EVO-DEVO

Heterochrony: the Evolution of Development

Kenneth J. McNamara

Published online: 5 June 2012# Springer Science+Business Media, LLC 2012

Abstract Heterochrony can be defined as change to thetiming or rate of development relative to the ancestor.Because organisms generally change in shape as well asincrease in size during their development, any variationto the duration of growth or to the rate of growth ofdifferent parts of the organism can cause morphologicalchanges in the descendant form. Heterochrony takes theform of both increased and decreased degrees of devel-opment, known as “peramorphosis” and “paedomorpho-sis,” respectively. These are the morphologicalconsequences of the operation of processes that changethe duration of the period of an individual’s growth,either starting or stopping it earlier or later than in theancestor, or by extending or contracting the period ofgrowth. Heterochrony operates both intra- and interspe-cifically and is the source of much intraspecific varia-tion. It is often also the cause of sexual dimorphism.Selection of a sequence of species with a specific het-erochronic trait can produce evolutionary trends in theform of pera- or paedomorphoclines. Many different lifehistory traits arise from the operation of heterochronicprocesses, and these may sometimes be the targets ofselection rather than morphological features themselves.It has been suggested that some significant steps inevolution, such as the evolution of vertebrates, wereengendered by heterochrony. Human evolution wasfuelled by heterochrony, with some traits, such as alarge brain, being peramorphic, whereas others, suchas reduced jaw size, are paedomorphic.

Keywords Evolution . Heterochrony . Paedomorphosis .

Peramorphosis . Sexual dimorphism . Evolutionary trends

Introduction

Lurking deep in Darwin’s monumental tome On the Originof Species, first published in 1859 (Darwin 1859), is a short,much neglected, section. Lying between pages 439 and 450in the first edition and between pages 386 and 396 in mycopy of the sixth edition published in 1878 is the kernel ofsome ideas that were intermittently to surface in the field ofevolutionary theory for the following 150 years. Theseinsights now form a major part of modern evolutionarytheory. The section in question was entitled “Embryology”by Darwin in the first edition, but “Development and Em-bryology” in the sixth, and highlights the importance toevolution of changes to the pattern of an organism’s onto-genetic development.

Darwin’s (1878, p. 386) view of development and em-bryology was that, “This is one of the most important sub-jects in the whole round of natural history.” But his ideas onthe significance of these intrinsic aspects of evolutionarytheory are scattered through much of the book and form thebasis for many of Darwin’s ideas on what generates thevariation that is the raw material upon which natural selec-tion operates. Darwin was undoubtedly influenced by ideasthat had been around since the early nineteenth century andpromulgated by embryologists like von Baer in Germanyand Serres in France (see Gould 1977). Darwin (1878, p.396) encapsulated these ideas by observing that, “Embryol-ogy rises greatly in interest, when we look at the embryo asa picture, more or less obscure, of the progenitor, either in itsadult or larval state, of all members of the same great class.”

K. J. McNamara (*)Department of Earth Sciences, University of Cambridge,Downing Street,Cambridge CB2 3EQ, UKe-mail: kjm47@cam.ac.uk

Evo Edu Outreach (2012) 5:203–218DOI 10.1007/s12052-012-0420-3

Evolution was perceived as having proceeded by anincrease in complexity and an increase in the extent ofontogenetic change, by terminal addition. This idea was tobe encapsulated by a great adherent of Darwin’s concept ofnatural selection, Ernest Haeckel (1866), who wrote that,“Ontogeny is the brief and rapid recapitulation of phylogenydependent on the physiological functions of heredity (repro-duction) and adaptation (nutrition).” Within the develop-mental history of a single individual, it was believed, laythe entire evolutionary history of the group. Each animal orplant was perceived as a repository of all that had gonebefore—an infinite number of evolutionary Russian dolls.

But to Darwin, developmental change was not alwaysunidirectional, leading to more complex forms. Darwin rec-ognized that there were many instances when species hadevolved that had undergone less developmental change thantheir ancestors: “…some animals are capable of reproducingat a very early age, before they have acquired their perfectcharacters; and if this power became thoroughly well devel-oped in a species, it seems probable that the adult stage ofdevelopment would sooner or later be lost; and in this case,especially if the larva differed much from the mature form,the character of the species would be greatly changed anddegraded.” (Darwin 1878, p. 149).

These views presaged ideas that resurfaced in the 1920sand were articulated by the English embryologist WalterGarstang, who argued that vertebrates could have evolvedfrom something as inconsequential as the larva of a tunicate(sea squirt). This tadpole-like juvenile possesses many ofthe attributes present in adult vertebrates (see below)(Garstang 1928). To get his point across, Garstang wasmoved to express his ideas about this phenomenon in theMexican salamander, or axolotl (Fig. 1), in verse:

Ambystoma's a giant newt who rears in swampywaters,As other newts are wont to do, a lot of fishy daughters:These Axolotls, having gills, pursue a life aquatic,

But, when they should transform to newts, are naughtyand erratic.They change upon compulsion, if the water grows toofoul,For then they have to use their lungs, and go ashore toprowl:But when a lake's attractive, nicely aired, and full offood,They cling to youth perpetual, and rear a tadpolebrood.And newts Perrenibranchiate have gone from bad toworse:They think aquatic life is bliss, terrestrial a curse.They do not even contemplate a change to suit theweather,But live as tadpoles, breed as tadpoles, tadpoles alltogether!

What Garstang argued was that major evolutionarychanges (including the evolution of vertebrates themselves)could have arisen from such arrested development and re-tention of ancestral juvenile traits by descendant adults.Garstang called this paedomorphosis. It was quite the op-posite to what Haeckel had suggested, his so-called “reca-pitulation.” With the rise in importance of genetics in theearly twentieth century, the role of developmental change inevolution all but disappeared from the literature.

