Some problems with assessing Cope's Rule

Cope's Rule states that the size of species tends to increase along an evolutionary lineage. A basic statistical framework is elucidated for testing Cope's Rule and some surprising complications are pointed out. If Cope's Rule is formulated in terms of mean size, then it is not invariant to the way in which size is measured. If Cope's Rule is formulated in terms of median size, then it is not invariant to the degree of separation between ancestral and descendant species. Some practical problems in assessing Cope's Rule are also described. These results have implications for the empirical assessment of Cope's Rule.     

Ecological specialization in fossil mammals explains Cope's rule

Cope's rule is the trend toward increasing body size in a lineage over geological time. The rule has been explained either as passive diffusion away from a small initial body size or as an active trend upheld by the ecological and evolutionary advantages that large body size confers. An explicit and phylogenetically informed analysis of body size evolution in Cenozoic mammals shows that body size increases significantly in most inclusive clades. This increase occurs through temporal substitution of incumbent species by larger-sized close relatives within the clades. These late-appearing species have smaller spatial and temporal ranges and are rarer than the incumbents they replace, traits that are typical of ecological specialists. Cope's rule, accordingly, appears to derive mainly from increasing ecological specialization and clade-level niche expansion rather than from active selection for larger size. However, overlain on a net trend toward average size increase, significant pulses in origination of large-sized species are concentrated in periods of global cooling. These pulses plausibly record direct selection for larger body size according to Bergmann's rule, which thus appears to be independent of but concomitant with Cope's.     

Body size evolution in Mesozoic birds: little evidence for Cope's rule

Cope's rule, the tendency towards evolutionary increases in body size, is a long-standing macroevolutionary generalization that has the potential to provide insights into directionality in evolution; however, both the definition and identification of Cope's rule are controversial and problematic. A recent study [J. Evol. Biol. 21 (2008) 618] examined body size evolution in Mesozoic birds, and claimed to have identified evidence of Cope's rule occurring as a result of among-lineage species sorting. We here reassess the results of this study, and additionally carry out novel analyses testing for within-lineage patterns in body size evolution in Mesozoic birds. We demonstrate that the nonphylogenetic methods used by this previous study cannot distinguish between among- and within-lineage processes, and that statistical support for their results and conclusions is extremely weak. Our ancestor-descendant within-lineage analyses explicitly incorporate recent phylogenetic hypotheses and find little compelling evidence for Cope's rule. Cope's rule is not supported in Mesozoic birds by the available data, and body size evolution currently provides no insights into avian survivorship through the Cretaceous-Paleogene mass extinction.     

Cope's Rule in a modular organism: Directional evolution without an overarching macroevolutionary trend

Cope's Rule describes increasing body size in evolutionary lineages through geological time. This pattern has been documented in unitary organisms but does it also apply to module size in colonial organisms? We address this question using 1169 cheilostome bryozoans ranging through the entire 150 million years of their evolutionary history. The temporal pattern evident in cheilostomes as a whole shows no overall change in zooid (module) size. However, individual subclades show size increases: within a genus, younger species often have larger zooids than older species. Analyses of (paleo)latitudinal shifts show that this pattern cannot be explained by latitudinal effects (Bergmann's Rule) coupled with younger species occupying higher latitudes than older species (an “out of the tropics” hypothesis). While it is plausible that size increase was linked to the advantages of large zooids in feeding, competition for trophic resources and living space, other proposed mechanisms for Cope's Rule in unitary organisms are either inapplicable to cheilostome zooid size or cannot be evaluated. Patterns and mechanisms in colonial organisms cannot and should not be extrapolated from the better‐studied unitary organisms. And even if macroevolution simply comprises repeated rounds of microevolution, evolutionary processes occurring within lineages are not always detectable from macroevolutionary patterns.     

Macroevolutionary trends in the Dinosauria: Cope's rule

Cope's rule is the tendency for body size to increase over time along a lineage. A set of 65 phylogenetically independent comparisons, between earlier and later genera, show that Cope's rule applied in dinosaurs: later genera were on average about 25% longer than the related earlier genera to which they were compared. The tendency for size to increase was not restricted to a particular clade within the group, nor to a particular time within its history. Small lineages were more likely to increase in size, and large lineages more likely to decrease: this pattern may indicate an intermediate optimum body size, but can also be explained as an artefact of data error. The rate of size increase estimated from the phylogenetic comparisons is significantly higher than the rate seen across the fauna as a whole. This difference could indicate that within-lineage selection for larger size was opposed by clade selection favouring smaller size, but data limitations mean that alternative explanations (which we discuss) cannot be excluded. We discuss ways of unlocking the full potential usefulness of phylogenies for studying the dynamics of evolutionary trends.     

