A Guide to the Nomenclature of Heterochrony Author(S): Kenneth J

Paleontological Society

A Guide to the Nomenclature of Heterochrony Author(s): Kenneth J. McNamara Source: Journal of Paleontology, Vol. 60, No. 1 (Jan., 1986), pp. 4-13 Published by: Paleontological Society Stable URL: http://www.jstor.org/stable/1305091 Accessed: 16-07-2018 10:52 UTC

REFERENCES Linked references are available on JSTOR for this article: http://www.jstor.org/stable/1305091?seq=1&cid=pdf-reference#references_tab_contents You may need to log in to JSTOR to access the linked references.

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact [email protected].

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at http://about.jstor.org/terms

Paleontological Society is collaborating with JSTOR to digitize, preserve and extend access to Journal of Paleontology

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms JOURNAL OF PALEONTOLOGY, V. 60, NO. 1, P. 4-13, 4 FIGS., JANUARY 1986

A GUIDE TO THE NOMENCLATURE OF HETEROCHRONY

KENNETH J. McNAMARA Western Australian Museum, Francis Street, Perth. Western Australia 6000

SINCE Haeckel's Biogenetic Law ('ontogeny sil record must be examined in detail for rel- recapitulates phylogeny') fell into disrepute evant examples. early in the twentieth century, there has been During the latter part of the nineteenth cen- intermittent debate, particularly in recent tury the Biogenetic Law was invoked by a years (de Beer, 1958; Gould, 1977; Alberch number of workers to explain many aspects et al., 1979; Alberch, 1980; Bonner, 1982; of the fossil record. In particular, the evolu- McNamara, 1982a), on the nature of the re- tion of some ammonite lineages was ascribed lationship between an individual's develop- to the workings of this doctrine. The main ment and phylogenetic history. Important proponent of this in ammonites was Hyatt questions under discussion include the fol- (1889, 1893). Another fervent advocate of lowing: If a strong causal relationship does the Biogenetic Law was Beecher, who based exist, what is its nature? How does it work? his classification of the Trilobita on the belief What is its importance in evolution? How that the phylogeny of the Trilobita was en- can it be recognized in the fossil record? capsulated within the ontogeny of later tri- The phenomenon of changes through time lobites. During the twentieth century, instead in the appearance or rate of development of of being interpreted in a 'recapitulation' light, ancestral characters is known as heterochrony the pendulum swung the other way and many (sensu de Beer, 1930). It is clear, from the trilobites and ammonites were interpreted as lack of substantial reference to heterochrony having arisen by paedomorphosis (called in many modem textbooks on evolution, that 'proterogenesis' in ammonites), principally its impact on the development of evolution- by Schinderwolf (1929) for ammonites, and ary concepts has diminished markedly during Stubblefield (1936, 1959) and Hupe (1953a, the twentieth century. This stems not only 1953b) for trilobites. from the fact that Haeckel's Biogenetic Law However, recent work, by Gould (1977) in has generally been discredited, carrying the particular, has shown that neither one phe- whole concept of heterochrony as an impor- nomenon nor the other need necessarily be tant factor in evolution with it, but also be- prevalent. Gould (1977) has done much to cause of the great proliferation of terms that unravel the tangled heterochronic web woven have been introduced to describe various as- by generations of evolutionary biologists and pects of heterochrony. For example, a small to provide a sound basis on which to examine selection includes: peramorphosis, paedo- the role of heterochrony in evolution; and morphosis, paedogenesis, palingenesis, phyl- Alberch et al. (1979) have attempted to place embryogenesis, proterogenesis, progenesis the study of heterochronic processes on a and prothetely! more sound, quantitative footing. This plethora of terms has contributed to The aim of this guide is essentially three- both their frequent misuse and much con- fold: to describe concisely each of the het- fusion as to the nature of the relationship erochronic processes recognized by Alberch between ontogeny and phylogeny. Another et al. (1979); to illustrate how the actions of reason for the general lack of acceptance of these phenomena may be recognized in the the importance of heterochrony in evolution fossil record; and, in order to facilitate this is probably the paucity of detailed examples, recognition, to show the morphological and at the species level, described from the fossil size relationships between inferred ancestral record. If due consideration is to be given to and descendant forms. References are given the role of heterochrony in evolution, the fos- to detailed examples of each of the processes.

