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Macroevolutionary Inferences from Primate Phylogeny
Proceedings of the Royal Society B
Abstract
We apply new statistical methods to a recent estimate of the phylogeny of all living primate species to test a range of models of cladogenesis. Null models in which probabilities of speciation and extinction do not differ among contemporaneous lineages are not consistent with the phylogeny. We present evidence that the net rate of cladogenesis (speciation rate minus extinction rate) increased in the lineage leading to the Cercopithecidae (Old World monkeys), and that there have been further increases in some lineages within that family. Such increases suggest the occurrence of clade selection, although we have not identified the selected trait or traits. There is no evidence that the net rate of cladogenesis is a function either of how many primate lineages are already present or of time. Intriguingly, three other clades--Strepsirhini, Platyrrhini and Hominoidea--appear to have had very similar rates of clade growth, in spite of their great biological differences.
... The first investigation to examine speciation and extinction rates in extant primates was conducted by Purvis et al. (1995). These authors detected rate heterogeneity by applying the birth-death model (e.g., to a time-scaled supertree containing all taxa recognized at the species level at the time of their study (n = 203; Corbet & Hill, 1991). ...
... These authors detected rate heterogeneity by applying the birth-death model (e.g., to a time-scaled supertree containing all taxa recognized at the species level at the time of their study (n = 203; Corbet & Hill, 1991). The main conclusion of Purvis et al. (1995) was that cercopithecoids differ from hominoids, platyrrhines, and strepsirrhines in having very high net rates of diversification (i.e., speciation rate minus extinction rate), indicating explosive growth over the last 10 million years of the clade's history. This result has been recovered in most subsequent studies of primate macroevolution and has survived substantial revisions to primate taxonomy and innovations in the methods used to reconstruct phylogeny and estimate macroevolutionary rates (Arbour & Santana, 2017;Fabre et al., 2009;Paradis, 1998). ...
... Whether other primates share a common macroevolutionary regime is an open question. There is some evidence that platyrrhines have higher net diversification rates than strepsirrhines (Purvis et al., 1995), and that certain platyrrhine clades may be similar to cercopithecoids (Fabre et al., 2009). This pattern of results is consistent with studies of trait-dependent diversification that indicate that diurnal primates (mostly monkeys) have diversified at higher rates than nocturnal lineages (mostly strepsirrhines) (Magnuson-Ford & Otto, 2012;Santini et al., 2015;Scott, 2018). ...
Objectives: This study examines how speciation and extinction rates vary across primates, with a focus on the recent macroevolutionary dynamics that have shaped extant primate biodiversity.
Materials and methods: Lineage-specific macroevolutionary rates were estimated for each tip in a tree containing 307 species using a hidden-state likelihood model. Differences in tip rates among major clades were evaluated using phylogenetic ANOVA. Differences among diurnal, nocturnal, and cathemeral lineages were also evaluated, based on previous work indicating that activity pattern influences primate diversification.
Results: Rate variation in extant primates is low within clades and high between clades. As in previous studies, cercopithecoids stand out in having high net diversification rates, driven by high speciation rates and very low extinction rates. Platyrrhines combine high speciation and high extinction rates, giving them high rates of lineage turnover. Strepsirrhines and tarsiids have low rates of speciation, extinction, turnover, and net diversification. Hominoids are intermediate between platyrrhines and the strepsirrhine-tarsiid group, and there is evidence for differentiation between hominids and hylobatids. Diurnal lineages have significantly higher speciation rates than nocturnal lineages.
Conclusions: Recent anthropoid macroevolution has been characterized by marked variation in diversification dynamics among clades. Strepsirrhines and tarsiids are more uniform, despite divergent evolutionary and biogeographic histories. Higher speciation rates in diurnal lineages may be driven by greater ecological opportunity or reliance on visual signals for mate recognition. However, the differences among anthropoids indicate that factors other than activity pattern (e.g., clade competition, historical contingency) have had a more influential role in shaping recent primate diversification.
... Previous investigations have demonstrated that primates have increased in species diversity since their origin (Purvis et al. 1995;Fabre et al. 2009;Springer et al. 2012;Arbour and Santana 2017;Herrera 2017). These investigations have found that diversification has been relatively constant over time; however, some diversification rate disparities have been noted, especially in the late Miocene/early Pliocene (Purvis et al. 1995;Fabre et al. 2009;Springer et al. 2012). ...