The evolution of large size: how does Cope's Rule work?

Cope's Rule is the tendency for organisms in evolving lineages to increase in size over time. The concept is detailed in many textbooks, but has rarely been demonstrated. Many suggestions of the benefits of large body size exist, but none has yet been confirmed empirically. Using a large-scale analysis of recent studies, Kingsolver and Pfennig have now shown how size benefits survival, mating success and fecundity, and they provide convincing arguments for a mechanism that is capable of driving Cope's Rule.     

Individual-level selection as a cause of Cope's rule of phyletic size increase

Cope's rule, the tendency for species within a lineage to evolve towards larger body size, has been widely reported in the fossil record, but the mechanisms leading to such phyletic size increase remain unclear. Here we show that selection acting on individual organisms generally favors larger body size. We performed an analysis of the strength of directional selection on size compared with other quantitative traits by evaluating 854 selection estimates from 42 studies of contemporaneous natural populations. For size, more than 79% of selection estimates exceed zero, whereas for other morphological traits positive and negative values are similar in frequency. The selective advantage of increased size occurs for traits implicated in both natural selection (e.g., differences in survival) and sexual selection (e.g., differences in mating success). The predominance of positive directional selection on size within populations could translate into a macroevolutionary trend toward increased size and thereby explain Cope's rule.     

Dyar's Rule and the Investment Principle: optimal moulting strategies if feeding rate is size-dependent and growth is discontinuous

We consider animals whose feeding rate depends on the size of structures that grow only by moulting (e.g. spiders'' legs). Our Investment Principle predicts optimum size increases at each moult; under simplifying assumptions these are a function of the scaling of feeding rate with size, the efficiency of moulting and the optimum size increase at the preceding moult. We show how to test this quantitatively, and make the qualitative prediction that size increases and instar durations change monotonically through development. Thus, this version of the model does not predict that proportional size increases necessarily remain constant, which is the pattern described by Dyar''s Rule. A literature survey shows that in nature size increases tend to decline and instar durations to increase, but exceptions to monotonicity occur frequently: we consider how relaxing certain assumptions of the model could explain this. Having specified various functions relating fitness to adult size and time of emergence, we calculate (using dynamic programming) the effect of manipulating food availability, time of hatching and size of the initial (or some intermediate) instar. The associated norms of reaction depend on the fitness function and differ from those when growth follows Dyar''s Rule or is continuous. We go on to consider optimization of the number of instars. The Investment Principle then predicts upper and lower limits to observed size increases and explains why increases usually change little or decline through development. This is thus a new adaptive explanation for Dyar''s Rule and for the most common deviation from the Rule.     

The evolution of body size, Cope's rule and the origin of amniotes

The evolution of body size in tetrapods is assessed using a database that includes 107 early stegocephalian species ranging in time from the Frasnian (Upper Devonian) to the Tatarian (Upper Permian). All analyses use methods that incorporate phylogenetic information (topology and branch lengths). In all tests, the impact of alternative topologies and branch lengths are assessed. Previous reports that raised doubts about the accuracy of squared-change parsimony assessment of ancestral character value appear to have used datasets in which there was no phylogenetic signal. Hence, squared-change parsimony may be more reliable than suggested in recent studies, at least when a phylogenetic signal is present in the datasets of interest. Analysis using random taxon reshuffling on three reference phylogenies shows that cranial and presacral length include a strong phylogenetic signal. Character optimization of body size in stegocephalians using squared-change parsimony on a time-calibrated phylogeny incorporating branch length information is used to test a previously published scenario on the origin of amniotes and of the amniotic egg that implies that the ancestors of amniotes were small (no more than 10 cm in snout-vent length), and that their size increased subsequent to the appearance of the amniotic egg. The optimization suggests that first amniotes were somewhat larger than previously hypothesized; the estimated snout-vent length is about 24 cm, and the lower end of the 95% confidence interval of the phylogeny that yields the smallest inferred size suggests that no ancestor of amniotes measured less than 12 cm in snout-vent length. Character optimization, permutational multiple linear regressions, and independent contrast analyses show that Cope's rule of phyletic size increase applies to early reptiliomorphs but that it does not apply to early stegocephalians globally.     

