“It's not all heterochrony.” Raff (1996)

“Heterochrony … explains everything.” McNamara (1997)

Few evolutionary topics have generated more confusion and controversy than heterochrony. Commonly defined as “evolution via change in rate or timing of development,” heterchrony has historically become associated with genocidal ideologies, simple-minded theories of evolution, and a bloated, baroque jargon describing patterns produced by largely unknown mechanisms. With a track record like that, perhaps the most surprising aspect of heterochrony is its continued, even rapid, growth as an area of productive scientific inquiry. For example, the number of papers devoted to heterochronic topics continues to increase in many evolutionary journals and books (reviews in Reilly et al. 1997; Klingenberg 1998), including those devoted to human development (Bogin 1997) and evolution (Vrba 1998; McKinney 1998; Parker and McKinney 1999).

Insects are the most diverse macroorganismic group to ever inhabit the planet, constituting a major share of the animal biomass in terrestrial and freshwater ecosystems. Since their first appearance in the fossil record some 400 million years ago, they have expanded ecologically into almost every niche except the ocean below the photic zone. When fossilized, their chitinous exoskeletons typically are well preserved, as evidenced by a respectable fossil record. They are found notably in lacustrine shales and amber but also occur in siderite nodules, lithographic limestone, sinter deposits, asphalt, and various glacial deposits. Insect fossils are major subjects in phylogenetic studies but are used to a lesser extent in understanding past ecological associations and reconstruction of ancient environments.

We have known since Trueman's classic work of 1922 that the Lower Jurassic Gryphaea of Britain exhibit phyletic size increase and heterochronic change in shape. Since Hallam's revisionary work in the 1960s, we have recognized that pronounced and generalized juvenilization of form accompanied this increasing size. This extensive literature provides invertebrate paleontology's most famous example of a biometrically documented, continuous anagenetic trend within a discrete lineage. But Gryphaea has also provoked great frustration because a key datum, required for a full solution, had been theoretically recognized but practically unavailable. We could identify the evolution of shape as paedomorphic, but could not specify the mode of heterochrony for this paedomorphic result because we could not standardize samples by common age or developmental stage.

In this paper, we provide sclerochronological data on sizes and shapes at specified ages marked by annual growth bands in two Jurassic sequences of Gryphaea: the classic Lower Jurassic series showing phyletic size increase with paedomorphosis, and an independent Middle–Upper Jurassic series illustrating neither size increase nor heterochrony. We prove that size increase in the classic series occurs entirely by faster growth (larger descendant sizes at the same ages as ancestors), and not by extended age (for descendants lived no longer than ancestors). The well-marked paedomorphosis of form probably arose as a correlated consequence of growing larger by extending and maintaining rapid juvenile growth rates—thus marking the heterochronic mode as a case of neoteny. The independent upper sequence, acting as a different replicate in a natural experiment, shows neither size increase nor heterochrony but does exhibit (in contrast with the classic sequence) evolution toward greater longevity.

Hallam's flow tank experiments indicated a strong adaptive advantage in shell stability for both larger size and paedomorphic form. Neotenous development provides an evolutionary pathway to the simultaneous acquisition of both favored traits—thus showing that “constraints” due to “correlations of growth” (Darwin's own phrase for the phenomenon) may be positive in promoting joint evolutionary advantages, and not only neutral (in carrying spandrels along with primary adaptations), or negative (by imposing inadaptive “baggage” upon trends in form through developmental correlation with selected traits).

Statistical analyses of occurrence data derived from new collections through scattered Caribbean sections indicate that increased speciation preceded a pulse of extinction during regional turnover of the Caribbean reef coral fauna in Plio-Pleistocene time. The data are based on samples that were newly collected and identified to species using standardized procedures. Age-dates were assigned using high-resolution chronostratigraphic methods. The results show that coral species with a wide range of ecological traits originated and were added to the species pool as much as 1–2 million years before extinction peaked at the end of the turnover interval. Local assemblages consisted of a mix of extinct and living species, which varied in composition but not in richness. Extinction was selective and resulted in a faunal shift to the large, fast-growing species that dominate Caribbean reefs today. The unusual relationship between origination and extinction may have been caused by changes in oceanic circulation associated with emergence of the Central American Isthmus, followed by the onset of Northern Hemisphere glaciation. The pattern of origination preceding extinction may have been responsible for the stability of reef ecosystems during the intense climatic fluctuations of the late Pleistocene, and for the composition and structure of modern Caribbean reef ecosystems.

Lipids found associated with skeletons represent an important avenue of study in molecular paleontology, because the chemical nature of these compounds means they are often biogenically specific and can survive in the geologic record over millions of years. Though it is clear that these skeletal compounds originate from the mineralizing organism, our understanding of the distributions and nutritional sources of lipids among invertebrates is still limited, requiring that baseline studies of modern taxa be completed to evaluate the potential of skeletal lipids in paleoecological studies.

