Kenneth J. McNamara

A guide to the nomenclature of heterochrony

Since Haeckels Biogenetic Law (‘ontogeny recapitulates phylogeny’) fell into disrepute early in the twentieth century, there has been intermittent debate, particularly in recent years (de Beer, 1958; Gould, 1977; Alberch et al., 1979; Alberch, 1980; Bonner, 1982; McNamara, 1982a), on the nature of the relationship between an individuals development and phylogenetic history. Important questions under discussion include the following: If a strong causal relationship does exist, what is its nature? How does it work? What is its importance in evolution? How can it be recognized in the fossil record?

THE ROLE OF HETEROCHRONY IN THE EVOLUTION OF CAMBRIAN TRILOBITES

1. Renewed interest in the role of changes to developmental regulation in organisms has highlighted the importance of heterochrony in the evolution of the Metazoa.

Heterochrony, disparity, and macroevolution

Abstract The concept of heterochrony has long had a central place in evolutionary theory. During their long history, heterochrony and several associated concepts such as paedomorphosis and neoteny have often been contentious and they continue to be criticized. Despite these criticisms, we review many examples showing that heterochrony and its associated concepts are increasingly cited and used in many areas of evolutionary study. Furthermore, major strides are being made in our understanding of the underlying genetic and developmental mechanisms of heterochrony, and in the methods used to describe heterochronic changes. A general theme of this accumulating research is that some of the simplistic notions of heterochrony, such as terminal addition, simple rate genes, and “pure” heterochronic categories are invalid. However, this research also shows that a more sophisticated view of the hierarchical nature of heterochrony provides many useful insights and improves our understanding of how ontogenetic changes are translated into phylogenetic changes.

The Abundance of Heterochrony in the Fossil Record

Paleontologists have long recognized that the fossil record seems to indicate a strong relationship between ontogeny and phylogeny. Any attempt to assess the nature of this relationship, however, is plagued by many problems, not the least of which are the dual specters of Ernst Haeckel and Walter Garstang, which have long haunted paleontologists. In the late 19th century the relationship between ontogeny and phylogeny was explained almost entirely in terms of recapitulation. In the same year that Haeckel proposed his biogenetic law, Hyatt (1866), working on fossil cephalopods, formulated a very similar scheme to interpret the evolutionary history of ammonoids. Hyatt’s ideas were to have a profound effect on many of his contemporary paleontologist colleagues and some of his students. For example, Jackson (1890, 1912) interpreted many aspects of bivalve and echinoid evolution in terms of recapitulation, as did Beecher (1893, 1987) on brachiopods and trilobites.

Australian Tertiary schizasterid echinoids

The taxonomy of schizasterid spatangoids is discussed and the term is restricted to include only Schizaster-like echinoids. Within the genus Schizaster Agassiz the following morphological subgenera are recognized: Paraster Pomel, Dipneustes Arnaud and Ova Gray. Seven species are described from Palaeocene to Miocene rocks of Australia. New species are S. (Paraster) carinatus, S. (Paraster) tatei, S. (Schizaster) halli and S. (Dipneustes) fosteri. Schizaster and its various morphotypes are thought to have evolved from a Linthia-like root stock through progressive morphological changes in test shape, form of ambulacra and adoral test morphology. Such changes are interpreted as being adaptations which allowed the sea urchins to occupy various levels of substrate in different sediment types. Morphotypes appear to have evolved iteratively, perhaps due to variation in the onset of sexual maturity.

Heterochrony: the Evolution of Development

Heterochrony can be defined as change to the timing or rate of development relative to the ancestor. Because organisms generally change in shape as well as increase in size during their development, any variation to the duration of growth or to the rate of growth of different parts of the organism can cause morphological changes in the descendant form. Heterochrony takes the form of both increased and decreased degrees of development, known as “peramorphosis” and “paedomorphosis,” respectively. These are the morphological consequences of the operation of processes that change the duration of the period of an individual’s growth, either starting or stopping it earlier or later than in the ancestor, or by extending or contracting the period of growth. Heterochrony operates both intra- and interspecifically and is the source of much intraspecific variation. It is often also the cause of sexual dimorphism. Selection of a sequence of species with a specific heterochronic trait can produce evolutionary trends in the form of pera- or paedomorphoclines. Many different life history traits arise from the operation of heterochronic processes, and these may sometimes be the targets of selection rather than morphological features themselves. It has been suggested that some significant steps in evolution, such as the evolution of vertebrates, were engendered by heterochrony. Human evolution was fuelled by heterochrony, with some traits, such as a large brain, being peramorphic, whereas others, such as reduced jaw size, are paedomorphic.

Maastrichtian heteromorph ammonites from the Carnarvon Basin, Western Australia

A comprehensive taxonomic revision of heteromorph ammonites from the Miria Formation and the uppermost horizon, a nodule bed, of the Korojon Calcarenite is presented, with major rationalisation of earlier nomenclature and new data on the faunal sequence. Eubaculites is present throughout the succession as three biostratigraphically discrete species and Nostoceras, represented by two species, is restricted to the nodule bed. Remaining elements of the heteromorph fauna are known only from the upper part of the Miria Formation, associated with a diverse assemblage of planispiral ammonites and other molluscs. Preservation of ammonites has been strongly influenced by taphonomic factors such that the biostratigraphic pattern now apparent is largely unrelated to life assemblages. Ammonites from the upper Miria Formation are of late Maastrichtian age whereas those from the nodule bed are ascribed to the early Maastrichtian.

Coccoid-like microstructures in a 3.0 Ga chert from western Australia

Organic-walled spheroidal microstructures were discovered in a 3.0 Ga chert of the Cleaverville Formation, Western Australia. The spheroids are composed of solitary or paired cell-like units enclosed by an outer envelope, which are apparently similar to cyanobacterial microfossils. However, some of the spheroidal structures appear to be related to the arrangement of the surrounding minerals, and some to overprint diagenetic fabrics. Despite several cell-like characteristics, such as organic composition, paired nature, and multi-layered envelopes, at least some spheroids were formed during diagenesis, and thus are of diagenetic origin rather than being fossilized cells. It has been generally difficult to distinguish Archean microfossils from abiotic carbonaceous structures, however, and such microscopic observations could demonstrate the abiotic origin of some superficially fossil-like structures produced during diagenesis.

A new species of Banksia (Proteaceae) from the Eocene Merlinleigh Sandstone of the Kennedy Range, Western Australia

A new species of Banksia, B. archaeocarpa, from the Merlinleigh Sandstone, Kennedy Range, Western Australia is described on the basis of fossilised fruiting bodies (infructescences). An additional single, incomplete, sterile inflorescence of Banksia is also described, but not formally named. Marine fauna present in the sandstones along with the plant material has allowed dating of the Merlinleigh Sandstone as Middle or Late Eocene. The presence of Banksia remains in rocks of this age in Western Australia represents the earliest unequivocal occurrence of Banksia in Australia. The infructescences are superficially very similar to some present day Western Australian species of Banksia. This suggests that the genus was morphologically well established by the Late Eocene.

Changing Times, Changing Places: Heterochrony and Heterotopy

Beyond Heterochrony: The Evolution of Development. Edited by Miriam Zelditch. Wiley-Liss, New York. 2001. 371 pages. Cloth