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.     

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.     

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.     

Evolutionary dynamics of vertebrate body mass range

Change in body mass with time has been considered for many clades, often with reference to Cope's rule, which predicts a tendency to increase in body size. A more general rule, namely increase in the range of body mass with time, is analyzed here for vertebrates. The log range of log vertebrate body mass is shown to increase linearly and highly significantly with the log of duration of clade existence. The resulting regression equations are used to predict the origin age, initial body mass, and subsequent dynamics of body mass range for primate clades such as the New World monkeys (Platyrrhini, 32 million years ago, initial mass of 1.7 kg) and the Anthropoidea (57 million years ago, initial mass of 0.12 kg), tested against the primate fossil record. Using these methods, other major primate clades such as Lemuriformes and Adapoidea are also estimated to have originated in the Tertiary (63 and 64 million years ago, respectively), with only the Plesiadapiformes originating in the Cretaceous (83 million years ago). Similarities of body mass range between primate and other vertebrate sister groups are discussed. Linear relationships of log range and log duration are considered with respect to Brownian processes, with the expected regression coefficients from the latter explored through simulations. The observed data produce regression coefficients that overlap with or are higher than those under Brownian processes. Overall, the analyses suggest the dynamics of vertebrate body mass range in morphologically disparate clades are highly predictable over many tens of million years and that the dynamics of phenotypic characteristics can assist molecular clock and fossil models in dating evolutionary events.     

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.     

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.     

Directionality theory and the evolution of body size

Directionality theory, a dynamic theory of evolution that integrates population genetics with demography, is based on the concept of evolutionary entropy, a measure of the variability in the age of reproducing individuals in a population. The main tenets of the theory are three principles relating the response to the ecological constraints a population experiences, with trends in entropy as the population evolves under mutation and natural selection. (i) Stationary size or fluctuations around a stationary size (bounded growth): a unidirectional increase in entropy; (ii) prolonged episodes of exponential growth (unbounded growth), large population size: a unidirectional decrease in entropy; and (iii) prolonged episodes of exponential growth (unbounded growth), small population size: random, non-directional change in entropy. We invoke these principles, together with an allometric relationship between entropy, and the morphometric variable body size, to provide evolutionary explanations of three empirical patterns pertaining to trends in body size, namely (i) Cope's rule, the tendency towards size increase within phyletic lineages; (ii) the island rule, which pertains to changes in body size that occur as species migrate from mainland populations to colonize island habitats; and (iii) Bergmann's rule, the tendency towards size increase with increasing latitude. The observation that these ecotypic patterns can be explained in terms of the directionality principles for entropy underscores the significance of evolutionary entropy as a unifying concept in forging a link between micro-evolution, the dynamics of gene frequency change, and macro-evolution, dynamic changes in morphometric variables.     

Evolution and development of the primate limb skeleton

The order Primates is composed of many closely related lineages, each having a relatively well established phylogeny supported by both the fossil record and molecular data. 1 Primate evolution is characterized by a series of adaptive radiations beginning early in the Cenozoic era. Studies of these radiations have uncovered two major trends. One is that substantial amounts of morphological diversity have been produced over short periods of evolutionary time. 2 The other is that consistent and repeated patterns (variational tendencies 3 ) are detected. Taxa within clades, such as the strepsirrhines of Madagascar and the platyrrhines of the Neotropics, have diversified in body size, substrate preference, and diet. 2 , 4 - 6 The diversification of adaptive strategies within such clades is accompanied by repeated patterns of change in cheiridial proportions 7 , 8 (Fig. 1) and tooth‐cusp morphology. 9 There are obvious adaptive, natural‐selection based explanations for these patterns. The hands and feet are in direct contact with a substrate, so their form would be expected to reflect substrate preference, whereas tooth shape is related directly to the functional demands of masticating foods having different mechanical properties. What remains unclear, however, is the role of developmental and genetic processes that underlie the evolutionary diversity of the primate body plan. Are variational tendencies a signature of constraints in developmental pathways? What is the genetic basis for similar morphological transformations among closely related species? These are a sampling of the types of questions we believe can be addressed by future research integrating evidence from paleontology, comparative morphology, and developmental genetics.     