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms NOMENCLATURE OF HETEROCHRONY 5

This guide draws heavily on the (Gould, clarifica- 1966, 1977). If the relative size and tion of the heterochronic processes shape by of Gould a morphological feature remain con- (1977) and Alberch et al. (1979). stant It differs with growth of the whole organism, the from the work of Alberch et al. (1979) growth in that is said to be isometric. More com- it follows a less quantitative approach, monly, duringwith juvenile growth, in particular, the aim of providing a didactic guide body tosize het- and structural shape changes are erochronic terminology that may dissociated, be of par- such that the shape and size of ticular use to paleontologists. A key particular to the structures may alter substantially heterochronic processes is presented, during and ontogeny. each With pronounced allome- process is illustrated in simplified try diagram- during ontogeny, size and shape changes matic form (Figures 2 and 3), in ordercan be quiteto aid dramatic. Slight alterations to in the identification of morphotypes the degree pro- of allometry may have profound duced by heterochrony. effects in the descendant adult. Allometry may be positive or negative. WHAT IS HETEROCHRONY? When allometry is positive for a particular Heterochrony has been defined as the structure the structure increases in size rela- "changes in relative time of appearance and tive to the whole organism and may sub- rate of development of characters already stantially change its overall shape. It will thus present in ancestors" (Gould, 1977, p. 2, fol- be larger than if its growth had been isomet- lowing de Beer, 1930). Such changes in tim- ric. When allometry is negative the structure ing of development also occur between par- becomes smaller during growth of the organ- ent and offspring within a species as part of ism. An example of positive allometry is the general phenotypic variation (e.g., Cock, increase in trunk size during growth in hu- 1966; Travis, 1981; McNamara, 1982b). If mans, while relative reduction in head size the morphological characteristics of the phe- occurs by negative allometry (Medawar, notype derived by heterochrony are of adap- 1945). tive significance, there may be preferential Extension or contraction of the period dur- selection of the derived morphotype and a ing which a particular structure develops by new species may evolve. allometry can likewise produce a descendant Thus, between parent and offspring, or be- showing quite different structural features to tween successive species, the morphological its ancestor. The classic example of this is the change during an organism's ontogeny may extension of positive allometry of the antlers be relatively increased or decreased. It is im- in the Irish Elk Megaloceros (Gould, 1974). portant when considering an organism's Heterochrony is concerned with changing al- growth to recognize that it is composed of lometries: by the variation of growth rates or two basic elements: morphological (i.e., by the extension or contraction of the period shape) change and overall size change. The during which these growth rates operate. decoupling of these two elements and their If a descendant passes through fewer stages temporal changes relative to one another may ofontogenetic development than its ancestor, result in heterochrony when either or both the descendant adult form will have mor- are affected by changes in rate of develop- phological characteristics which occurred in ment. Variation in the timing of onset or ces- juveniles of the ancestor. This phenomenon sation of morphological development and size has been termed paedomorphosis (Garstang, change may also result in heterochrony. In 1928). Conversely, should a descendant pass some instances there may be no morpholog- through more ontogenetic stages of devel- ical change between ancestor and descendant, opment than its ancestor, the adult form will but there may be size differences: relative size have developed 'beyond' that of the ancestor. decrease is dwarfism and relative size in- This has been termed peramorphosis (Al- crease, giantism. These terms are self-ex- berch et al., 1979). Both paedomorphosis and planatory and will not be described further, peramorphosis express the morphological re- although they are included in the key. sult of processes affecting the timing of de- The relationship between size and shape velopmentof (Figure 1). They are not processes particular structures is known as allometry themselves, merely the end result of hetero-

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms 6 KENNETH J. McNAMARA

HETEROCHRONY _I

PAEDOMORPHOSIS PERAMORPHOSIS

I I

PROGENESIS NEOTENY POST-DISPLACEMENT HYPERMORPHOSIS HYPERMORPHOSI SACCELERATION ACCELERATION PRE-DISPLACEMENT PRE-DISPLACEMENT (precocious (reduced rate (delayed onset (delayed sexual (increased rate (earlier onset sexual of morphological of growth) maturation) of morphological of growth) maturation) development) development)

