© Springer Science + Business Media, LLC 2008 2008
Received: 19 April 2008
Accepted: 23 April 2008
Published: 25 June 2008
The occurrence, generality, and causes of large-scale evolutionary trends—directional changes over long periods of time—have been the subject of intensive study and debate in evolutionary science. Large-scale patterns in the history of life have also been of considerable interest to nonspecialists, although misinterpretations and misunderstandings of this important issue are common and can have significant implications for an overall understanding of evolution. This paper provides an overview of how trends are identified, categorized, and explained in evolutionary biology. Rather than reviewing any particular trend in detail, the intent is to provide a framework for understanding large-scale evolutionary patterns in general and to highlight the fact that both the patterns and their underlying causes are usually quite complex.
The detection, characterization, and explanation of patterns represent major components of the scientific endeavor. However, those who seek to study patterns objectively must overcome several quirks of human psychology, including tendencies to identify patterns where there are none, to make assumptions regarding cause from the observation of a pattern alone, to extrapolate from individual cases to entire systems, and to focus on extremes rather than recognizing diversity. This is especially true in the study of historically contingent processes such as evolution, which spans nearly four billion years and encompasses the rise and disappearance of hundreds of millions, if not billions, of species and the struggles of an unimaginably large number of individual organisms.
This article provides a basic introduction to the way evolutionary trends are identified and explained in modern evolutionary biology. The general concepts reviewed in this article provide a framework for understanding large-scale patterns in evolutionary history. The most important message is that trends are real phenomena worthy of investigation, but that their properties and underlying causes are rarely simple.
Questions About Trends
Many broad trends have been postulated to characterize the history of life. For example, McShea (1998) listed eight potential large-scale trends, including overall directional changes in “entropy, energy intensiveness, evolutionary versatility, developmental depth, structural depth, adaptedness, size, and complexity.” Of these, patterns of change involving increases in body size and morphological complexity are the most familiar, and it is not difficult to see why: it is obvious that, on average, organisms today are larger and more complex than they were in the distant past. In the beginning, all life was almost certainly small and relatively simple, whereas the largest and most complex species ever to have existed (as far as is known) are still alive today, having arrived on the scene very recently in Earth history. Because they have been discussed extensively in the scientific literature (see, e.g., Valentine et al. 1994; Gould 1996; McShea 1996; Kingsolver and Pfennig 2004; Hone and Benton 2005; Purvis and Orme 2005; Adamowicz et al. 2008) and because they are the most familiar, trends toward increases in body size and complexity will form the basis of most of the examples used in this paper. However, worthy as they are of detailed discussion in their own right, a comprehensive review of these trends falls outside the scope of this article.
Of course, one must interpret even the most familiar patterns with caution. An increase in the average value of a particular trait counts as a trend in the most basic sense, but averages and other summary statistics are not real entities, and biological systems are most often characterized by extensive variation. As such, a change in average by itself should not be overestimated in its importance (Gould 1988, 1996). Moreover, simple comparisons between the earliest versus a few of the most recent forms of life provide few insights regarding the possible trends that may pertain to life as a whole nor about the causes of any such trends that may exist. To gain a better grasp of a given trend, several key questions must be answered about it, the most important of which are outlined in the following sections.
Is There Really a Trend?
The most obvious question to ask first is whether a trend exists at all. This may seem straightforward, but the most reliable demonstration of a trend is one that includes detailed historical information that can be difficult to obtain. Comparisons of fossils and/or inferences drawn from phylogenetic analyses2 are usually necessary to establish the existence of a trend, and these generally require considerable effort. As a result, there can be disagreement among researchers regarding the existence or generality of even the most widely studied trends such as those involving increases in body size or complexity (e.g., Gould 1996, 1997; McShea 1996). In short, trends cannot be assumed to exist but must be demonstrated empirically, no matter how intuitive their occurrence may seem.
Local or Global?
When a trend is identified on the basis of reliable historical data, it is important to ask how universal it is or, conversely, to what taxonomic groups or time spans it is limited. That is to say, it is useful to determine whether the trend is “global” taxonomically (i.e., applies to a major group, up to and including all of life) or temporally (i.e., applies to the entire history of a group, up to and including the history of all life), or if it is only “local” in taxonomic or temporal scope.
As an example, it is often claimed that lineages in general tend to exhibit gradual increases in body size over time, an observation known as “Cope’s Rule” after nineteenth century paleontologist E.D. Cope. This tendency is often taken as a global trend that applies to many lineages, if not to life at large. However, more detailed analyses of particular groups have shown it not to apply in some cases (e.g., Jablonski 1997) or to be local rather than global even in so-called classic examples of the trend.