Primate origins: evolutionary change in digital ray patterning and segmentation

This study presents evidence that the first primates share with extant lemurs, tarsiers, and anthropoids hand proportions unlike those of their close relatives, the tree shrews (Scandentia), colugos (Dermoptera), and plesiadapiforms. Specifically, early primates as well as modern strepsirhines and haplorhines have relatively short metacarpals and long proximal phalanges giving them a grasping, prehensile hand. Limb development was studied in the primate Microcebus murinus and a comparative sample of rodents, artiodactyls, and marsupials to investigate the role of embryonic patterning in the morphogenesis and evolution of primate hand proportions. Comparative analysis shows that the derived finger proportions of primates are generated during the early phases of digital ray patterning and segmentation, when the interzone cells marking the presumptive metacarpo- and interphalangeal joints first appear. Interspecific variation in relative digit and metapodial proportions therefore has high developmental penetrance; that is, adult differences are observed at early ontogenetic stages. The paleontological, comparative, and developmental data are therefore consistent with the hypothesis that the early Cenozoic origin of primates involved an evolutionary change in digital ray pattern formation ultimately yielding a grasping, prehensile hand.     

THE EVOLUTIONARY HISTORY OF CETACEAN BRAIN AND BODY SIZE

Cetaceans rival primates in brain size relative to body size and include species with the largest brains and biggest bodies to have ever evolved. Cetaceans are remarkably diverse, varying in both phenotypes by several orders of magnitude, with notable differences between the two extant suborders, Mysticeti and Odontoceti. We analyzed the evolutionary history of brain and body mass, and relative brain size measured by the encephalization quotient (EQ), using a data set of extinct and extant taxa to capture temporal variation in the mode and direction of evolution. Our results suggest that cetacean brain and body mass evolved under strong directional trends to increase through time, but decreases in EQ were widespread. Mysticetes have significantly lower EQs than odontocetes due to a shift in brain:body allometry following the divergence of the suborders, caused by rapid increases in body mass in Mysticeti and a period of body mass reduction in Odontoceti. The pattern in Cetacea contrasts with that in primates, which experienced strong trends to increase brain mass and relative brain size, but not body mass. We discuss what these analyses reveal about the convergent evolution of large brains, and highlight that until recently the most encephalized mammals were odontocetes, not primates.     

Adaptive origins of primates revisited

Interpretation of the adaptive profile of ancestral primates is controversial and has been constrained for decades by general acceptance of the premise that the first primates were very small. Here we show that neither the fossil record nor modern species provide evidence that the last common ancestor of living primates was small. Instead, comparative weight distributions of arboreal mammals and a phylogenetic reconstruction of ancestral primate body mass indicate that the reduction of functional claws to nails -- a primate characteristic that had up until now eluded satisfactory explanation - resulted from an increase in body mass to around 1000 g or more in the primate stem lineage. The associated shift to a largely vegetarian diet coincided with increased angiosperm diversity and the evolution of larger fruit size during the Late Cretaceous.     

Scaling of Size and Dimorphism in Primates II: Macroevolution

Previous researchers found positive scaling of body size and sexual size dimorphism (SSD) in primates, known as Rensch's rule. The pattern is present in Haplorhini, but absent in Strepsirhini. I found that positive evolutionary correlations between size and SSD drive positive scaling relationships within Haplorhini as a whole and Platyrrhini, Cercopithecinae, Colobinae, and Hominoidea individually at the generic level and higher, but that evolutionary correlations within genera in these clades are often nonsignificant or negative. I suggest that positive evolutionary correlations result from greater change in male than in female size, usually because of sexual selection acting on polygynous populations. I suggest that negative evolutionary correlations result from greater change in female size, owing to either natural selection or, in Callitrichidae, sexual selection acting on polyandrous populations. The high incidence of negative evolutionary correlations within Haplorhini suggests a relatively large influence of natural selection on SSD, at least with regard to differences in SSD between congeners. I propose two possible explanations for the difference in intrageneric and supergeneric evolutionary patterns: 1) natural selection is a relatively weak force for modifying SSD and has a noticeable effect only when one compares related species experiencing similar levels of sexual selection, and 2) natural selection is a relatively strong force for modifying SSD but is less likely than sexual selection to affect higher level taxonomic comparisons noticeably because of the cumulative effect over time of marginal differences in mortality rates of these two types of selection. I discuss types of data required to test these explanations and implications for reconstructing fossil behavior.     