FIGURE 1-The hierarchy of heterochrony. chronic processes. Paedomorphs and pera- have been used widely in the literature as morphs may be the same size as their ances- heterochronic terms when, in fact, they are tors, or they may be larger or smaller, not involved in changes to the timing or rate depending on the heterochronic process which of appearance of features at all (Gould, 1977). has operated. These terms relate to the introduction of new In their classification of heterochrony, Al- features and, consequently, are not relevant berch et al. (1979) defined heterochronic pro- to this guide. Cenogenesis (syn. archallaxis) cesses, their morphological expression (i.e., sensu de Beer (1930) is the introduction of paedomorphosis and peramorphosis), and the new features during the juvenile or embry- resultant phylogenetic phenomena. They re- onic stages of development. Anaboly was a garded the phylogenetic expression of pera- term used by Severtzov (1927) to describe morphosis as 'recapitulation,' and of pae- the introduction of new features at the end domorphosis as 'reverse recapitulation.' I of the embryonic stage. prefer not to use these terms. Firstly, because 'recapitulation' immediately conjures up IDENTIFICATION OF HETEROCHRONY connotations of Haeckel's all pervasive Bio- IN THE FOSSIL RECORD genetic Law. Secondly, because I consider the The observation in the fossil record of het- term 'recapitulation' to be basically inappro- erochronic species can be made both dia- priate: peramorphic processes do more than chronously and synchronously. By observing recapitulate the ancestor's ontogeny. The im- the time ranges of diachronous species portant point is that the descendant's ontog- through a stratigraphic succession (assuming eny develops further-that is, it is more than that the stratigraphic ranges provide some just recapitulated. It follows that the term indication of the true temporal ranges of the introduced by Alberch et al. (1979) as a coun- species) heterochronic ancestor/descendant terpart to 'recapitulation,' 'reverse recapitu- relationships can be inferred and either pae- lation,' is similarly inappropriate, and there- domorphosis or peramorphosis can be iden- fore rejected. tified by comparing ontogenetic transfor- Processes that result in either paedomor- mations between successive species (e.g., phosis or peramorphosis are temporal phe- McNamara, 1982a, 1983a, 1984). Alterna- nomena that occur within species, at the level tively, it is possible to observe a number of of successive generations. Effects of these het- synchronous species, either in the fossil rec- erochronic processes may appear in the fossil ord or at the present day, and identify them record at the species level, following selection as heterochronic species (e.g., McNamara, for and genetic fixation of the heterochronic 1978, 1982b, 1983a). In order to ascertain morphotype. Either way, whether the changes which is the ancestral form and, consequent- are intra- or inter-specific, the processes and ly, whether the descendant is a paedomorph resultant morphologies are the same. Thus in or peramorph, out-group comparison must this paper paedomorphosis and peramor- be made with material from other time planes, phosis are also used in a phylogenetic sense. so as to identify the likely ancestral form. Certain terms, cenogenesis in particular, It is possible to identify a series of sequen-

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms NOMENCLATURE OF HETEROCHRONY 7

tial ancestor/descendant relationships fecting within morphological development are rec- a lineage. It has been suggested (McNamara, ognized. 1982a) that some evolutionary trends In order have to outline clearly these hetero- occurred as a result of the selection of suc- chronic processes, reference will be made to cessive heterochronic species through time, Figures 2 and 3. These figures attempt to il- resulting in directional speciation. Such lustrate diagrammatic ontogenies of ancestral trends, termed paedomorphoclines and pera- and descendant forms of an idealized organ- morphoclines (McNamara, 1982a), can oc- ism. The ancestral form is considered in each cur when new morphotypes, resulting from case to pass through four arbitrary morpho- heterochronic processes, are adaptively sig- logical stages A to D. In each of the paedo- nificant along an environmental gradient. morphic situations (Figure 2) the descendant Recent critics of the use of the fossil record attains only morphological stage C at cessa- for evolutionary studies (e.g., Nelson, 1978; tion of growth. However, Figure 2 illustrates Fink, 1982) have advocated the use of on- how the various paedomorphic processes af- togenetic character transformations to assess fect ontogenetic pathways and their relation- phylogenetic relationships. However, such ships to the ancestral ontogeny. Similarly, the adherents to the cladistic school are content ontogenies which have been affected by pera- to analyze the ontogenies of living organisms morphic processes (Figure 3), are compared and attempt to formulate phylogenies from with the ancestral ontogenetic pathway and an analysis of organisms only on a single time shown in each case to attain morphological plane. They do not appear to be prepared stage to E, but by different ontogenetic strate- analyze ontogenies of fossil species. Their gies.se- It must be stressed that the morpholog- lectivity of available data, ignoring infor- ical stages A to E may be either saltatory (as mation from other time planes, makes for in arthropod development) or gradual; but weak phylogenetic analysis. Incorporation the of same heterochronic processes operate. The information from the fossil record can only idealized organisms in Figures 2 and 3 have improve phylogenetic analysis. To ignore suchappendages that increase in size isometrical- a welter of information is, to say the least, ly, and a central pore that increases in size myopic. By analyzing variation in rates ofby positive allometry. ontogenetic character changes in successive species through the fossil record, likely ances- PAEDOMORPHOSIS tor/descendant relationships can be pro- (Syn. fetalization, proterogenesis, lipopal- posed. The aim of this guide is to facilitate ingenesis, superlarvation, reverse recapitu- such studies. lation.) Retention of ancestral juvenile characters in the descendant adult phase can be THE HETEROCHRONIC PROCESSES achieved in three ways: by reducing the rate Most morphological change during of anmorphological or- development through the ganism's ontogeny occurs during the juvenile juvenile phase of growth (neoteny), by pre- phase of growth, particularly during cociousearly ju- sexual maturation (progenesis), or by venile development. Cessation or severe delay inre- onset of morphological development duction in rate of morphological (post-displacement). development generally accompanies onset of Neoteny sexual (Kollman, 1885).--(Syn. brachy- maturity. Similarly, cessation of increasegenesis, inmetathetely, retardation.) Reduced size may also accompany maturity rate and of re-morphological development during the duced rate of morphological development. juvenile phase results in a morphologically However, in many organisms size increase,retarded adult. This is termed neoteny. If ma- generally to a specific maximum, which turity may occurs at the same age as in the ances- be related to the period of juvenile tor, growth, the neotenic adult will be of equal size continues during part of the adult tophase. the ancestralAs adult, though morphologi- noted above, any changes to rate of cally devel- retarded (Figure 4). If, as is often the opment, or to onset or cessation of case growth during neoteny, onset of sexual maturity can have profound effects on the descendantis delayed, a longer period will have been morphologies, particularly if the growthspent in is the juvenile phase of rapid size in- allometric. Six heterochronic processes crease. af- Consequently, the adult will be larger