... Previous investigations have demonstrated that primates have increased in species diversity since their origin (Purvis et al. 1995;Fabre et al. 2009;Springer et al. 2012;Arbour and Santana 2017;Herrera 2017). These investigations have found that diversification has been relatively constant over time; however, some diversification rate disparities have been noted, especially in the late Miocene/early Pliocene (Purvis et al. 1995;Fabre et al. 2009;Springer et al. 2012). When species diversification rate heterogeneity is identified, it is attributed primarily to catarrhines, and in particular to Cercopithecidae, which exhibits elevated rates of diversification compared to other clades (Purvis et al. 1995;Fabre et al. 2009;Arbour and Santana 2017). ...
... These investigations have found that diversification has been relatively constant over time; however, some diversification rate disparities have been noted, especially in the late Miocene/early Pliocene (Purvis et al. 1995;Fabre et al. 2009;Springer et al. 2012). When species diversification rate heterogeneity is identified, it is attributed primarily to catarrhines, and in particular to Cercopithecidae, which exhibits elevated rates of diversification compared to other clades (Purvis et al. 1995;Fabre et al. 2009;Arbour and Santana 2017). This increase in diversification rate has been attributed to either accelerated speciation rates (Purvis et al. 1995;Fabre et al. 2009) or to a reduction in extinction rates (Arbour and Santana 2017). ...
Many authors have hypothesized an association between rates of morphological evolution and rates of species diversification, however, this association has yet to be empirically tested in the primate cranium. In this investigation, we used phylogeny-based approaches to examine the relationship between rates of species diversification, rates of cranial size and shape evolution, and observed cranial morphological disparity of extant catarrhines (Order: Primates). We used 34 3D landmarks digitized from 2038 crania representing 42 catarrhine species and a time-calibrated molecular phylogeny to determine the rates of evolution of cranial size and shape, rates of lineage diversification, and levels of morphological disparity by clade. The only significant relationship among these variables was for evolutionary rates of size and shape change. We discuss these results in the context of primate and mammalian macroevolution, and in light of the proposed hypothesis that size is a “line of least evolutionary resistance” in cranial evolution.
... The informational and conceptual integration has projected comparative studies of primates far beyond the initial scope of comparative primatology over the past three decades (e.g. Purvis et al. 1995, Purvis & Webster 1999, Kamilar & Cooper 2013, Duran & Pie 2015, Kappeler & Pozzi 2019. Furthermore, boosted by computational modelling and data science, modern studies have built upon the longknown links among different features to predict a range of behavioural, ecological, and social aspects (e.g. ...
Given the position of humans in the tree of life, comparative research on non‐human primates has attracted the interest of researchers in biology, medical sciences, anthropology, psychology, and sociology. Covariation of species' phenotypes has been of particular interest.
Learning from the historical development of comparative research with primates should thus be particularly valuable for evolutionary ecology and to improve understanding of phenotypic integration and diversity. Such learning would also help identify knowledge gaps, disputed questions, and new avenues of both basic and applied research in relation to the evolution of primate features and the conservation of our close relatives.
We conducted a historical assessment through a non‐systematic review and a systematic review, focusing on how the integration of different research lines in evolutionary ecology focused on primate phenotypic covariation unfolded throughout the 20th Century. The non‐systematic review allowed us to reconstruct the history of the discipline from its earliest origins, when bibliometric assessments were more limited in scope, and to identify the most appropriate keywords for the systematic review. We employed a standard protocol for the systematic review, applying two complementary analyses: co‐occurrence of keywords and bibliographic coupling of references. These analyses described the development of the conceptual and intellectual structures of comparative primatology from 1966 to 2020.
By identifying the most influential researchers and concept interrelations, we highlight primate phenotypes critical for the development of the discipline (in particular, brain and body sizes and behavioural patterns), showcasing the reach of these investigations for evolutionary ecology. Overall, our findings emphasise the crucial role that comparative primatology has played in developing the study of phenotypic integration and the very onset of phylogenetic comparative methods.