Although the 55-My-old fossil horse sequence has been used as a classic example of Cope’s Rule, this notion is now known to be incorrect. Rather than a linear progression toward larger body size, fossil horse macroevolution is characterized by two distinctly different phases. From 55 to 20 Ma [million years ago], primitive horses had estimated body sizes between ∼10 and 50 kg. In contrast, from 20 Ma until the present, fossil horses were more diverse in their body sizes. Some clades became larger (like those that gave rise to Equus [modern horses and their relatives]), others remained relatively static in body size, and others became smaller over time. [See also MacFadden (1986, 1992)].
There evidently is a trend toward increased body size in horses, but it is localized to certain genera and time periods and reflects increasing diversity rather than a strong global tendency across all lineages. Merely comparing modern genera (Equus) with the earliest members of the group (Hyracotherium) may reveal an average increase in size, but this provides a greatly oversimplified view of a complex and interesting pattern. It also fails to indicate that had a different horse lineage, such as the dwarfed members of the genus Nannippus, been the sole survivor to the present instead of the familiar, large-bodied Equus—both of which went extinct in their original New World ranges in North America with migrant populations of Equus surviving in the Old World—then any such trend would hardly have been so apparent (Gould 1987).
Branching or No Branching?
What Accounts for the Trend? Dynamics, Causes, and Bases
Dynamics. Digging down one level from the large-scale trend itself, one may ask about the patterns of change that have occurred within component lineages and over shorter timescales. In particular, whether the internal dynamics of the larger trend have involved consistent change in all lineages or whether the trend represents the net outcome of a more complex internal dynamic (McShea 1994).
Causes. Proceeding a step farther, one may investigate the causes behind the internal dynamics that add up to a trend. For example, are these dynamics caused by natural selection or a nonadaptive constraint (see below)?
Bases. Finally, any particular cause (which results in dynamics that add up to a trend) must have a basis (or bases). For example, if the cause is determined to be natural selection operating among individuals in a population, one may ask what the basis is, i.e., what survival and/or reproductive advantage relative to alternatives is involved in generating nonrandom differences in success among individuals. This could be anything from enhancing prey capture to avoiding being eaten to attracting more mates or some combination of several such factors.
Summary of the levels of explanation for large-scale evolutionary trends with hypothetical examples of each
A pattern of large-scale change in a parameter in a given direction, especially in terms of the average across multiple lineages and long periods of time.
An observed pattern in which average body size increases within several major lineages of animals over millions of years.
The characteristics of changes among component lineages or at smaller time scales that underlie a large-scale trend. If the dynamics occur consistently in one direction, then the trend is driven, whereas if the dynamics vary, then the trend is passive.
A driven trend in which descendant species consistently have larger bodies on average than their ancestors, or a passive trend in which lineages begin at small size such that a bounded increase in variance results in an increase in average size.
The cause(s) of the dynamics that generate trends.
A driven trend caused by natural selection operating among individuals, or a passive trend resulting from a developmental constraint that limits change in one direction.
The specific underlying basis (or bases) for the cause(s) of trend dynamics.
Natural selection for larger body size on the basis of larger individuals being more effective predators or acquiring better territories relative to smaller individuals, or developmental constraints related to limitations on organ function at very small sizes.
Not only do influences at each of these levels play a role in producing trends (and, therefore, remain important in explaining any given trend), but to further complicate the situation, it is possible that several factors are at play at each of these levels or that different ones apply at different times in the long-term history of a group (e.g., Trammer and Haim 1999). Fortunately, evolutionary biologists have developed a series of analytical methods for testing and understanding the dynamics underlying trends, the causes that generate them, and both adaptive and nonadaptive bases behind the causes.
Trend Dynamics: Driven Versus Passive Trends
Driven Versus Passive Trends: What They Are and Why it Matters
Given these caveats regarding the way that driven versus passive trends can (or more properly, cannot) be interpreted, one may wonder why there has been so much interest among biologists in applying these designations to observed trends. A simple reason is that determining whether a trend is driven or passive can help to focus the inquiry regarding causes. For example, identifying a trend as driven may not automatically imply that it results from adaptive change, but it does highlight the need to investigate this possibility further. Discovering more complex dynamics while evaluating whether a trend is driven or passive may also help to direct further investigations, for example, by indicating which lineages follow the trend and which do not, with the differences allowing hypotheses to be formulated and tested regarding the causes of the dynamics.