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms 8 KENNETH J. McNAMARA

PROGENESIS than the ancestral adult, but have morpho- A B C logical characteristics of an ancestral juvenile stage. Thus, by comparison with an ancestral ontogeny A to D (Figure 2) at, for instance, the size at which the ancestor changes from morphological stage C to D, the neotenic form would be only at morphological stage B, on account of the reduced rate of morphological development. Neoteny may only affect some structures, or it may affect the whole organ- POST- DISPLACEMENT ism (termed 'dissociated' and 'global' re- A B C spectively by McKinney (1984). Examples of neoteny have been described from the fossil record in molluscs (Gould, 1969, 1970; Nevesskaya, 1967; Hallam, 1982), brachiopods (McNamara, 1983a), tri- Oo lobites (Ludvigsen, 1979; McNamara, 1981) and echinoids (McNamara, 1982b; Mc- Kinney, 1984). Progenesis (Giard, 1887).--(Syn. paedo- NEOTENY genesis, prothetely.) If onset of maturity occurs at an earlier stage of development in the A B C 1 descendant, morphological and size changes will be stopped or severely retarded preco- ciously. The resultant progenetic adult will thus retain ancestral juvenile characters, but, unlike the neotenic situation, it will be smaller than the ancestral adult as a shorter period will have been spent in the phase of rapid size increase (Figure 4). Progenetic forms also differ from neotenic ANCESTOR forms in their early ontogenetic strategy. The juvenile rate of development prior to matu- A B C D rity is the same in progenetic forms as in their ancestors (Figure 2). During the same, early ontogenetic period, the rate of development of the neotenic forms is reduced. Progenesis is global, affecting the whole organism. How- (Dg ever, certain characters will have a more overtly juvenile aspect than others. In many organisms a certain degree of morphological development occurs after the onset of ma- FIGURE 2-Relationship of the three paedo- turity. Thus a progenetic species differs to morphic processes to the ancestral form. In neoteny, rate of development is reduced. Here, on-some degree from the ancestral juvenile form. set of maturity is also retarded, resulting in the In arthropods progenesis can occur in two descendant adult reaching a larger maximum ways (McNamara, 1983b): by the 'normal' size. In post-displacement, the onset of growth premature maturation (terminal progenesis), of spots and spines is delayed. Subsequent rate or by a shortening of the period spent in each and cessation of growth are the same in the de-molt stage (sequential progenesis). scendant as in the ancestor, but the delayed onset of development means that ancestral juvenile characters occur in the descendant adult. In progenesis, precocious sexual maturation results ontogenetic development is the same in descen- in an adult smaller than in the ancestor. Early dant as in ancestor.