But, in 1977, in his seminal book Ontogeny and Phylog-eny, Steven J. Gould argued that not only was developmen-tal change a fundamental aspect of evolution but that thetwo “forms,” paedomorphosis and recapitulation, both oc-curred: development could slow down or speed up, or beshortened or prolonged, in the descendent relative to theancestor. This is what generated much of the raw materialfor natural selection to work on and reflected ideas articu-lated by Darwin about 120 years earlier, but largelyforgotten.

Darwin, though, was not one for using jargon, and Isuspect that it is for this reason that his insights have beenneglected. Gould was at the forefront of the renaissance inrecent years in the relationship between development andevolution. Although subsequently touted as the “new” as-pect of evolutionary theory in the guise of evolutionarydevelopmental biology, many of the old ideas that Gouldand others espoused in the 1970s and 1980s had been amal-gamated under the banner of “heterochrony,” a term coined byHaeckel. This formed the basis for the resurgence in interest inthe role of developmental change in evolution, which has seena profusion of papers on developmental genetics to explainmany of the changes seen in the phenotype.

Until the 1970s, evolution was thought to center on theclassical Darwinian paradigm of natural selection and

Fig. 1 The classic example of paedomorphosis, the axolotl, or Mex-ican salamander Ambystoma mexicanum. Reproduced with permissionfrom McNamara (1997)

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genetics: genes provide the mutations on which naturalselection operates. However, the publication of Gould’sOntogeny and Phylogeny highlighted the added significanceof developmental changes in evolution. Much of the earlyresearch in this field was carried out by paleontologists inthe 1980s, focusing on macroevolutionary changes resultingfrom heterochrony (see McKinney 1988; McKinney andMcNamara 1991; McNamara 1995a, 1997). In the 1990s,an increasing number of biologists began to recognize theimportance of developmental change in evolution (Hall1992).

What Is Heterochrony?

Heterochrony can be defined as “change to the timing or rateof developmental events, relative to the same events in theancestor” (Alberch et al. 1979; McKinney and McNamara1991). All organisms have an ontogeny. This is their lifehistory, from the time of conception until death. Whileorganisms increase in size as they grow, from an initialegg, through larval or embryonic stages, to juvenile andthen adult stages, they also change in shape. You, for in-stance, look very different now from what you looked likewhen you were born, for the simple reason that many partsof your body have changed in relative shape during yourontogeny. Most organisms have a finite period of growth,which usually ends at the onset of sexual maturity, both sizeand shape slowing down markedly, or stopping. Withinpopulations of a single species, individuals do not all growand develop at the same rate or for the same duration;individuals grow at slightly different rates and for slightlydifferent durations. The same holds for many species,where, between closely related species, the main morpho-logical differences arise from variations to the rate andduration of growth.

Certain parts of a single individual may grow for relativelydifferent lengths of time and at different relative rates. Thus, inmany vertebrates, for instance, the rate of growth of the head isrelatively greater than growth of the trunk or limbs during theembryonic phase of growth, whereas after birth, these post-cranial parts undergo a relatively greater amount of growth.Likewise, the formation of finger bones in dolphins can arisefrom an extension of the period of growth of these parts of thelimbs (Richardson and Oelschläger 2002). Thus, slightchanges to the rate or duration of growth of various parts ofthe body during ontogeny can greatly impact upon the appear-ance of the final adult form. All such changes to the rate andduration of growth of all or part of an organism compared withits ancestor are what define heterochrony.

An organism’s growth is determined by its genetic makeup.The genes determine, to a large degree, its morphological,physiological, and behavioral characteristics—so what it

looks like, how it functions, and how it behaves. It is nowrecognized that developmental genes, particularly those regu-lating embryonic or larval development, play a major role inevolution (Richardson and Brakefield 2003). One group ofgenes known as homeotic genes controls the timing of expres-sion of growth factors that determine when and where aparticular morphological structure starts to develop and itsduration of growth. Thus, any changes to the timing of ex-pression of these controlling genes, or the period during whichthey influence growth, will result in a descendant that can lookmarkedly different from its immediate ancestor.

Any genes that control the regulation of development arenow collectively known as “heterochronic genes.” Slackand Ruvkun (1998, p. 375) wrote that, “Genes that controlthe temporal dimension of development, heterochronicgenes, can be thought of as the temporal analogs of thehomeotic genes, which regulate spatial dimensions (e.g.,anterior-posterior, dorsal-ventral axes) during developmentof metazoans. These pathways generate graded or binarylevels of regulatory factors that pattern one axis of thedeveloping animal. Heterochronic genes may be the targetof mutations that cause heterochronic change in phylogeny.”

Subtle morphological changes therefore occur continual-ly within populations, arising from slight variations betweenindividuals in the duration and rate of growth of the wholeorganism, or of just particular traits. Within populations, thisproduces so-called intraspecific variation: heterochronicchange being targeted by natural selection. Because hetero-chrony is so important in providing raw material on whichnatural selection can operate, it plays a very important rolein evolution (McKinney and McNamara 1991; McNamara1995a, b, 1997; Tills et al. 2011). As well as operatingwithin species at this level of intraspecific variation, it alsooccurs between sexes (McNamara 1995b); between species,in generating evolutionary trends (McNamara 1982, 1990);and in the evolution of major morphological novelties, such asvertebrates and birds (McNamara 1997; McNamara andMcKinney 2005).