If such a trend in primates exists and it is driven, that is, if the trend is a direct result of concerted forces acting on most lineages across the intelligence spectrum, then the inference is justified. But if it is passive, that is, forces act only on lineages at the low-intelligence end, then most lineages will have no increasing tendency. In that case, most primate species—especially those out on the right tail of the distribution like ours—would be just as likely to lose intelligence as to gain it in subsequent evolution (if they change at all).
Clearly, then, determining whether trends are driven or passive is an important aspect of their study. To this end, evolutionary biologists have developed several tests that can be applied to fossil data to address this question. In many cases these are used together, in part because no single test provides a conclusive designation on its own.
Test of the Minimum
Subclade and Skewness Tests
Test of Ancestor–Descendant Pairings
Causes of Trends
Whether the dynamics underlying a particular trend are driven, passive, or some combination of both, they in turn call out for an explanation based on an identification of their underlying causes (and, at an even deeper level of resolution, the bases for those causes; Table 1). There are numerous processes capable of causing either driven or passive trends, which by and large are not mutually exclusive and may interact in interesting ways (Alroy 2000; Gould 2002). Some of these relate to processes operating within populations, or what can be considered standard neo-Darwinian evolution, and may involve either external factors (e.g., related to the environment in which organisms live) or internal ones (e.g., related to the development of organisms). Still others exert their influence only at higher levels, such as through sorting among species, and are, therefore, part of a broader, “macroevolutionary” view of evolution (e.g., Alroy 2000; Gould 2002). There is disagreement among evolutionary biologists as to whether population- or species-level processes predominate in the creation of most large-scale trends (Gould 1988, 2002; Maurer et al. 1992; Hallam 1998), but it is worth considering the various possible causes that have been proposed.
Natural Selection and Constraints
Driven dynamic caused by natural selection. This is the situation described above, in which standard neo-Darwinian natural selection engenders persistent, adaptive change at the population level which, over time, is extrapolated into larger-scale patterns. In terms of body size, for example, data from a range of species indicate that there is often a tendency for larger individuals to be at an advantage relative to smaller members of the population for many reasons (Fig. 12), such as better defense against predation, improved success as predators, increased success in competition for resources or mates, larger brain size, higher thermal tolerance, and longer lifespan (Kingsolver and Pfennig 2004; Hone and Benton 2005).
Passive dynamic caused by natural selection. It is important to note that the outcome of natural selection can be conservative as well as directional, meaning that some forms (known as purifying selection or stabilizing selection) may prevent changes in certain traits. In particular, if the morphology of organisms in a population is well suited to their environment, then any deviations from this could lead to lower fitness. If this limitation on change occurs primarily in one direction, for example if there is a lower boundary on complexity in which a reduction becomes maladaptive, then selection would prevent decreases in the minimum within a distribution such that any increase in diversity (which may, of course, represent adaptive change) would be in one direction and a passive trend would be the result. Thus, selection can be a cause of either driven or passive trends, depending on whether it is directional or stabilizing.
Driven dynamic caused by constraints. The development of organisms consists of a complex and interconnected series of programmed changes that can often be limited in flexibility. That is, some forms of mutation may be more likely to appear in the population than others, resulting in changes that occur consistently in only one direction—i.e., a driven trend. If this is based on internal constraints on the sorts of changes that are possible, then it would differ from the selective constraints described above. A driven trend may also result from a tendency for serially repeated or modular structures within organisms that begin similar to each other to become more different simply because there are more ways for such structures to differ than to be the same. Serially repeated limbs in arthropods, for example, may be very similar to each other when they first evolve, such that any changes to the characteristics of their limbs will almost certainly involve divergence between them and, hence, greater limb complexity (McShea 2005).
Passive dynamic caused by constraints. Not all limitations to expanding variance are the result of natural selection. Some simply represent physical limits on the range of morphologies that are possible. For example, the minimum number of cells of which a living organism can be composed is one. If life began as single-celled, then expanding diversity could only involve increases in maximum cell number (see, e.g., Valentine et al. 1994).
Whether they relate to directional selection, selective constraints, or nonadaptive constraints (or some combination thereof), these causes often are assumed to operate at the level of organisms within populations. Their influence on large-scale trends would, therefore, involve extending these effects through long periods of time, which is consistent with the principles of neo-Darwinian theory. However, it has also been postulated that factors operating among species can generate trends at higher levels. It is interesting to note that many of these are recognizable as analogs of population-level processes.