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms NOMENCLATURE OF HETEROCHRONY 9

HYPERMORPHOSIS Examples of progenesis have been described from the fossil record in bivalves A B C D E (Stanley, 1972), trilobites (McNamara, 1978, 1981, 1983b), ammonites (Wright and Ken- nedy, 1980), brachiopods (McNamara, G) 1983a), echinoids (Philip, 1963) and edrioas- teroids (Sprinkle and Bell, 1978). Post-displacement (Alberch et al. 1979).- Unlike progenesis and neoteny, post-displacement does not arise by changes to rate of development or timing of cessation of de- PRE-DISPLACEMENT velopment. Indeed, paedomorphosis by post- displacement can occur even if the rate of B C D E development and cessation of growth are the same as in the ancestor. Post-displacement occurs by a change in timing of onset of development of certain structures. By comparison with the ancestor, one or more organs or structures will commence development at a later stage with respect to other parts of the organism. In other words, commencement of development of the organ at ACCELERATION stage A occurs when the ancestral organ was AB C D E at state B, relative to the whole organism (Fig- ure 2). If subsequent rate of development and cessation of growth are the same as in the ancestor, the particular organ or structure that commenced development later will be relatively retarded with respect to the ancestor, having reached only stage C at cessation of growth, whereas the comparable organ or structure in the ancestor would have reached ANCESTOR morphological stage D. The adult morphology of the descendant will therefore resemble A B C D a juvenile stage of the ancestor. The shorter period of growth will result in the structure being smaller than in the ancestor. Post-displacement only affects certain organs or structures, not the whole organism. Thus, whereas the progenetic adult similarly is smaller and retarded with respect to the ancestor, post-displacement results in only a certain number of organs or structures, not FIGURE 3-Relationship of the three peramorphic processes to the ancestral the whole organism, form. being retarded In acceleration,and increased rate of development smaller. It is feasible for post-displacement results in ancestral adult characters and occurringneoteny to operate concurrently, in the if bothdescendant juvenile. In this example onset of maturity is also accelerated, resulting in the descendant adult being smaller than meansthe that ancestral the descendant adult morphologyadult. In pre- displacement, onset ofhas developed growth beyond that of of the spots ancestor. In and spines is initiated at an earlier hypermorphosis, stage onset of sexualof maturity ontogeny is de- than in the ancestor. Subsequent layed, with the consequence rate that theand descendant cessation of growth are the same adult is larger in and descendant morphologically more de- and ancestor. However, the earlier veloped than the onsetancestral adult. of development

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms 10 KENNETH J. McNAMARA

small increase in rate of development initi- ACCELERATION ated at an early stage of development can result in quite profound morphological differences between descendant and ancestor, if / X HYPERMOF growth is allometric. In such cases, the descendant will pass through the adult stage of the ancestor during its ontogeny. Maturity may occur when the descendant is the same size as the ancestor; if, however, onset of maturity is also accelerated, the descendant adult may be smaller than the ancestral adult, but be morphologically more advanced (Figure 4). Thus, for example, it can be seen in Figure 3 that, by comparison with the ancestral ontogeny at commencement of stage D, the accelerated organism would, at the same size, be approaching morphological stage E. Ac- celeration may affect the whole organism, or only certain organs or stuctures. Examples have been described in ammonites (Newell, 1949), graptolites (Elles, 1922, SIZE- - 1923; Urbanek, 1973; Gould, 1977), echinoids (McNamara, 1984) and titanotheres FIGURE 4-Diagrammatic (McKinney plotand Schoch, of 1985). morphological development against size to illustrate the effect of acceleration and hypermorphosis Hypermorphosis (de Beer, 1930).--An on ex- the ancestral growth curve tension to of the produce juvenile growth period,peramorphic caused descendants, and of by neoteny a delay in onset of and maturation, progenesis will result to produce paedomorphic in peramorphosis. descendants. This process is the opposite of progenesis. Early juvenile development will commence at the same time and onset of growth is proceed delayed at the same and rate as inrate the ancestor of development is retarded. (Figure 3). Extension of late ontogenetic de- Examples of post-displacement velopment may result in morphological have char- been described in zebras (Bard, 1977) and sala- acteristics quite different from the ancestral manders (Wake, 1966). The reduction in adult. The longer period spent in the juvenile number of lenses in eyes in some lineages of phase of growth will result in the attainment phacopid trilobites (Richter, 1933) may also of a larger maximum size. The descendant represent post-displacement. adult will therefore be larger than the ancestral adult (Figure 4). Thus, in Figure 3, in- PERAMORPHOSIS stead of becoming mature at the end of mor- (Syn. adultation, recapitulation, palingene-phological stage D, the hypermorphic form sis.) The occurrence of the ancestral will continue adult developing into morphological morphology in a descendant juvenile stage stage E; maturity of will thus be attained at a development can be achieved in three larger ways: size than in the ancestor. Hypermor- by an increase in the rate of morphological phosis affects the whole organism. development (acceleration), by delay A of classic onset example ofhypermorphosis is the of sexual maturity (hypermorphosis), evolution or ofby the Irish Elk, Megaloceros earlier initiation of morphological (Gould, develop- 1974). Hypermorphosis has also been ment (pre-displacement). described in echinoids (McNamara and Phil- Acceleration (Cope, 1887).-(Syn. tachy- ip, 1980, 1984; McKinney, 1984). genesis.) As its name implies, this pera- Pre-displacement (Alberch et al., 1979).- morphic process consists of an increase in the As with the operation of pure post-displace- rate of morphological development during ment, rate of development and cessation of ontogeny. It is the opposite of neoteny. Agrowth may be the same as in the ancestor.