Classifying Heterochrony

Heterochrony can be separated into two different types:paedomorphosis (literally “child-shape”) and peramorpho-sis (literally “beyond-shape”). A descendant organism,whether it be a descendant individual within a populationor a geologically younger species, when compared with itsancestor, can show either “less” or “more” growth. Paedo-morphosis is the type of heterochrony where there is lessgrowth during ontogeny in a descendant form, comparedwith its ancestor. The name reflects the fact that descendantadults resemble the juvenile condition of the ancestor. In theother form of heterochrony, the descendant undergoes more

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development and is said to show peramorphosis. Frequently,though certainly not inevitably, paedomorphic forms may besmaller than their ancestor, while peramorphic forms tend tobe larger. Paedomorphosis and peramorphosis are not evo-lutionary processes in themselves but are descriptive termsthat describe the appearance of the descendant morphology.They are the morphological (and sometimes behavioral) endresult of the operation of a variety of heterochronicprocesses.

Paedomorphosis and peramorphosis can each be pro-duced by three different, complementary processes: varia-tions in time of cessation of growth, variation in time ofcommencement of growth, and change in rate of growth(Alberch et al. 1979; McNamara 1986a). Paedomorphosisoccurs if the period of growth of the descendant form isstopped prematurely—progenesis (hypomorphosis of Reillyet al. 1997); if onset of growth is delayed—postdisplace-ment; or if the rate of growth is less in the descendant than inthe ancestor—neoteny (deceleration of Reilly et al. 1997)(Figs. 2 and 3). Progenesis will affect the entire organism ifpremature cessation of growth is caused by the earlier onsetof sexual maturity. Like neoteny and postdisplacement, itmay, though, also target specific morphological features.

Peramorphosis occurs if the period of growth in thedescendant is extended (hypermorphosis), if the onset ofgrowth occurs earlier in the descendant than in the ancestor(predisplacement), or if the growth rate is increased (accel-eration). Hypermorphosis, like progenesis, can affect thewhole organism when the onset of sexual maturity isdelayed, because fast juvenile growth rates will persist fora longer period. Alternatively, hypermorphosis can targetjust certain traits. Acceleration and predisplacement willaffect only specific features, not the entire organism.

While this categorization of heterochrony into these sixbasic processes appears to have much utility, it has beenargued that this presupposes a uniformity of morphologicalchange during ontogeny, which may not always be the case(Rice 1997). It is often possible to compartmentalize ontog-eny into discrete growth phases, such as embryonic,

infantile, and juvenile growth in mammals, or discretegrowth instars in arthropods. Each of these phases can haveits own ontogenetic trajectory, which might be at variancewith other growth phases. Each can be subjected to its ownheterochronic variation, involving extensions or contrac-tions of these phases, or discrete variation in growth rates.This type of intra-ontogenetic heterochrony is called se-quential heterochrony (McNamara 2002).

The terminology of heterochrony can be used to describethe appearance of discrete structures formed during ontoge-ny, such as the number of vertebrae or digits (so-called“meristic” characters) that develop during ontogeny. It canalso be applied to the subsequent changes in shape of thesestructures during growth. These have been termed mitoticand growth heterochrony, respectively (McKinney andMcNamara 1991). In many organisms, mitotic hetero-chrony, particularly that induced by pre- and postdisplace-ment, can play a very significant role during very earlydevelopmental stages. This is due to variations betweenancestors and descendants in the timing of onset of devel-opment of major morphological features. Neoteny and ac-celeration, in other words reduced and accelerated growthrates, respectively, will be especially common during laterontogenetic development.

The relationship between size and shape is known asallometry and arises from differential growth rates betweendifferent parts of the body or in different axes on the samestructure. For instance, as a bone grows, it may becomerelatively longer and thinner because growth is occurringat a faster rate along one axis than another. Should therelative size and shape of a structure remain the samethroughout ontogeny, relative to the organism’s overall bodysize, growth is described as isometric. Although very feworganisms grow isometrically (Klingenberg 1998), someindividual traits, such as vertebrate skeletal elements, canbe isometric. Usually, though, a structure such as a bone willchange shape and size relative to the size and shape of thewhole organism during ontogeny. If the bone increases inrelative size, growth is said to occur by positive allometry.

Fig. 2 The hierarchicalclassification of heterochrony(based on Alberch et al. 1979)

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However, if there is a relative reduction in size, growth issaid to show negative allometry.

There is a close relationship between allometry and het-erochrony because heterochrony involves changes not onlyin time but also in shape and size. The consequence ofchanging growth rates (acceleration and neoteny) is to cause

such allometric changes. Extensions or contractions of theperiod of growth–in other words, hypermorphosis or pro-genesis–have the effect of accentuating or reducing theeffects of allometric changes. Consequently, those organ-isms that undergo pronounced allometric change duringgrowth are more likely to generate very different descendant

Fig. 3 A hypothetical animal which, during its ontogeny, undergoes anumber of morphological changes. Peramorphic descendants develop“beyond” the ancestor; padomorphic descendants retain juvenile an-cestral features. In hypermorphosis, growth stops later; in acceleration,the horns and tails grow faster; in predisplacement, the horns and tail

start growing earlier. In progenesis, growth stops earlier; in neoteny,the horns and tail grow at a slower rate; in postdisplacement, the hornsand tail start their growth relatively later. Reproduced with permissionfrom McNamara (1997)

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adult morphologies if rates or durations of growth havechanged.

For example, when the skull of the domestic dog, Canisfamiliaris, is compared with that of the domestic cat, Felisdomestica, the dog skull can be seen to undergo pronouncedpositive allometric change during ontogeny, particularly bystrong growth of the muzzle (Fig. 4). By artificially chang-ing growth rates and timing, a wide range of breeds that varysubstantially in cranial morphology have been produced.For instance, tiny dogs like chihuahuas or King Charlesspaniels are very paedomorphic, but large Irish wolfhoundsare peramorphic (Fig. 5). In contrast, the extent of allometricchange is minimal in the domestic cat, so that breeds do notdiffer greatly in morphology (Wayne 1986). In the naturalworld, the same effect occurs. Those organisms that producea wider range of variation because of greater ontogeneticallometric change produce more raw material for natural

selection, leading to the evolution of a wide range ofdescendants.