... Methods of quantifying taxonomic error are not specific to paleobiology and could be applied easily to Recent mammals-if more details could be added to the current picture of the history of taxonomy (Alroy 2002) and, indeed, if more primary taxonomic research could be funded. This kind of reassessment might substantially change our view of major biological patterns, such as the latitudinal diversity gradient (Badgley and Fox 2000;Simpson 1964), the differences between clades in diversification rates (Purvis et al. 1995), the relationship between body size and diversity (Gardezi and da Silva 1999;Gittleman and Purvis 1998), or the body mass distributions of continental mammal faunas (Brown and Nicoletto 1991;Chown and Gaston 1997;Marquet and Cofré 1999). There never has been a better time to take up the study of taxonomic diversity in extant and extinct mammals. ...
Body mass distributions of mammalian species are a major focus of macroecological and macroevolutionary studies. However, these distributions may be obscured by taxonomic error, just like any other aspect of biodiversity. The key problem with taxonomy is that many currently used names are synonyms of each other or are biologically indeterminate. This article reassesses body mass patterns in the fossil record of North American mammals using the recently developed flux ratio method for estimating the underlying proportion of invalid names. Current name quality varies very strongly with body mass: small species names are highly unreliable, but names of large species have been evaluated thoroughly. The main reason is that there has been a dramatic fall through historical time in the average size of described species. Hence, there simply has not been enough time yet to reevaluate the names of most small species. This bias only accentuates the previously described bimodal diversity distribution for North American mammals, which suggests the existence of dual body mass optima—so not all evolutionary lineages converge on 100 g. The historical shift in the underlying quality and body mass of newly described species also differentially affects our picture of biodiversity in major taxonomic groups. On the one hand, ungulate and carnivoran names are much more likely to be invalid in the 1st place than are rodent and insectivoran names. On the other hand, most of the invalid names for large mammals already have been identified, but this is not true for the small-mammal groups. Therefore, the most fruitful strategy for future taxonomic research would be to focus on small- and medium-sized mammals.
... For example, Sanderson and Donoghue (1994) found that shifts in diversification rates within angiosperms are not coincident with several hypothesized "key innovations". By analyzing a phylogeny of Primates, Purvis et al. (1995) detected an increase in the diversification rate of the lineage leading to the Old World monkeys, which might be related to habitat changes, land bridges, and dietary adaptations (Fleagle 1988;Conroy 1990). Alfaro et al. (2009) identify nine periods in vertebrate history where the tempo of diversification changes; the most significant of these lying at the base of a clade that includes most of the coral-reef associated fishes as well as cichlids and perches. ...
The term adaptive radiation has been recurrently used to describe evolutionary patterns of several lineages, and has been proposed as the main driver of biological diversification. Different definitions and criteria have been proposed to distinguish an adaptive radiation, and the current literature shows disagreements as to how radiating lineages should be circumscribed. Inconsistencies increase when authors try to differentiate a clade under adaptive radiation from clades evolving under ‘regular’ speciation with adaptation, a pattern anticipated and predicted by the evolutionary theory in any lineage. The most important disagreement is as to which evolutionary rate (phenotypical or taxonomical) authors analyze to characterize a radiation; a discussion embedded in a prevailing inability to provide mechanistic explanations of the relationship among evolutionary rates. The union of pattern and process in the same term, the inadequacy of reported null hypotheses, and the frequent use of ad hoc comparisons between lineages have also contributed to the lack of consensus. A rigorous use of available terms and the articulation of solid criteria with objective methodologies in distinguishing evolutionary patterns are imperative. Given the difficulties in detecting adaptation, the use of the ‘adaptive’ term to qualify a radiation should be avoided unless methodologically tested. As an unambiguous method to distinguish radiating lineages, the statistical detection of significant increases in taxonomic diversification rates on monophyletic lineages can be considered a distinctive signature of a radiation. After recognizing this pattern, causal hypotheses explaining them can be stated, as well as correlates with other rates of evolution.
