

In animals, viviparity is development of the embryo inside the body of the mother, with the maternal circulation providing for the metabolic needs of the embryo's development, until the mother gives birth to a fully or partially developed juvenile that is at least metabolically independent. This is opposed to oviparity, where the embryos develop independently outside the mother in eggs until they are developed enough to break out as hatchlings; and ovoviviparity, where the embryos are developed in eggs that remain carried inside the mother's body until the hatchlings emerge from the mother as juveniles, similar to a live birth.

<span class="mw-page-title-main">Dollo's law of irreversibility</span> Hypothesis by Louis Dollo in 1893, which states evolution is not exactly reversible

Dollo's law of irreversibility, proposed in 1893 by Belgian paleontologist Louis Dollo states that, "an organism never returns exactly to a former state, even if it finds itself placed in conditions of existence identical to those in which it has previously lived ... it always keeps some trace of the intermediate stages through which it has passed."

<span class="mw-page-title-main">Pharyngeal slit</span> Repeated openings that appear along the pharynx of chordates

Pharyngeal slits are filter-feeding organs found among deuterostomes. Pharyngeal slits are repeated openings that appear along the pharynx caudal to the mouth. With this position, they allow for the movement of water in the mouth and out the pharyngeal slits. It is postulated that this is how pharyngeal slits first assisted in filter-feeding, and later, with the addition of gills along their walls, aided in respiration of aquatic chordates. These repeated segments are controlled by similar developmental mechanisms. Some hemichordate species can have as many as 200 gill slits. Pharyngeal clefts resembling gill slits are transiently present during the embryonic stages of tetrapod development. The presence of pharyngeal arches and clefts in the neck of the developing human embryo famously led Ernst Haeckel to postulate that "ontogeny recapitulates phylogeny"; this hypothesis, while false, contains elements of truth, as explored by Stephen Jay Gould in Ontogeny and Phylogeny. However, it is now accepted that it is the vertebrate pharyngeal pouches and not the neck slits that are homologous to the pharyngeal slits of invertebrate chordates. Pharyngeal arches, pouches, and clefts are, at some stage of life, found in all chordates. One theory of their origin is the fusion of nephridia which opened both on the outside and the gut, creating openings between the gut and the environment.

<span class="mw-page-title-main">Body plan</span> Set of morphological features common to members of a phylum of animals

A body plan, Bauplan, or ground plan is a set of morphological features common to many members of a phylum of animals. The vertebrates share one body plan, while invertebrates have many.

<span class="mw-page-title-main">Gavin de Beer</span> British evolutionary embryologist (1899–1972)

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

<i>Ontogeny and Phylogeny</i> Book by Stephen Jay Gould

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

<span class="mw-page-title-main">Morphogenetic field</span> Developmental biology concept

In the developmental biology of the early twentieth century, a morphogenetic field is a group of cells able to respond to discrete, localized biochemical signals leading to the development of specific morphological structures or organs. The spatial and temporal extents of the embryonic field are dynamic, and within the field is a collection of interacting cells out of which a particular organ is formed. As a group, the cells within a given morphogenetic field are constrained: thus, cells in a limb field will become a limb tissue, those in a cardiac field will become heart tissue. However, specific cellular programming of individual cells in a field is flexible: an individual cell in a cardiac field can be redirected via cell-to-cell signaling to replace specific damaged or missing cells. Imaginal discs in insect larvae are examples of morphogenetic fields.

The urbilaterian is the hypothetical last common ancestor of the bilaterian clade, i.e., all animals having a bilateral symmetry.

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

<span class="mw-page-title-main">Neoteny in humans</span> Retention of juvenile traits into adulthood

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

In Embryology a phylotypic stage or phylotypic period is a particular developmental stage or developmental period during mid-embryogenesis where embryos of related species within a phylum express the highest degree of morphological and molecular resemblance. Recent molecular studies in various plant and animal species were able to quantify the expression of genes covering crucial stages of embryo development and found that during the morphologically defined phylotypic period the evolutionary oldest genes, genes with similar temporal expression patterns, and genes under strongest purifying selection are most active throughout the phylotypic period.

Human evolutionary developmental biology or informally human evo-devo is the human-specific subset of evolutionary developmental biology. Evolutionary developmental biology is the study of the evolution of developmental processes across different organisms. It is utilized within multiple disciplines, primarily evolutionary biology and anthropology. Groundwork for the theory that "evolutionary modifications in primate development might have led to … modern humans" was laid by Geoffroy Saint-Hilaire, Ernst Haeckel, Louis Bolk, and Adolph Schultz. Evolutionary developmental biology is primarily concerned with the ways in which evolution affects development, and seeks to unravel the causes of evolutionary innovations.

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