It may be trifle hard to imagine but your fluffy littlePekingese dog peering at you with doting eyes is really awolf. This is because, as one of the numerous breeds ofdomestic dog (many unwittingly selected for by humans forparticular heterochronic traits), it “evolved” from a wolf. Allthe traits present in the first known domestic dogs, whichdate back to at least 30,000 years (Germonpré et al. 2009),occur in puppies of wolves: shortened muzzles; steeper,wider foreheads; and smaller body size (Fig. 6). Thus,domestic dogs are essentially paedomorphic wolves (Morey1994). But Mesolithic man was unlikely to have beenselecting for these traits. He was more likely to have beenselecting aspects of juvenile wolf behavior. Such more ame-nable juvenile behavior is more likely to have put wolf pupsin contact with humans. Socialization in dogs is best devel-oped when they are between three and 12 weeks old, at atime when primary bonds are formed. Those that fail to

Fig. 4 Proportionate differences in skull shapes of domestic dogs andcats as they grow up. Dogs undergo much greater shape changes thando cats. This explains the greater diversity of skull shapes in differentbreeds of dogs, compared with cats. Modified and redrawn fromWayne (1986)

Fig. 5 The large differences in shape of the skull between threedifferent breeds of dogs, shown in longitudinal section: the “most”paedomorphic at the top, the “most” peramorphic at the bottom. Theshorter the face, the more vaulted the cranium. Modified and redrawnfrom Wayne (1986)

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bond with humans are likely to have been driven away orkilled.

Identifying Heterochrony

Recognizing the effect of heterochronic processesrequires knowledge of ontogenetic information fromboth ancestral and descendant forms. Whereas manyontogenetic changes will be species specific, there aremany general changes that occur within particulargroups of higher taxa, so that even if the ontogeny ofthe descendant and presumed ancestral form are notknown in detail, a number of inferences concerninglikely occurrence of heterochrony can still be made.Many examples of heterochrony have been documentedin the fossil record (McNamara 1995a, 1997). Whendealing with fossil material, two of the factors involvedin heterochrony, namely shape and size, are alwaysavailable. As such, it is possible to assess whether aparticular species is either peramorphic or paedomor-phic. However, understanding which processes havecaused the heterochrony can be difficult when dealingwith fossil material, as accurate details of the durationof rate of growth are often unknown.

However, one group that can provide such information isdinosaurs. A number of studies have been made describinggrowth rates and time of onset of sexual maturity andcessation or reduction in growth in dinosaurs (McNamaraand Long 2012). For instance, studies of bone microstruc-ture in a range of dinosaurs show that periodic, possiblyseasonal, growth is reflected in growth lines in the bone (see

below). This allows “real”-time information to be obtainedfrom such fossil material, making it possible to producerelatively accurate inferences of the type of heterochronicprocesses operating in extinct species.

Many paleontological studies have used size as a proxy fortime—that is, if one species is smaller than another, it isassumed that it grew for a shorter period of time. Conse-quently, assumptions are made that, for example, a descen-dant that is smaller than its ancestor and shows paedomorphicmorphological characteristics, ceased growing at an earlierage and therefore arose by progenesis. So, for instance, thesmall late Cretaceous tyrannosaurid dinosaur, Maleevosau-rus, which was “only” five meters long, is smaller than itspresumed ancestor but also possesses some paedomorphicfeatures. As I have pointed out, paedomorphosis can becaused by neoteny or progenesis. Either process could ex-plain paedomorphosis in these smaller tyrannosaurs. Howev-er, studies in other groups of organisms show that neotenytends to target only specific structures, not the whole organ-ism. In the case of Maleevosaurus, although progenesis ismore probable, in the absence of actual growth rate data, it isnot possible to determine the process precisely.

While it may often seem to be relatively straightforwardto identify heterochrony, such as a reduction or increase innumber of segments in adults of different species of trilo-bites (Fig. 8), identifying subtle allometric changes betweenancestor and descendant may be less obvious. One tech-nique used in a number of studies is morphometrics. Here,fixed positions (known as landmarks) on, say, a trilobitehead, are recorded for different ontogenetic stages. Theseare then compared with the same positions on a presumeddescendant species. Subtle variations in growth rates of parts

Fig. 6 Evolution of thedomestic dog from the wolf bypaedomorphosis, showing thesimilarity of the skull of earlydomestic adult dogs with that ofjuvenile wolves. Modified andredrawn from Morey (1994)

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of the structure will occur by heterochronic processes that canbe identified (e.g., Webster et al. 2001). Mitteroecker et al.(2005) have applied this technique to a study of the evolutionof cranial growth in chimpanzees. However, they cautionagainst the use of single characters when trying to interpretheterochrony. Rather, they argue (Mitteroecker et al. 2005, p.255), “…that a single morphological characterization,descriptions in terms of bigger/smaller or more/less of some-thing, should generally not be subjected to heterochronicinterpretation, nor should single ratios. Multivariate analysiscircumvents this theoretical problem when heterochrony isdefined as multivariate ontogenetic scaling along a commonontogenetic trajectory.”

Relative Frequency of Heterochrony

It has been argued that theoretically, paedomorphosis andperamorphosis should occur with roughly equal frequencies(Gould 1977). Yet studies of heterochrony in the fossil recordsuggest that this may not always be the case. Amphibiansshow a preponderance of paedomorphosis (McNamara 1988),which may be related to their large cell size, causing a reducedrate of cellular division (McNamara 1997).