The evolution of body size in extant groups of North American freshwater fishes: speciation,size distributions,and Cope's rule

Change in body size within an evolutionary lineage over time has been under investigation since the synthesis of Cope's rule, which suggested that there is a tendency for mammals to evolve larger body size. Data from the fossil record have subsequently been examined for several other taxonomic groups to determine whether they also displayed an evolutionary increase in body size. However, we are not aware of any species-level study that has investigated the evolution of body size within an extant continental group. Data acquired from the fossil record and data derived from the evolutionary relationships of extant species are not similar, with each set exhibiting both strengths and weaknesses related to inferring evolutionary patterns. Consequently, expectation that general trends exhibited in the fossil record will correspond to patterns in extant groups is not necessarily warranted. Using phylogenetic relationships of extant species, we show that five of nine families of North American freshwater fishes exhibit an evolutionary trend of decreasing body size. These trends result from the basal position of large species and the more derived position of small species within families. Such trends may be caused by the invasion of small streams and subsequent isolation and speciation. This pattern, potentially influenced by size-biased dispersal rates and the high percentage of small streams in North America, suggests a scenario that could result in the generation of the size-frequency distribution of North American freshwater fishes.     

Cope's rule in cryptodiran turtles: do the body sizes of extant species reflect a trend of phyletic size increase?

Cope's rule of phyletic size increase is questioned as a general pattern of body size evolution. Most studies of Cope's rule have examined trends in the paleontological record. However, neontological approaches are now possible due to the development of model-based comparative methods, as well as the availability of an abundance of phylogenetic data. I examined whether the phylogenetic distribution of body sizes in extant cryptodiran turtles is consistent with Cope's rule. To do this, I examined body size evolution in each of six major clades of cryptodiran turtles and also across the whole tree of cryptodirans (n = 201 taxa). Extant cryptodiran turtles do not appear to follow Cope's rule, as no clade showed a significant phyletic body size trend. Previous analyses in other extant vertebrates have also found no evidence for phyletic size increase, which is in contrast to the paleontological data that support the rule in a number of extinct vertebrate taxa.     

Body size evolution in Mesozoic birds

The tendency for the mean body size of taxa within a clade to increase through evolution (Cope's Rule) has been demonstrated in a number of terrestrial vertebrate groups. However, because avian body size is strongly constrained by flight, any increase in size during the evolution of this lineage should be limited - there is a maximum size that can be attained by a bird for it to be able to get off the ground. Contrary to previous interpretations of early avian evolution, we demonstrate an overall increase in body size across Jurassic and Cretaceous flying birds: taxon body size increases from the earliest Jurassic through to the end of the Cretaceous, across a time span of 70 Myr. Although evidence is limited that this change is directional, it is certainly nonrandom. Relative size increase occurred presumably as the result of an increase in variance as the avian clade diversified after the origin of flight: a progression towards larger body size is seen clearly within the clades Pygostylia and Ornithothoraces. In contrast, a decrease in body size characterizes the most crownward lineage Ornithuromorpha, the clade that includes all extant taxa, and potentially may explain the survival of these birds across the Cretaceous-Palaeogene boundary. As in all other dinosaurs, counter selection for small size is seen in some clades, whereas body size is increasing overall.     

Body size evolution in an old insect order: No evidence for Cope's Rule in spite of fitness benefits of large size

We integrate field data and phylogenetic comparative analyses to investigate causes of body size evolution and stasis in an old insect order: odonates (“dragonflies and damselflies”). Fossil evidence for “Cope's Rule” in odonates is weak or nonexistent since the last major extinction event 65 million years ago, yet selection studies show consistent positive selection for increased body size among adults. In particular, we find that large males in natural populations of the banded demoiselle (Calopteryx splendens) over several generations have consistent fitness benefits both in terms of survival and mating success. Additionally, there was no evidence for stabilizing or conflicting selection between fitness components within the adult life‐stage. This lack of stabilizing selection during the adult life‐stage was independently supported by a literature survey on different male and female fitness components from several odonate species. We did detect several significant body size shifts among extant taxa using comparative methods and a large new molecular phylogeny for odonates. We suggest that the lack of Cope's rule in odonates results from conflicting selection between fitness advantages of large adult size and costs of long larval development. We also discuss competing explanations for body size stasis in this insect group.     