Bringing together the viewpoints of leading ecologists concerned with the processes that generate patterns of diversity, and evolutionary biologists who focus on mechanisms of speciation, this book opens up discussion in order to broaden understanding of how speciation affects patterns of biological diversity, especially the uneven distribution of diversity across time, space and taxa studied by macroecologists. The contributors discuss questions such as: Are species equivalent units, providing meaningful measures of diversity? To what extent do mechanisms of speciation affect the functional nature and distribution of species diversity? How can speciation rates be measured using molecular phylogenies or data from the fossil record? What are the factors that explain variation in rates? Written for graduate students and academic researchers, the book promotes a more complete understanding of the interaction between mechanisms and rates of speciation and these patterns in biological diversity.
Bringing together the viewpoints of leading ecologists concerned with the processes that generate patterns of diversity, and evolutionary biologists who focus on mechanisms of speciation, this book opens up discussion in order to broaden understanding of how speciation affects patterns of biological diversity, especially the uneven distribution of diversity across time, space and taxa studied by macroecologists. The contributors discuss questions such as: Are species equivalent units, providing meaningful measures of diversity? To what extent do mechanisms of speciation affect the functional nature and distribution of species diversity? How can speciation rates be measured using molecular phylogenies or data from the fossil record? What are the factors that explain variation in rates? Written for graduate students and academic researchers, the book promotes a more complete understanding of the interaction between mechanisms and rates of speciation and these patterns in biological diversity.
A major goal in post‐synthesis evolutionary biology has been to better understand how complex interactions between traits drive movement along and facilitate the formation of distinct evolutionary pathways. I present analyses of a character matrix sampled across the haplorrhine skeleton that revealed several modules of characters displaying distinct patterns in macroevolutionary disparity. Comparison of these patterns to those in neurological development showed that early ape evolution was characterized by an intense regime of evolutionary and developmental flexibility. Shifting and reduced constraint in apes was met with episodic bursts in phenotypic innovation that built a wide array of functional diversity over a foundation of shared developmental and anatomical structure. Shifts in modularity drove dramatic evolutionary changes across the ape body plan in two distinct ways: 1) an episode of relaxed integration early in hominoid evolution coincided with bursts in evolutionary rate across multiple character suites; 2) the formation of two new trait modules along the branch leading to chimps and humans preceded rapid and dramatic evolutionary shifts in the carpus and pelvis. Changes to the structure of evolutionary mosaicism may correspond to enhanced evolvability that has a ‘preadaptive’ effect by catalyzing later episodes of dramatic morphological remodeling. This article is protected by copyright. All rights reserved
Aim
Community phylogenetic studies use information about the evolutionary relationships of species to understand the ecological processes of community assembly. A central premise of the field is that the evolution of species maps onto ecological patterns, and phylogeny reveals something more than species traits alone about the ecological mechanisms structuring communities, such as environmental filtering, competition, and facilitation. We argue, therefore, that there is a need for better understanding and modelling of the interaction of phylogeny with species traits and community composition.
Innovation
We outline a new approach that identifies clades that are ecophylogenetically clustered or overdispersed and assesses whether those clades have different rates of trait evolution. Ecophylogenetic theory would predict that the traits of clustered or overdispersed clades might have evolved differently, in terms of either tempo (fast or slow) or mode (e.g., under constraint or neutrally). We suggest that modelling the evolution of independent trait data in these clades represents a strong test of whether there is an association between the ecological co‐occurrence patterns of a species and its evolutionary history.
Main conclusions
Using an empirical dataset of mammals from around the world, we identify two clades of rodents whose species tend not to co‐occur in the same local assemblages (are phylogenetically overdispersed) and find independent evidence of slower rates of body mass evolution in these clades. Our approach, which assumes nothing about the mode of species trait evolution but instead seeks to explain it using ecological information, presents a new way to examine ecophylogenetic structure.