Paedomorphosis has occurred many times in frogs, forexample, resulting in the development of many miniaturespecies. The 29 smallest species (with the smallest havingan average body length of just 7.7 millimeters) are spreadacross five families and 11 genera (Rittmeyer et al. 2012).As well as very reduced size, these frogs have reducedfecundity and show paedomorphic traits of reduced

ossification and lack of digits. Moreover, many of thesefrogs are direct developers, lacking a tadpole stage, and assuch form a distinct ecological guild (Rittmeyer et al. 2012).

In contrast, peramorphosis may have beenmore frequent indinosaurs, in particular being a major contributing factor to theevolution of very large body size (McNamara and Long2012). Many types of dinosaurs, such as sauropods, ceratop-sians, theropods, and ornithopods, show not only trends to-ward increased body size but also the attainment of larger,more complex morphologies by peramorphosis (Fig. 7).

Heterochrony played a very important role in the evolu-tion of trilobites. This is thought to have been due to theirdevelopmental systems having been poorly constrainedwhen they first evolved in the Early Cambrian (McNamara1986b). This is shown by the high variability in segmentnumber, both within and between species in these earliesttrilobites. Through Cambrian times, there is progressiveimprovement in the trilobites’ developmental systems, sothat by post-Cambrian times, many families of trilobiteshave fixed thoracic segment number. Moreover, documentedcases indicate that in Cambrian trilobites, natural selectionfavored paedomorphic processes more than peramorphicones (Fig. 8). However, greater morphological diversity ofpost-Cambrian trilobites may have been facilitated by a shiftto selection for mainly peramorphic processes.

Heterochrony and Sexual Dimorphism

Many species of animals exhibit sexual dimorphism. Thiscan take the form of differences in average maximum size

Fig. 7 Peramorphic evolutionof protoceratopsian dinosaurs.Reproduced with permissionfrom McNamara (1997)

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between males and females and/or differences in morpho-logical features. This size and morphological variance arisesfrom either variations in growth rates or differences in therelative times of onset of sexual maturity; in other words, itarises from heterochrony (see, for example, the work byDenoël et al. (2009) on European newts). A relative modestexample occurs in the Indian Ocean blue boxfish, Strophiur-ichthys robustus, where both male and female juvenileshave a diamond-shaped body and a body pattern dominatedby spots. During their development, males change theirbody shape, so that it becomes more oval in outline. Thisprobably reflects a change in their degree of maneuverabil-ity when swimming. Their body pattern also changes fromspots to a series of elongate wavy patterns. The females,however, retain the juvenile features of diamond-shapedbody and body pattern of spots (Fig. 9). Thus, the femalescan be regarded as paedomorphic, compared with the males(McNamara 1995b).

A more extreme case occurs in deep sea angler fish, suchas Photocorynus, where the male is very much smaller thanthe female, retains early juvenile morphological features,

and lives parasitically attached to the female’s head (McNamara1997, p. 116). Perhaps one of the most extreme examples ofsexual dimorphism is in eulimid gastropods. These animals liveparasitically within holothuroids (sea cucumbers). The malesare exceedingly reduced in size and complexity and themselveslive within the body of the female where they live attached to aspecial receptacle and grow to be little more than a testis(Fig. 10). Such extreme dimorphism, of a smaller, paedomor-phic male living within or upon a female, is not that uncommoninmarine invertebrates, examples having been documented in anumber of groups of mollusks and echinoderms. Many exam-ples of less extreme sexual dimorphism brought about byheterochrony have been described in primates, in particular inmacaques (German et al. 1994).

Many species of beetles develop very enlarged front legs,mandibles, horns, or other protruding structures on theirhead. These are the product of positive allometry and soare more well developed in larger individuals that havegrown for longer. Frequently, males grow for longer periodsthan females during development and end up possessingthese prominent structures while females do not (McNamara

Fig. 8 Paedomorphic evolutionof species of the oryctocephalidtrilobite Arthricocephalus fromthe Early Cambrian of GuizhouProvince, China. Numbers referto thoracic segments. Modifiedfrom McNamara et al. (2006)

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1995b). Sometimes, even within a single sex, this charactermay be dimorphic. Cook (1987) showed that one of thesexual dimorphic characters in the dung beetle Onthophagusferox are the horns, which occur on the males but not thefemales. Even here, there are two distinctive male morphs,

one with a small body size and lacking horns, the otherlarger and with horns. Such male dimorphism, arising fromallometric scaling of horn size, occurs in a number of otherbeetles and shows that such horns form due to differences ineither growth rates or timing of cessation of growth, inconjunction with strong positive allometry in the structure.A similar example occurs in the New Zealand tree wetaHemideina crassidens (Kelly and Adams 2010), two malemorphs differing in head weaponry, which is reduced infemales, the differences rising from variations to durationof growth during ontogeny.

How big a beetle grows and thus whether or not the maledevelops large structures are partly dependent on availabil-ity of food. Brown and Lockwood (1986) found that in theforked fungus beetle Bolitotherus cornutus, individuals thatas larvae feed on more nutritious fungi emerge as adults at alarger size and attain a larger adult size. Consequently, themales form relatively larger horns than individuals feedingon less nutritious fungi. Moreover, even the developmentalstate of the fungus can affect the beetle’s growth rates. Sobeetle larvae feeding on younger fungi grow faster andattain a larger body size than those feeding on older fungithat are less nutritious.