Predation and primate evolution

This paper presents the results of a general review of predation on nonhuman primates as a selective force in primate evolution. Testable hypotheses derived from the literature on predation on primates, concerning sexual dimorphism, male defense, group size, solitaries, transfer, subgrouping, and sex ratio, were applied to the available data on populations with varying predation rates in search of significant correlations. All seven hypotheses were supported, indicating that predation is and has been an important determinant of primate evolutionary history. Suggestions for accumulating a larger and more accurate body of information on predation rates on primates are offered.     

Females drive primate social evolution

Within and across species of primates, the number of males in primate groups is correlated with the number of females. This correlation may arise owing to ecological forces operating on females, with subsequent competition among males for access to groups of females. The temporal relationship between changes in male and female group membership remains unexplored in primates and other mammalian groups. We used a phylogenetic comparative method for detecting evolutionary lag to test whether evolutionary change in the number of males lags behind change in the number of females. We found that change in male membership in primate groups is positively correlated with divergence time in pairwise comparisons. This result is consistent with male numbers adjusting to female group size and highlights the importance of focusing on females when studying primate social evolution.     

The evolutionary radiation of plesiadapiforms

Very shortly after the disappearance of the non‐avian dinosaurs, the first mammals that had features similar to those of primates started appearing. These first primitive forms went on to spawn a rich diversity of plesiadapiforms, often referred to as archaic primates. Like many living primates, plesiadapiforms were small arboreal animals that generally ate fruit, insects, and, occasionally, leaves. However, this group lacked several diagnostic features of euprimates. They also had extraordinarily diverse specializations, represented in eleven families and more than 140 species, which, in some cases, were like nothing seen since in the primate order. Plesiadapiforms are known from all three Northern continents, with representatives that persisted until at least 37 million years ago. In this article we provide a summary of the incredible diversity of plesiadapiform morphology and adaptations, reviewing our knowledge of all eleven families. We also discuss the challenges that remain in our understanding of their ecology and evolution.     

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.     

Relief index of second mandibular molars is a correlate of diet among prosimian primates and other euarchontan mammals

This study describes and tests a new method of calculating a shape metric known as the relief index (RFI) on lower second molars of extant euarchontan mammals, including scandentians (treeshrews), dermopterans (flying lemurs), and prosimian primates (strepsirhines and tarsiers). RFI is the ratio of the tooth crown three-dimensional area to two-dimensional planar area. It essentially expresses hypsodonty and complexity of tooth shape. Like other measurements of complexity, RFI ignores taxon-specific features, such as certain cusps and crests, which are usually considered in more traditional studies of tooth function. Traditional statistical analyses of the study sample show that RFI distinguishes taxa with differing amounts of structural carbohydrates in their diets, with frugivore/gramnivores being significantly lower in RFI than omnivores, and insectivores/folivores being significantly higher in RFI than the other two. Information on absolute size, or body mass, is needed to reliably parse out insectivores and folivores; however, if the study sample is limited to Primates, RFI alone distinguishes many folivores (lower) from insectivores (higher). Finally, phylogenetically independent contrasts of RFI and dietary preference are strongly correlated with one another, indicating that variance in RFI is better explained by dietary diversity than phylogenetic affinity in this sample. Because of the accuracy and phylogenetic insensitivity of the RFI among Euarchonta, this method can be applied to fossil primates and stem-primates (plesiadapiforms) and used to elucidate and compare their dietary preferences. Such comparisons are important for developing a more detailed view of primate evolution.     