It is also possible that once a change occurs in a new species, it cannot be undone. According to “Dollo’s Law,” many substantial changes during the course of evolution are irreversible. For example, it has been suggested that once lost, a complex feature cannot be regained as the probability of its reemergence is too slight. Possible exceptions to this principle have been noted (e.g., Collin and Cipriani 2003; Domes et al. 2007), but it remains the case that a tendency toward irreversibility would produce a trend resulting from directional speciation. Changes in a certain direction would create a “moving wall” under such a scenario, making further changes possible in only one direction. In another scenario proposed by Wagner (1996), reversals of evolution remain possible until a certain threshold has been crossed, at which point the lineage remains “trapped” and may continue to change only in one direction from that point on. This, too, could result in a large-scale trend (Fig. 13b).
Differential Speciation Rate
If larger-bodied individuals tend to leave more offspring than their smaller counterparts and if their offspring inherit their parents’ large size, then over time the average body size of the population will increase. A similar process may operate at the species level if the same basic requirements of differential reproduction and heritability are met. Thus, if species exhibiting a larger value for some characteristic tend to undergo speciation more often (i.e., to leave more daughter species) and these descendant species inherit this higher value from their ancestors, then a trend toward an increase in that characteristic can result (Fig. 13c; Gould 1990, 2002).
Differential Species Longevity
Like organisms, species produced through cladogenesis (branching of lineages) have a “birth” (speciation) and a “death” (extinction) in between which is a lifespan. As in the case of differential reproduction, differential longevity of species (i.e., longer duration before extinction based on particular characteristics) can generate large-scale trends over long time periods as species with this characteristic persist and become more abundant whereas those lacking it disappear more quickly (Fig. 13d).
The classical Darwinian response works just as well at the level of species elimination within clades. Suppose that patterns of speciation are entirely random with respect to the direction of a trend… Differential extinction can move a cladal mode anywhere within the spectrum of variation among species. With a new mode at the old periphery, random speciation can reconstitute variation that moves into a previously unoccupied morphospace, and directional extinction can then continue to accentuate the trend.
Differential Survival Through Mass Extinctions
Because species within clades exist in small numbers compared to the number of organisms in populations, Gould (1990) argued that differential extinction will often be dominated more by chance (a species-level analog of genetic drift, as it were, which is stronger in small samples) rather than by species-level selection. Nowhere is this more apparent than in the case of mass extinctions: drastic and accelerated losses of biodiversity because of chance events (essentially species-level analogs of population bottlenecks).
Adaptive changes occurring within populations during “normal” conditions may have little bearing on whether a species survives a mass extinction event. Nevertheless, whether by chance or the possession of traits that are relevant for survival during such extraordinary circumstances, differential survival through mass extinction events does occur. This not only can halt trends that had been proceeding before the event, it also can generate trends of its own (Fig. 13e)—in fact, it is possible that trends generated during normal times can be reversed by those resulting from a mass extinction.
The Effect Hypothesis
Whereas some authors contend that large-scale trends are the end result of directional natural selection operating within species, others argue that differential speciation or extinction—perhaps even constituting a form of “species selection”—are more important. A third alternative was presented by Vrba (1980, 1983), which she dubbed the “effect hypothesis.” Under this view, anagenetic change that may be adaptive within species can have incidental consequences for species diversification or extinction, thereby generating cladogenetic trends. In other words, large-scale trends can be nonadaptive side effects of small-scale, adaptive processes.
Organisms are integrated entities, and changes in one feature often engender correlated changes in other features. For this reason, it is possible that some trends, although they are well-supported by careful analysis, are merely spurious (Wagner 1996). That is to say, the trait showing a trend is merely correlated to another trait that is actually driving the trend. As an example, a driven trend toward increased body size will automatically bring with it many additional changes (e.g., longer generation time) that would exhibit trends along with body size. This process has been called “species hitchhiking,” as an analogy to genetic hitchhiking in which a variant of a gene spreads in a population over many generations not because it confers an advantage itself but because it is linked to a different gene that does (Wagner 1996; Levinton 2001).
Why Don’t Trends Continue Indefinitely?
Physical limits. Organisms are subject to various physical limitations that can place a cap on the extent of change that is possible. For example, land-dwelling mammals are probably limited to a certain maximum size by the effects of gravity (which is lessened in water because of the effects of buoyancy) and insects may be limited to a maximum body size by their mostly passive respiratory systems.
Genetic limits. Consistent, directional change requires the continual addition of new variation (by mutation at the population level, by speciation at the species level). It is possible that, at some stage, the requisite mutations simply never occur and directional change slows or stops as a result.
Ecological limits. In addition to limitations inherent to individual organisms, there may be external limits imposed by the environment. By way of example, larger organisms require more energy intake, and it is possible that this becomes impossible to achieve beyond a certain size.
Reaching an optimum. In some cases, adaptive change may continue only to a certain point where an optimum is reached, beyond which any additional increase is less adaptive. Driven change in this case will occur only during the period before the point where this optimum is reached.