Heterochrony and the Evolution of Large Body Size

The pattern of evolutionary trends of increased body sizethat occurs very frequently in the fossil record is known asCope's rule (Hone and Benton 2005). It is probable thatperamorphosis is a prime factor in generating such increasesin body size, either by hypermorphosis or acceleration(McNamara 1997). Studies of lineages of Jurassic bivalves

Fig. 9 The adult female of theblue boxfish Stropiurichthysrobustus is paedomorphiccompared with the male,resembling the juvenile in bodyshape and body patterning.Reproduced with permissionfrom McNamara (1997)

Fig. 10 Extreme sexual dimorphism in the parasitic gastropod Thyo-nicola living within a holothuroid (sea cucumber). The male is ex-tremely reduced and is parasitic within the female, spending its entirelife in a special receptacle, fertilizing the female

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and ammonites (Hallam 1975) demonstrated that many showtrends to increased body size. Similar patterns occur inforaminifers, primates, and other mammals (McKinneyin McNamara 1990) and in pterosaurs (Hone and Benton2007).

The effect of peramorphosis in driving trends of in-creased body size is best shown by dinosaurs (McNamaraand Long 2012). The peramorphic trends of increases inbody size in sauropods, ceratopsians, theropods, and orni-thopods produced not only increases in body size, but alsoincreased complexity of many morphological features(Fig. 7). Recent research on bone microstructure has shownthat many juvenile dinosaurs experienced very rapid growthrates (Padian et al. 2001; Sander and Klein 2005), implyingthat acceleration was the process responsible for the attain-ment of the peramorphic features. However, studies of the-ropod growth patterns support the argument that theevolution of very large body sizes of many dinosaurs mayhave occurred by a combination of both acceleration andhypermorphosis.

In a study of tyrannosaurid theropods, growth rate data forfour genera, Albertosaurus,Gorgosaurus,Daspletosaurus, andTyrannosaurus, were compared (Erickson et al. 2004). Alber-tosaurus and Gorgosaurus are the smallest, Daspletosaurus alittle larger, and Tyrannosaurus appreciably the largest. Usingbone histology, it was calculated that the body size of Tyran-nosaurus was about 5.5 tons. It grew fastest for about the firstfour years of its life, when it was adding about two kilogramsper day. Growth slowed after that until full maturity wasreached when the dinosaur was about 18.5 years old.

The other three theropods were relatively smaller, reachingmaximum body sizes of about one ton in Gorgosaurus andAlbertosaurus, and about 1.5 tons in Daspletosaurus. Theirmaximum growth rates also persisted for up to about fouryears but were much less than in Tyrannosaurus rex, beingabout one-third to one-half kilogram per day. These generawould have also become mature at a younger age than T. rex,between about 14 and 16 years. So not only was T. rexgrowing much faster (acceleration) than other tyrannosaurids,but it also had a delayed offset of growth (hypermorphosis).When these four tyrannosaurids are compared with geologi-cally older theropods, such as Syntarsus, the earlier formsbecame mature at the much younger age of about four yearsand had a maximum growth rate of only nine kilograms peryear (Chinsamy 1990). It is significant that the evolution ofgigantism in other reptiles, notably crocodiles and lizards, wasattained only by hypermorphosis (Erickson et al. 2003).

Heterochrony and Developmental Trade-Offs

Most organisms are not just paedomorphic or peramorphicbut a mixture of traits that evolved by both peramorphic and

paedomorphic processes. Such a mixture is known as dis-sociated heterochrony. It has been suggested that there maybe a relationship between the peramorphic and paedomor-phic traits, such that the paedomorphic traits may be devel-opmental trade-offs for the peramorphic features(McNamara 1997). For instance, peramorphosis and sizeincrease are often associated with the development of somepaedomorphic traits. Evolutionary trends toward increasedbody size result in the organisms being required to input agreater amount of energy to attain the larger body and theaccompanying more complex morphological featurers thanin ancestral forms. This can be achieved by trade-offs, withselection pressure preferentially favoring some structures.

A classic example of a developmental trade-off is thedinosaur T. rex which as well having a huge body, possessedextremely reduced paedomorphic forelimbs and a hand withonly two digits. This paedomorphic forelimb of T. rex isvery unlikely to have had any adaptive significance but mayhave been a developmental trade-off for the evolution of itslarge body size, particularly the hind limbs and the head.The peramorphic development of a large body size in com-bination with increased complexity and size of the skull andhind limbs is offset by the paedomorphic reduction in theforelimbs and digits.

This phenomenon has also been recognized in hominidevolution, where it is known as the “expensive tissue hy-pothesis” (Aiello and Wheeler 1995). Here, while selectionhas favored larger body size and brain in humans by hyper-morphic extension of the growth period, the trade-off toevolve metabolically hungry brain tissue is the reductionof the size of the gut, the lower jaw, and teeth. Likewise, inlarge ratite birds such as the ostrich and emu, trends to alarge body size and very large hind limbs are offset by apaedomorphic reduction in the wings and a flightless habit.

Heterochrony and Evolutionary Novelties

Heterochrony has often been suggested as playing asignificant role in the evolution of major evolutionarynovelties (McKinney and McNamara 1991; Jablonski2000; McNamara and McKinney 2005). In the 1920s,Walter Garstang suggested that vertebrates evolved froma tunicate-like larva by paedomorphosis (Garstang 1928).Adult tunicates, or sea squirts, are jelly-like organismsthat attach to a hard substrate such as a rock. The larvae,though, have many of the attributes one would expectfrom a vertebrate: a notochord, gill slits, and a postanalpropulsive tail. Garstang suggested that attainment ofsexual maturity at a very early growth stage would have“frozen” the tunicate in its larval form, in which it couldreproduce.