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms NOMENCLATURE OF HETEROCHRONY 11

However, initiation of development oflayed; one subsequent rate of development or a number of organs or structures atsame a rel-as ancestor Post-displacement atively earlier stage of development Time of ofthe onset of morphological development same as ancestor 4 whole organism, with respect to the ancestor, 4. Rate of juvenile development retarded; allows a longer period for their growth adult and as large as, or larger than, ancestral development. Thus, by comparison with adult the Neoteny same structure in the ancestral form Juvenile (Figure development same as ancestor ini- 3) the peramorphic form will be at stagetially; B sexual maturity occurs at earlier when the same structure in the ancestral stage ju- of development; adult smaller than venile was commencing growth. If cessation ancestral adult Progenesis 5. Morphological development of particular of growth and rate of morphological organs/structures devel- initiated earlier in or- opment are the same as in the ancestor, ganism's the ontogeny Pre-displacement peramorphic structure which initiated Time growth of onset of morphological develop- earlier will be morphologically more ment ad- same as ancestor 6 vanced and larger than the equivalent 6. Juvenile struc- rate of development accelerated; ture in the ancestral adult. adult no larger, often smaller, than ancestral adult Acceleration Alberch et al. (1979) believed it is possible Juvenile development same as ancestor; for all three peramorphic processes, acceler- onset of sexual maturity delayed; adult ation, hypermorphosis and pre-displace- larger than ancestral adult ment, to be operating concurrently in a single Hypermorphosis species. They believed that the peramor- 7. Descendant adult smaller than ancestral phosis in Palaeozoic ammonoids described adult Dwarfism Descendant adult larger than ancestral adult by Newell (1949), can be explained by the Giantism joint effects of the three different processes. Evolution of species within the rugose coral ACKNOWLEDGMENTS Amplexizaphrentis, as described by Caruth- A. Baynes, S. J. Gould, M. L. McKinney ers (1910), may have occurred by progressive and W. J. Kennedy kindly read the manu- pre-displacement along a peramorphocline script and offered suggestions for its improve- (sensu McNamara, 1982a). McKinney(1984) ment. has described pre-displacement, hypermorphosis and neoteny all occurring concurrently in an Eocene echinoid, illustrating how dif- REFERENCES ferent morphological features may be simul- ALBERCH, P. 1980. Ontogenesis and morpholog- taneously affected by different heterochronic ical diversification. American Zoologist, 20:653- processes. 667. , S. J. GOULD, G. F. OSTER AND D. B. WAKE. 1979. Size and shape in ontogeny and phylog- KEY TO HETEROCHRONIC PROCESSES eny. Paleobiology, 5:296-317. BARD, J. B. L. 1977. A unity underlying the dif- Diagnostic characters of each process ferent relate zebra striping patterns. Journal of Zool- to change manifest in the inferred descendant ogy, 183:527-539. with respect to the ancestor's morphology, BONNER, J. T. (ed.). 1982. Evolution and Devel- either of some morphological structure(s) opment. or Springer-Verlag, Berlin, 356 p. the whole organism. CARUTHERS, R. G. 1910. On the evolution of Zaphrentis delanoui in Lower Carboniferous 1. Descendant adult morphology differs fromtimes. Quarterly Journal of the Geological So- ancestral adult; size same or different ciety ..... of2 London, 66:523-538. Descendant adult morphology same asCOCK, an- A. G. 1966. Genetical aspects of metrical cestral adult; size different 7 growth and form in animals. Quarterly Review 2. Descendant adult morphology resembles of Biology, 41:131-190. juvenile ancestor (paedomorphosis) COPE, ...... E. D. 1887. 3 The Origin of the Fittest. Mac- Ancestral adult morphology present millan, in ju- New York, 467 p. venile phase of descendant; descendant DE BEER, G. R. 1930. Embryology and Evolu- morphology then develops 'beyond' tion. that Clarendon, Oxford, 116 p. of ancestor (peramorphosis) 3 .1958. Embryos and Ancestors. Clarendon, 3. Time of onset of morphological develop- Oxford, 197 p. ment of particular organs/structures ELLES, de- G. L. 1922. The graptolite fauna of the