In this study, skeletal lipids from nine modern invertebrate taxa (five mollusks, a brachiopod, an echinoid, a coral, and a barnacle) were extracted and analyzed. Though the major classes of lipids found in the skeletons are remarkably consistent, the sterol profiles from these organisms contain both dietary and environmental information. The skeletons of filter feeders generally have two to three times the variety of sterols as compared with carnivores and grazers. In addition, specific steroidal contributions from several plant and algal groups (including dinosterol, 22-dehydrocholesterol, and β- and γ-sitosterol) can be identified. The limited nature and distribution of sterols in the carnivore skeleton implies that both sterol-recycling and some degree of molecular selectivity may be occurring in this taxon. Taxa living in nearshore shallow marine habitats have significant sterol contributions from higher plants, while deepwater organisms have relatively little. Since the geologically stable form of sterols often retains the three-dimensional structure necessary to recognize the biological precursor, these compounds may be used for determining the ecology of fossil invertebrates.

A number of natural events can cause ozone depletion, including asteroid and comet impacts, large-scale volcanism involving the stratospheric injection of chlorine, and close cosmic events such as supernovae. These events have previously been postulated to have been sole or contributory causes of mass extinctions. Following such events, UV-B radiation would have been elevated at the surface of the earth. The possibilities for detecting elevated UV-B as a kill mechanism in the fossil record are discussed. In the case of impact events and large-scale volcanism, the taxa affected by increases in UV-B radiation are likely to be similar to those affected by cooling and by the initial drop in irradiance caused by stratospheric dust injection. Thus UV-B may synergistically exacerbate the effects of these other environmental changes and contribute to stress in the biosphere, although UV-B alone is unlikely to cause a mass extinction. By the same token, however, this similarity in affected taxa is likely to make delineating the involvement of UV-B radiation in the fossil record more difficult. Cosmic events such as supernovae may produce smaller extinction events, but ones that are “cleaner” UV catastrophes without the involvement of other environmental changes.

One of the major obstacles in dealing with any form of data derived from fossils is the effects of time-averaging, which are the result of mixing the remains of organisms that did not live contemporaneously. Although this process results in loss of temporal resolution, it also serves to filter out short-term variations. Temporal resolution of a collection depends not only on the range of fossil ages, but also on their frequency distribution. Previous studies of marine molluscs indicate that most shells in an accumulation are relatively young. Such a distribution of shell ages can be fit by an exponential curve (assuming both a constant probability of shell loss and a constant rate of shell addition), which implies that 90% of the shells were added during the last 50% of the time interval represented by the collection. That is to say, differences between two collections can be discerned even if they overlap 50% in time, because the proportion of shells with shared ages is only 10%. Applying the exponential model to previously published data suggests that long-term rates of destruction are controlled by how frequently shells from the taphonomically active zone are re-exposed to rapid destruction. To take advantage of the “noise-filtering” property of time-averaging, samples need to be large enough to catch the full range of environmental variation recorded by an accumulation. A simple probability formula indicates that samples of easily achievable size can give satisfactory time-averaged results depending on the level of confidence and sampling density defined by the researcher.

Variance and taxonomic selectivity were studied as functions of time across the Phanerozoic for duration of genera and families in the fossil record and for habitat of fossil families. The variance of duration increases temporarily before mass extinctions but otherwise decreases across the Phanerozoic, and the variance of habitat increases to an asymptote. For both duration and habitat, the percentage of variance explained by differences among orders and classes shows no temporal trend, whereas the percentage of variance explained by differences among phyla decreases across the Phanerozoic. The latter decrease depends upon the time elapsed since the origination of classes within phyla in the early Paleozoic; a similar decrease appears in differences among classes if the analysis is restricted to orders that originate before the Silurian. The observed patterns can be described by bounded random walks that include some infrequent but large steps.

Two major ichnotypes of sauropod trackways have been described: “narrow-gauge,” in which both manus and pes prints approach or intersect the trackway midline, and “wide-gauge,” in which these prints are well apart from the midline. This gauge disparity could be the result of differences in behavior, body size, or morphology between the respective trackmakers. However, the biomechanics of locomotion in large terrestrial vertebrates suggest that sauropods were probably restricted in locomotor behavior, and the lack of systematic size differences between footprint gauges argues against body-size-related influences. We argue that skeletal morphology is responsible for gauge differences and integrate data from locomotor biomechanics and systematics with the track record to predict the hindlimb morphology of wide-gauge trackmakers. Broader foot stances in large, graviportal animals entail predictable mechanical consequences and hindlimb modifications. These could include outwardly angled femora, offset knee condyles, and a more eccentric femoral midshaft cross-section. A survey of sauropod hindlimb morphology reveals that these features are synapomorphies of titanosaurs, suggesting that they were the makers of wide-gauge trackways. The temporal and geographic distribution of titanosaurs is consistent with this hypothesis because wide-gauge trackways predominate during the Cretaceous and are found worldwide. Additional appendicular synapomorphies of titanosaurs are interpreted in light of identifying these animals as wide-gauge trackmakers. We suggest that titanosaurs may have used a bipedal stance more frequently than did other sauropods. These correlations between ichnology, biomechanics, and systematics imply that titanosaurs were unique among sauropods in having a more varied repertoire of locomotor habits.