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The reason that early maturation, or progenesis, has beenproposed as potentially the most important heterochronicprocess to produce evolutionary novelties (Gould 1977) isthat progenesis involves not just the pronounced morpho-logical disparity between ancestor and descendant due to themuch earlier offset of growth, but selection may also targetthe life history strategy of precocious maturation (see be-low) rather than morphology itself. However, other hetero-chronic processes, such as neoteny and hypermorphosis,may also play a significant role in macroevolution. A studyof the largest-ever terrestrial lizard, the Australian Pleisto-cene varanid Varanus (Megalania) prisca, has shown how itevolved by hypermorphosis (Erickson et al. 2003). Thisgiant reptilian carnivore, measuring about seven meters inlength and weighing more than half a ton, was more thantwice the length of any living varanid. It reached its enor-mous size by delaying its time of onset of maturity by threeto four years compared with other varanids.

Limb loss in snakes and whales also demonstrates theimportance of paedomorphosis in the evolution of morpho-logical novelties. Here again, rather than progenesis, theprocess is more likely to have been neoteny or postdisplace-ment, or perhaps a combination of the two. The apparentdominance of paedomorphosis in the evolution of majormorphological novelties is due, in part, to the greater degreeof morphological difference between very early embryonicand adult forms than between adult morphologies that havebeen accelerated or extended by hypermorphosis. Havingsaid that, however, it may be that peramorphic changes veryearly in development, such as an earlier onset of growth ofspecific morphological traits, might play as significant a rolein the formation of morphological novelties as paedomor-phic delays.

Sometimes, the evolution of a major new group of organ-isms can be attributed to dissociated heterochrony, with theevolution of critical paedomorphic and peramorphic traitscombining to produce a radically different organism. Aclassic example of this is the evolution of birds from dino-saurs. It is now known from the superbly preserved EarlyCretaceous dinosaurs of Liaoning in China that many smalldinosaurs possessed feathers. It is feasible that feathers werealso present not only on some small adult dinosaurs but alsoon juveniles of larger forms. If this was the case, then thesmall-bodied dinosaurs, such as the feathered Sinosaurop-teryx and Caudipteryx, can be interpreted as paedomorphicdinosaurs. Similarly, the retention of feathers in birds can beconsidered as being by paedomorphosis. Early birds thatevolved in the Late Jurassic to Early Cretaceous show otherpaedomorphic traits, such as reduction in some digits; asmall body size; retention of a number of unfused bones; agracile, elongate skull; large orbit; and a relatively largebrain case. However, a critical feature of early birds, suchas Archaeopteryx, is the possession of greatly enlarged

forelimbs that enabled the development of flight. Theseformed by peramorphic processes targeting these particularskeletal elements.

Heterochrony and Evolutionary Trends

Heterochrony is also important in the generation of evolu-tionary trends (McNamara 1982, 1990). This is because thelink between evolutionary trends and heterochrony is due tothe inherent directionality in evolutionary trends that alsooccurs in organisms’ development. For an evolutionarytrend to become established, selection of either more andmore paedomorphic or peramorphic traits must take placealong an environmental gradient. For instance, in the aquaticenvironment, this could be from deep to shallow water orfrom coarse- to fine-grained sediments. In the case of evo-lutionary trends generated by heterochrony in dinosaurssituated in the terrestrial environment, the agents of selec-tion are harder to quantify but may relate to “arms races”between predators and prey: as a prey species evolves alarger body size to combat the effect of predation from aparticular source, so selection will favor larger predators.

Any evolutionary trend that shows increasingly morepaedomorphic characters between ancestors to descendantsis called a paedomorphocline. If increasingly more peramor-phic descendants evolve, it is called a peramorphocline(McNamara 1982). The driving force behind such hetero-chronically driven trends is generally either competition orpredation pressure. When the trend forms by competition,the ancestral form will persist and force selection in a singledirection, away from the ancestral species. However, selec-tion brought on by predation pressure will produce anage-netic evolutionary trends, where ancestral species areprogressively replaced by the descendant forms and do notpersist. Examples of paedomorphoclines have been describedin Cenozoic brachiopods (McKinney and McNamara 1991),where the environmental gradient was from deep to shallowwater (Fig. 11); in trilobites (McNamara 1986a); and inammonoids (Dommergues 1990; Korn 1995; Gerber 2011).The best examples of peramorphoclines are in dinosaurs(McNamara and Long 2012).

Heterochrony and Life History Strategies

A close relationship exists between life history strategiesand heterochrony. Life history strategies include a numberof factors: size at birth; growth rate; age at maturation; bodysize at maturity; number, size, and sex of offspring; andlifespan. Many of these factors are determined by hetero-chrony. There have been numerous attempts to categorizelife history traits. These have met with limited success. The

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most well known is the “r–K continuum.” This describesboth environments and life history traits of the organismsthat inhabit these environments. Despite the r–K continuummodel being an oversimplification of life history strategies,it appears to offer some applicability at higher taxonomiclevels as well as containing many elements that fit withcurrent ideas on density-dependent regulation, resourceavailability, and environmental fluctuations (see Reznick etal. 2002 for a review of the controversy over the use of thetheory).