Body Size Evolution in Extant Oryzomyini Rodents: Cope's Rule or Miniaturization?

At the macroevolutionary level, one of the first and most important hypotheses that proposes an evolutionary tendency in the evolution of body sizes is "Cope's rule". This rule has considerable empirical support in the fossil record and predicts that the size of species within a lineage increases over evolutionary time. Nevertheless, there is also a large amount of evidence indicating the opposite pattern of miniaturization over evolutionary time. A recent analysis using a single phylogenetic tree approach and a bayesian based model of evolution found no evidence for Cope's rule in extant mammal species. Here we utilize a likelihood-based phylogenetic method, to test the evolutionary trend in body size, which considers phylogenetic uncertainty, to discern between Cope's rule and miniaturization, using extant Oryzomyini rodents as a study model. We evaluated body size trends using two principal predictions: (a) phylogenetically related species are more similar in their body size, than expected by chance; (b) body size increased (Cope's rule)/decreased (miniaturization) over time. Consequently the distribution of forces and/or constraints that affect the tendency are homogenous and generate this directional process from a small/large sized ancestor. Results showed that body size in the Oryzomyini tribe evolved according to phylogenetic relationships, with a positive trend, from a small sized ancestor. Our results support that the high diversity and specialization currently observed in the Oryzomyini tribe is a consequence of the evolutionary trend of increased body size, following and supporting Cope's rule.     

A TEST FOR COPE'S RULE

Cope's Rule refers to the tendency of body size to increase along an evolutionary lineage. This rule is commonly tested by comparing size differences in pairs of taxa, one of which is assumed to be ancestral to the other. It has recently been pointed out that this approach fails to account for the unknown number of speciation events separating each pair. Here, a test that does account for this degree of separation is described and applied to some published data for dinosaurs. A by-product of the analysis is an estimate of the origination rate of dinosaur species.     

Locomotor mode, maximum running speed, and basal metabolic rate in placental mammals

The locomotor performance (absolute maximum running speed [MRS]) of 120 mammals was analyzed for four different locomotor modes (plantigrade, digitigrade, unguligrade, and lagomorph-like) in terms of body size and basal metabolic rate (BMR). Analyses of conventional species data showed that the MRS of plantigrade and digitigrade mammals and lagomorphs increases with body mass, whereas that of unguligrade mammals decreases with body mass. These trends were confirmed in plantigrade mammals and lagomorphs using phylogenetically independent contrasts. Multiple regression analyses of MRS contrasts (dependent variable) as a function of body mass and BMR contrasts (predictor variables) revealed that BMR was a significant predictor of MRS in the complete data set, as well as in plantigrade and nonplantigrade mammals. However, there was severe multicollinearity in the nonplantigrade model that may influence the interpretation of these models. Although these data show mass-independent correlation between BMR and MRS, they are not necessarily indicative of a cause-effect relationship. However, the analyses do identify a negligible role of body size associated with MRS once phylogenetic and BMR effects are controlled, suggesting that the body size increase in large mammals over time (i.e., Cope's rule) can probably rule out MRS as a driving variable.     

Linking macrotrends and microrates: Re‐evaluating microevolutionary support for Cope's rule

Cope's rule, wherein a lineage increases in body size through time, was originally motivated by macroevolutionary patterns observed in the fossil record. More recently, some authors have argued that evidence exists for generally positive selection on individual body size in contemporary populations, providing a microevolutionary mechanism for Cope's rule. If larger body size confers individual fitness advantages as the selection estimates suggest, thereby explaining Cope's rule, then body size should increase over microevolutionary time scales. We test this corollary by assembling a large database of studies reporting changes in phenotypic body size through time in contemporary populations, as well as studies reporting average breeding values for body size through time. Trends in body size were quite variable with an absence of any general trend, and many populations trended toward smaller body sizes. Although selection estimates can be interpreted to support Cope's rule, our results suggest that actual rates of phenotypic change for body size cannot. We discuss potential reasons for this discrepancy and its implications for the understanding of Cope's rule.     