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms 12 KENNETH J. McNAMARA

British Isles. Proceedings of the Geologists' phological As- change as a by-product of size selec- sociation, 33:168-200. tion. Paleobiology, 10:407-419. . 1923. Evolutionalpalaeontologyin relation AND R. M. SCHOCH. 1985. Titanothere al- to the Lower Palaeozoic rocks. Report of the lometry, heterochrony, and biomechanics: re- British Association for the Advancement of Sci- vising an evolutionary classic. Evolution, 39: ence, 91:83-107. 1352-1363. FINK, W. L. 1982. The conceptual relationship MCNAMARA, K. J. 1978. Paedomorphosis in between ontogeny and phylogeny. Paleobiology, Scottish olenellid trilobites (early Cambrian). 8:254-264. Palaeontology, 21:635-655. GARSTANG, M. 1928. The morphology of the 1981. The role of paedomorphosis in the Tunicata, and its bearing on the phylogeny evolution of of Cambrian trilobites. Open-File Re- the Chordata. Quarterly Journal of Microscop- port of the U.S. Geological Survey, 81-743:126- ical Science, 72:51-187. 129. GIARD, D. 1887. La castration parasitaire et son . 1982a. Heterochrony and phylogenetic influence sur les caracteres exterieurs du sexe trends. Paleobiology, 8:130-142. male ches les crustaces decapodes. Bulletin 1982b. Taxonomy and evolution of living scientifique du departement du Nord, 18:1-28. species of Breynia (Echinoidea: Spatangoida) GOULD, S. J. 1966. Allometry and size in on- from Australia. Records of the Western Austra- togeny and phylogeny. Biological Reviews, 41: lian Museum, 10:167-197. 587-640. 1983a. The earliest Tegulorhynchia .1969. An evolutionary microcosm: Pleis- (Brachiopoda: Rhynchonellida) and its evolu- tocene and recent history of the land snail tionary P. significance. Journal of Paleontology, 57: (Poecilozonites) in Bermuda. Bulletin of the 461-473.Mu- seum of Comparative Zoology at Harvard Col- 1983b. Progenesis in trilobites, p. 59-68. lege, 138:407-532. In D. E. G. Briggs and P. D. Lane (eds.), Tri- .1970. Land snail communities and Pleis- lobites and Other Arthropods: Papers in Hon- tocene climates in Bermuda: a multivariate our of H. B. Whittington, F.R.S. Special Papers analysis of microgastropod diversity. Proceed- in Palaeontology, 31:59-68. ings of the North American Paleontological 1984. Taxonomy and evolution of the Cai- Convention, part E, 486-521. nozoic spatangoid echinoid Protenaster. Pa- 1974. The evolutionary significance of'bi- laeontology, 28:311-330. zarre' structures: antler size and skull size in the AND G. M. PHILIP. 1980. Australian Ter- 'Irish Elk', Megaloceros gigantans. Evolution, tiary schizasterid echinoids. Alcheringa, 4:47- 28:191-220. 65. 1977. Ontogeny and Phylogeny. Belknap, - AND . 1984. A revision of the spatan- Cambridge, 501 p. goid echinoid Pericosmus from the Tertiary of HALLAM, A. 1982. Patterns of speciation in Australia. Ju- Records of the Western Australian rassic Gryphaea. Paleobiology, 8:354-366. Museum, 11:319-356. HUPt, P. 1953a. Contribution a l'etude du Cam- MEDAWAR, P. B. 1945. Size, shape and age, p. brien Inferieur et du Precambrian III de l'Anti- 157-187. In W. E. LeGros Clark and P. B. Med- Atlas Morocain. Notes et Memoires du Service awar (eds.), Essays on Growth and Form. Clar- des Mines et de la Carte geologique du Maroc, endon Press, Oxford. 103:41-402. NEVESSAKAYA, L. A. 1967. Problems of species . 1953b. Classification des trilobites. An- differentiation in light of paleontological data. nales de Paleontologie, 39:1-110. Paleontological Journal, 4:1-17. HYATT, A. 1889. Genesis of the Arietidae. Bul- NELSON, G. J. 1978. Ontogeny, phylogeny, pa- letin of the Museum of Comparative Zoology leontology, and the biogenetic law. Systematic at Harvard College, 16:1-238. Zoology, 27:324-345. 1893. Phylogeny of an acquired charac- NEWELL, N. D. 1949. Phyletic size increase, an teristic. Proceedings of the American Philo- important trend illustrated by fossil inverte- sophical Society, 32:349-647. brates. Evolution, 3:103-124. KOLLMAN, J. 1885. Das Ueberwintern von eu- PHILIP, G. M. 1963. Two Australian Tertiary ropiiischen Frosch- und Tritonlarven und die neolampadids and the classification of cassid- Umwandlung des mexikanischen Axolotl. Ver- uloid echinoids. Palaeontology, 6:718-726. handlungen der Naturforschenden Gesellschaft RICHTER, R. 1933. Crustacea, p. 840-863. In in Basel, 7:387-398. Handworterbuch der Naturwissenschaften. Jena. LUDVIGSEN, R. 1979. The Ordovician trilobite SCHINDERWOLF, O. H. 1929. Ontogenie und phy- Pseudogygites Kobayashi in eastern and Arctic logenie. Paliiontologische.Zeitschrift, 11:54-67. North America. Life Science Contributions of SEVERTZOV, A. N. 1926. Uber die Beziehungen the Royal Ontario Museum, 120:1-41. zwischen der Ontogenese und der Phylogenese McKINNEY, M. L. 1984. Allometry and heter- der Tiere. Jenaische Zeitschrift fur Naturwis- ochrony in an Eocene echinoid lineage: mor- senschaft, 56:51-180.