The “r-selected” end of the continuum consists of unpre-dictable, often ephemeral, environments. As a result, selec-tion pressure for organisms that inhabit such environmentsfavors those that mature rapidly, have short life spans, andhave small body size. These are all features of progenesis.Organisms that are r-selected typically produce large numb-ers of offspring. At the other end of the r–K continuum are“K-selected” organisms that occupy predictable, stable envi-ronments. These organisms typically have a relativelydelayed onset of reproduction, long life span, and conse-quent large body size, all features of hypermorphosis. Suchorganisms produce few, large offspring. In addition to beinggenerated by progenesis, r-selected characteristics may alsobe produced by acceleration (McKinney and McNamara1991). Moreover, many K-selected organisms appear to

Fig. 11 Over a period of about60 million years, theAustralasian brachiopodsTegulorhynchia and Notosariahave become increasinglypaedomorphic, forming anevolutionary trend in the formof a paedomorphocline. Theretention of morepaedomorphic features hasallowed successive species tocolonize increasingly shallowwater. The earliest formsinhabited deep, quiet water. Thespecies at the end of thepaedomorphocline inhabits theintertidal zone. Reproducedwith permission fromMcNamara (1997)

Fig. 12 The tiny progenetic kangarooMicrodipodops (top) has a bodylength of just 75 millimeters. The kangaroo rat Dipodomys (middle) isneotenic, with a body length of about 200 millimeters. The pocketgopher Orthogeomys (bottom) is a much larger hypermorphic rodentthat has a body length of about a third of a meter. Reproduced withpermission from McNamara (1997)

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show some traits that evolved by neoteny, as well as hyper-morphosis, so a reduction in growth rate rather than a delayin offset of maturity.

A good example of the role of heterochrony in the evo-lution of life history strategies occurs in the kangaroomouse, kangaroo rat, and pocket gopher that live in NorthAmerica (Fig. 12). Natural selection did not favor the lengthof their tail, color of their fur, nor size of their eyes, but thelife history strategy of the animals. It used to be argued thatthe evolution in these heteromyid rodents of morphologicalfeatures such as big hind feet, large eyes, and long tail wasan adaptation to a life in the desert, the large head counter-balancing the rodent as it hopped purposefully through thecool desert nights on large sand-paddle feet, hunting forfood using its big eyes and steering with the large rudder-like tail (McKinney and McNamara 1991).

However, research by Hafner and Hafner (1988) indi-cates that the small size and paedomorphic traits of the adultkangaroo mouse Microdipodops were due to selection forthe earlier maturation, producing a body length of just eightcentimeters. By contrast, the adult of the larger kangaroo ratDipodomys evolved by a reduction in rate of development.This genus has a longer life span, slower development,larger body size (20-centimeter length), longer gestationperiod, and smaller litters than the mouse. These are classicK-selected features. A third, related rodent, the pocket go-pher Orthogeomys, grows to about a third of a meter inlength. But instead of retardation of growth, there has beena hypermorphic extension of the growth period, producing arobust body form.

Extrinsic factors such as climate change can have a directimpact on life history traits in some types of plants byinducing heterochronic changes in descendants. Studies ofevolutionary change in the annual plant Brassica collectedin California before and after a five-year drought found thatthese drought conditions produced many changes in descen-dant life history traits that relate to changes to timing ofdevelopment (Franks and Weis 2008). These include achange to earlier flowering time, as well as longer durationof flowering. These descendants also had thinner stems andfewer leaf nodes at flowering time than ancestral forms,showing that the result of the drought was selection forplants that flowered at a smaller size and at an earlierontogenetic stage instead of selecting for plants that justdeveloped more rapidly.

Conclusions

For the last half-billion years, this Earth has been populatedby an astounding menagerie of organisms. Millions of spe-cies have come and gone—they have evolved; they havegone extinct. What has enabled this great panoply of forms

to evolve has been the inherent flexibility within the ge-nomic systems of organisms that has enabled subtle varia-tions to take place within populations in the rate of growthand variations in the timing of initiation and cessation ofgrowth. Controlled by critical heterochronic genes thatswitch growth on and off at different times and the genesthat control the growth hormones that dictate the extent towhich particular traits will develop, evolution of morpholo-gy and consequently, behavior, is very much determined byheterochrony.

But what of you and me? Is there any reason why we tooshouldn’t also have had our evolutionary histories moldedby the all-pervasive influence of heterochrony? No reason atall. As far back as the 1920s, it was being suggested thatmany of our morphological features appeared to be charac-teristic of juvenile apes: our flat faces, reduced body hair,relatively large brains housed in thin skull bones, absence ofbrow ridges, and reduced jaw with too many teeth. Thesefeatures would all seem to indicate that we are paedo-morphs. But has that been the sum total of our evolutionaryhistory, to be merely little more than overgrown juvenileapes? More recent studies, however, have shown that manyof our morphological features are, on the contrary, peramor-phic (see Minugh-Purvis and McNamara 2002 for a review).

The structure at the base of our skull that enables us towalk upright and face forward is nothing at all like anystructure in juvenile apes. Our overall large body size,relatively large legs, structure of our pelvis, enlarged crani-um and brain, and even our big feet are peramorphic fea-tures arising from the delay in onset of our maturity(hypermorphosis) compared with ancestral apes. In termsof our extended growth period, we are the late finishers ofthe ape world. Each part of our development–embryonic,infantile, and juvenile–has been relatively extended, com-pared with our ancestors. Such extension of succeedinggrowth stages during ontogeny is known as “sequentialhypermorphosis” (McNamara 2002) and has been shownto be critical in the evolution of our brain (Rice 2002). Thisprolonged period of pre-adult development has resulted notonly in our large body but especially our larger brain, whichhas allowed a longer period to be spent in the critical phaseof learning. We are a classic example of dissociated hetero-chrony, where some peramorphic features are developmen-tal trade-offs for other, paedomorphic, features: some partsof our anatomy are relatively retarded, compared with ourancestors, but others have developed beyond. Arguably, it isthese peramorphic features which are the ones that have ledto the success of our species on this planet, and all that thatentails.

Acknowledgments I am grateful to Kat Willmore for inviting me tocontribute to this volume. I also wish to thank Philipp Mitteroecker and

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an anonymous referee for their constructive comments on themanuscript.

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