HOW DO GEOLOGICAL SAMPLING BIASES AFFECT STUDIES OF MORPHOLOGICAL EVOLUTION IN DEEP TIME? A CASE STUDY OF PTEROSAUR (REPTILIA: ARCHOSAURIA) DISPARITY

A fundamental contribution of paleobiology to macroevolutionary theory has been the illumination of deep time patterns of diversification. However, recent work has suggested that taxonomic diversity counts taken from the fossil record may be strongly biased by uneven spatiotemporal sampling. Although morphological diversity (disparity) is also frequently used to examine evolutionary radiations, no empirical work has yet addressed how disparity might be affected by uneven fossil record sampling. Here, we use pterosaurs (Mesozoic flying reptiles) as an exemplar group to address this problem. We calculate multiple disparity metrics based upon a comprehensive anatomical dataset including a novel phylogenetic correction for missing data, statistically compare these metrics to four geological sampling proxies, and use multiple regression modeling to assess the importance of uneven sampling and exceptional fossil deposits (Lagerstätten). We find that range‐based disparity metrics are strongly affected by uneven fossil record sampling, and should therefore be interpreted cautiously. The robustness of variance‐based metrics to sample size and geological sampling suggests that they can be more confidently interpreted as reflecting true biological signals. In addition, our results highlight the problem of high levels of missing data for disparity analyses, indicating a pressing need for more theoretical and empirical work.     

Per-stage growth rates of head and body sizes in scarab larvae (Coleoptera: Scarabaeidae) decrease across ontogeny following a species-specific pattern

It has been widely assumed that the stepwise increase in the exoskeleton size of larval insects approximately follows a geometric progression from instar to instar, known as Dyar's Rule. However, it is not clear whether the per-instar increase in body size follows this rule. In insects, Dyar's Rule has been identified either by regressing the log-scaled size on the instar number (log-linear regression analysis) or by comparing the postmolt/premolt size ratio between instars (growth rate analysis). A previous study on the body mass of caterpillars showed the methodological pitfall that Dyar's Rule was statistically supported by log-linear regression analysis, but not at all by growth rates analysis. I considered this concern here by examining the per-stage growth rates of head and body sizes for larvae of the beetle Trypoxylus dichotomus using both methods and compared the resulting growth rates for body size within and between taxonomic orders. Dyar's Rule was statistically supported by the log-linear regression analysis but not by growth rate analysis for both the head and body sizes in T. dichotomus. The body size growth rate in T. dichotomus decreased as the instar progressed. This developmental pattern was also found in reported data for the other six scarabs, but not in data for Lepidoptera or Hymenoptera. These findings confirm that the per-stage growth rate of body size does not follow Dyar's Rule in a wide range of insects, and suggest that developmental change in the body size growth rate varies among insect groups.     

Do different disparity proxies converge on a common signal? Insights from the cranial morphometrics and evolutionary history of Pterosauria (Diapsida: Archosauria)

Disparity, or morphological diversity, is often quantified by evolutionary biologists investigating the macroevolutionary history of clades over geological timescales. Disparity is typically quantified using proxies for morphology, such as measurements, discrete anatomical characters, or geometric morphometrics. If different proxies produce differing results, then the accurate quantification of disparity in deep time may be problematic. However, despite this, few studies have attempted to examine disparity of a single clade using multiple morphological proxies. Here, as a case study for this question, we examine the disparity of the volant Mesozoic fossil reptile clade Pterosauria, an intensively studied group that achieved substantial morphological, ecological and taxonomic diversity during their 145+ million-year evolutionary history. We characterize broadscale patterns of cranial morphological disparity for pterosaurs for the first time using landmark-based geometric morphometrics and make comparisons to calculations of pterosaur disparity based on alternative metrics. Landmark-based disparity calculations suggest that monofenestratan pterosaurs were more diverse cranially than basal non-monofenestratan pterosaurs (at least when the aberrant anurognathids are excluded), and that peak cranial disparity may have occurred in the Early Cretaceous, relatively late in pterosaur evolution. Significantly, our cranial disparity results are broadly congruent with those based on whole skeleton discrete character and limb proportion data sets, indicating that these divergent approaches document a consistent pattern of pterosaur morphological evolution. Therefore, pterosaurs provide an exemplar case demonstrating that different proxies for morphological form can converge on the same disparity signal, which is encouraging because often only one such proxy is available for extinct clades represented by fossils. Furthermore, mapping phylogeny into cranial morphospace demonstrates that pterosaur cranial morphology is significantly correlated with, and potentially constrained by, phylogenetic relationships.