Sexual Size Dimorphism,Canine Dimorphism,and Male-Male Competition in Primates

Sexual size dimorphism is generally associated with sexual selection via agonistic male competition in nonhuman primates. These primate models play an important role in understanding the origins and evolution of human behavior. Human size dimorphism is often hypothesized to be associated with high rates of male violence and polygyny. This raises the question of whether human dimorphism and patterns of male violence are inherited from a common ancestor with chimpanzees or are uniquely derived. Here I review patterns of, and causal models for, dimorphism in humans and other primates. While dimorphism in primates is associated with agonistic male mate competition, a variety of factors can affect male and female size, and thereby dimorphism. The causes of human sexual size dimorphism are uncertain, and could involve several non-mutually-exclusive mechanisms, such as mate competition, resource competition, intergroup violence, and female choice. A phylogenetic reconstruction of the evolution of dimorphism, including fossil hominins, indicates that the modern human condition is derived. This suggests that at least some behavioral similarities with Pan associated with dimorphism may have arisen independently, and not directly from a common ancestor.     

Intrinsic hand proportions of euarchontans and other mammals: implications for the locomotor behavior of plesiadapiforms

Arboreal primates have distinctive intrinsic hand proportions compared with many other mammals. Within Euarchonta, platyrrhines and strepsirrhines have longer manual proximal phalanges relative to metacarpal length than colugos and terrestrial tree shrews. This trait is part of a complex of features allowing primates to grasp small-diameter arboreal substrates. In addition to many living and Eocene primates, relative elongation of proximal manual phalanges is also present in most plesiadapiforms. In order to evaluate the functional and evolutionary implications of manual similarities between crown primates and plesiadapiforms, we measured the lengths of the metacarpal, proximal phalanx, and intermediate phalanx of manual ray III for 132 extant mammal species (n=702 individuals). These data were compared with measurements of hands in six plesiadapiform species using ternary diagrams and phalangeal indices. Our analyses reveal that many arboreal mammals (including some tree shrews, rodents, marsupials, and carnivorans) have manual ray III proportions similar to those of various arboreal primates. By contrast, terrestrial tree shrews have hand proportions most similar to those of other terrestrial mammals, and colugos are highly derived in having relatively long intermediate phalanges. Phalangeal indices of arboreal species are significantly greater than those of the terrestrial species in our sample, reflecting the utility of having relatively long digits in an arboreal context. Although mammals known to be capable of prehensile grips demonstrate long digits relative to palm length, this feature is not uniquely associated with manual prehension and should be interpreted with caution in fossil taxa. Among plesiadapiforms, Carpolestes, Nannodectes, Ignacius, and Dryomomys have manual ray III proportions that are unlike those of most terrestrial species and most similar to those of various arboreal species of primates, tree shrews, and rodents. Within Euarchonta, Ignacius and Carpolestes have intrinsic hand proportions most comparable to those of living arboreal primates, while Nannodectes is very similar to the arboreal tree shrew Tupaia minor. These results provide additional evidence that plesiadapiforms were arboreal and support the hypothesis that Euarchonta originated in an arboreal milieu.     

Problems of body-weight estimation in fossil primates

Body-weight estimates of fossil primates are commonly used to infer many important aspects of primate paleobiology, including diet, ecology, and relative encephalization. It is important to examine carefully the methodologies and problems associated with such estimates and the degree to which one can have confidence in them. New regression equations for predicting body weight in fossil primates are given which provide body-weight estimates for most nonhominid primate species in the fossil record. The consequences of using different subgroups (evolutionary “grades”) of primate species to estimate fossil-primate body weights are explored and the implications of these results for interpreting the primate fossil record are discussed. All species (fossil and extant) were separated into the following “grades”: prosimian grade, monkey grade, ape grade, anthropoid grade, and all-primates grade. Regression equations relating lower molar size to body weight for each of these grades were then calculated. In addition, a female-anthropoid grade regression was also calculated for predicting body weight infernales of extinct, sexually dimorphic anthropoid species. These equations were then used to generate the fossil-primate body weights. In many instances, the predicted fossil-primate body weights differ substantially from previous estimates.