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms NOMENCLA TURE OF HETEROCHRONY 13

SPRINKLE, J. AND B. M. BELL. 1978. Paedomor- Boardman, A. H. Cheetham and W. A. Oliver phosis in edrioasteroid echinoderms. Paleo- (eds.), Animal Colonies, Dowden, Hutchinson biology, 4:82-88. & Ross, Stroudsburg. STANLEY, S. M. 1972. Functional morphology WAKE, D. B. 1966. Comparative osteology and and evolution of byssally attached bivalve mol- evolution of the lungless salamanders, family lusks. Journal of Paleontology, 46:165-212. Plethodontidae. Memoirs, Southern California STUBBLEFIELD, C. J. 1936. Cephalic sutures and Academy of Sciences, 4:1-111. their bearing on current classifications of trilo- WRIGHT, C. W. AND W. J. KENNEDY. 1980. Or- bites. Biological Reviews, 11:407-440. igin, evolution and systematics of the dwarf .1959. Evolution in trilobites. Quarterly acanthoceratid Protancanthoceras Spath, 1923. Journal of the Geological Society of London, (Cretaceous Ammonoidea). Bulletin of the Brit- 115:145-162. ish Museum (Natural History) (Geology), 34: TRAVIS, J. 1981. Control of larval growth vari-65-107. ation in a population of Pseudacris triseriata MANUSCRIPT RECEIVED 10 MARCH 1983 (Anura: Hylidae). Evolution, 35:423-432. REVISED MANUSCRIPT RECEIVED 8 FEBRUARY 1984 URBANEK, A. 1973. Organization and evolution of graptolite colonies, p. 441-514. In R. S.

PALEONTOLOGICAL SOCIETY CANDIDATES FOR OFFICE, 1986 ANNUAL BALLOT

At its meeting in Orlando, Florida, on October 30, 1985, Council of The Paleontological Society selected the following candidates for Society offices from nominees proposed by the Nominating Committee: For: President-Elect (1986-87) N. Gary Lane, Bloomington, Indiana Councilor (1986-88) Roger J. Cuffey, University Park, Pennsylvania Program Coordinator (1986-89) Jennifer A. Kitchell, Ann Arbor, Michigan Paleobiology Editors (1986-89) Richard Cowen and Philip W. Signor, Davis, Cali- fornia This slate will be submitted to the Membership on the Annual Ballot in August 1986. Additional nominations made in accordance with provisions of Section 3, Chapter 2 of the By-Laws will be accepted by the Secretary until July 1, 1986, and will be included as special tickets with the regular ticket announced above. John Pojeta, Jr. Secretary

This content downloaded from 131.111.64.116 on Mon, 16 Jul 2018 10:52:49 UTC All use subject to http://about.jstor.org/terms