Changing environments. Driven trends caused by natural selection will continue only so long as the selective pressure exists. In a world of changing physical and biological environments, specific selective pressures that generate directional change are often only temporary.
Organism-level trade-offs. As noted previously, changes to one feature almost certainly instigate correlated changes in other features. In some cases, this is neutral or even positive, but in others it is negative. When changes in a particular feature begin to compromise the function of others, this may place a limit on further modification.
Species-level trade-offs. It is possible for directional changes occurring as a result of short-term, population-level processes to exert consequences for the species in the long term. For example, increases in body size may be favored within species (Kingsolver and Pfennig 2004), but larger animals tend to be less abundant and to have slower reproductive cycles, which can make them more prone to extinction (McKinney 1997; Hone and Benton 2005; Purvis and Orme 2005). Overall, then, there may be anagenetic increases within lineages creating a trend that is counteracted by the effects of differential species longevity. In North American canids, for example, there appears to have been a trend toward increased body size within lineages which then became more prone to extinction (Van Valkenburgh et al. 2004).
Mass extinction. Regardless of the trends that had been underway during normal times, the massive, mostly indiscriminate loss of biodiversity during mass extinctions may fundamentally change the distribution of species and halt, reset, or even reverse previous trends. For example, there appears to have been a trend toward increased body size among dinosaurs, but obviously this ceased when they disappeared during the Cretaceous–Tertiary (K/T) extinction event (Hone et al. 2005). Subsequently, a trend toward increased average body size began among mammals (Alroy 1998). In most early bird lineages, there was a trend toward increased body size before the K/T event, but only the lineage from which modern birds evolved, which had been undergoing a trend toward reduction in body size, survived this event (Hone et al. 2008).
Just as there are numerous complex and potentially interacting causes of trends, so too are there many reasons why trends may be limited in scope or duration.
The identification and explanation of large-scale patterns in the history of life represents an important but challenging component of evolutionary research. It is apparent that many different mechanisms can result in large-scale evolutionary trends with natural selection operating within populations representing only one of these. Both constraints and higher-level processes may be responsible for generating trends, which may be passive as well as driven and may be influenced by a number of factors. Many trends are localized either taxonomically or in time, and there is no evidence to support popular conceptions of evolution as an inexorable march in any direction, be it toward larger size, greater complexity, heightened intelligence, or any other trait. Rather, the processes and patterns of evolution are, like its products, intriguingly diverse.
Some authors consider only consistent, directional change within lineages to constitute a trend, but a broader definition that allows for changes in average traits within entire clades is used in this article. This is in line with several more technical definitions of an evolutionary trend that have been presented previously, which include “a long-term directional change in a summary statistic for a clade, such as the mean” (McShea 2005) and “a directional character gradient through time in a well-defined monophyletic clade” (Gould 1990). According to McKinney (1990), “Trends are persistent statistical tendencies in some state variable(s) in an evolutionary time series. Such variables may be point estimates (e.g., mean, maximum) of a group (e.g., cladogenetic, concerning a number of species) or a single lineage (anagenetic, concerning a number of individuals in a species).” For a review of the terms “clade” and “monophyly”, see Gregory (2008).
Phylogenies, or evolutionary trees, provide information regarding the relationships among lineages (see Gregory 2008) and can be used—with due caution—to infer the characteristics of hypothetical ancestors for comparison with those of their modern descendants.
Some authors have used the term “directed” in a manner similar to “driven” (e.g., McKinney 1990), and the term “active” has been used interchangeably with “driven” by others (e.g., McShea 1993; Trammer and Kaim 1999; Alroy 2000). On the other hand, Wagner (1996) defined “active” trends as ones in which there is replacement of ancestral morphologies with more derived ones over time (Fig. 1C), which is a broader category that includes McShea’s (1994) driven trends as a subset (see also Finarelli 2007). At the same time, Wagner (1996) considered passive trends to be strictly those resulting from expansions of variance that can occur in only one direction (Fig. 6), which is more restrictive than McShea’s (1994) definition. More recently, Alroy (2000) criticized the entire driven versus passive dichotomy as oversimplified, although McShea (2000) and Wang (2005) argued in favor of maintaining these terms. Debates about terminology and the concepts that it reflects are not uncommon when dealing with complex topics such as this. As McShea (2000) noted, “It has been said that most scientists would rather use another scientist’s toothbrush than his terminology.”
I thank Sarah Adamowicz and Niles Eldredge for helpful comments on an earlier draft of the paper. I also thank Sean, Makiko, and Julian of the Gregory/Kajimura family for their gracious hospitality in Japan while this paper was in preparation.
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