Three null models have been proposed to predict the relative frequencies of topologies of phylogenetic trees. One null model assumes each distinguishable n-member tree is equally likely (proportional-to-distinguishable-arrangements model). A second model assumes that each topological type is equally likely (equiprobable model). A third model assumes that the probability of each topological type is determined by random speciation (Markov model). We sampled published phylogenetic trees from three major groups of organisms: division Angiospermae, class Insecta, and superclass Tetrapoda. Our sampling was more restricted than previous studies and was designed to test whether observed topological frequencies were distinguishable from those predicted by the three null models. The pattern of evolution reflected in five-member phylogenetic trees is different from predictions of the equiprobable and Markov model but is indistinguishable from the proportional-to-distinguishable-arrangements model. This indicates that 1) speciation (and/or extinction) is not equally likely among all taxa, even for small phylogenies; or 2) systematists' attempts at reconstructing small phylogenies are, on average, indistinguishable from those expected if they had merely selected a tree at random from the pool of all possible trees. The topology frequencies were not different among the three groups of organisms, suggesting that factors shaping patterns of speciation and extinction are consistent among major taxonomic groups.
One tool in the study of the forces that determine species diversity is the null, or simple, model. The fit of predictions to observations, good or bad, leads to a useful paradigm or to knowledge of forces not accounted for, respectively. It is shown how simple models of speciation and extinction lead directly to predictions of the structure of phylogenetic trees. These predictions include both essential attributes of phylogenetic trees: lengths, in the form of internode distances; and topology, in the form of internode links. These models also lead directly to statistical tests which can be used to compare predictions with phylogenetic trees that are estimated from data. Two different models and eight data sets are considered. A model without species extinction consistently yielded predictions closer to observations than did a model that included extinction. It is proposed that it may be useful to think of the diversification of recently formed monophyletic groups as a random speciation process without extinction.
Phylogenies that are reconstructed without fossil material often contain approximate dates for lineage splitting. For example, particular nodes on molecular phylogenies may be dated by known geographic events that caused lineages to split, thereby calibrating a molecular clock that is used to date other nodes. On the one hand, such phylogenies contain no information about lineages that have become extinct. On the other hand, they do provide a potentially useful testing ground for ideas about evolutionary processes. Here we first ask what such reconstructed phylogenies should be expected to look like under a birth-death process in which the birth and death parameters of lineages remain constant through time. We show that it is possible to estimate both the birth and death rates of lineages from the reconstructed phylogenies, even though they contain no explicit information about extinct lineages. We also show how such phylogenies can reveal mass extinctions and how their characteristic footprint can be distinguished from similar ones produced by density-dependent cladogenesis.
The history of life is replete with apparent order. Much of this order may reflect the deterministic causes conventionally invoked, but we cannot be sure until we measure and subtract the order that arises in simple random systems. Consequently, we have constructed a random model that builds evolutionary trees by allowing lineages to branch and become extinct at equal probabilities. We proceed by dividing our simulated tree into clades and by comparing their sizes and shapes with the patterns exhibited by “real” clades as recorded by fossils.
We regard the similarity of real and random clades as the outstanding result of this comparison. In both real and random systems, extinct clades arising after an “ecological barrel” had been filled have their maximum diversity at the midpoint of their duration; clades arising during the initial “filling” reach an earlier climax during this preequilibrial period of rapid diversification. However, some potential differences also emerge. Clades still living are much larger than extinct clades. We may attribute this to the morphological superiority of survivors, but we can also simulate it in a model that chooses the originators of clades at random. Real clades undergo greater fluctuations in diversity than do random clades, but the effect is not marked.
Many aspects of primate anatomy are associated with aspects of behavior or ecology. These associations can be used to reconstruct the behavior and ecology of fossil species known only from bones and teeth. Body size is correlated with many aspects of ecology and behavior, including diet, locomotion, and life history. Other anatomical features associated with dietary differences include feature of dental anatomy, and the proportions of the digestive system. Primates show several distinct types of locomotion, including arboreal quadrupedalism, terrestrial quadrupedalism, leaping, suspension, and bipedalism. Each of these is associated with details of the structure on the limbs and trunk. Differences in primate social behavior are associated with dimorphism of the canine teeth and body mass as well as features of the reproductive system.
Using computer simulations and analytic calculations, we have evaluated whether conspicuous expansions and contractions of natural clades may have represented chance fluctuations that occurred while probabilities of speciation and extinction remained equal and constant. Our results differ from those of previous workers, who have not scaled generating parameters empirically at the species level. We have found that the waxing and waning of many real clades have almost certainly resulted from changes in probabilities of speciation and extinction. For some of these changes, likely explanations are evident. The emplacement of adaptive innovations, for example, has at times elevated probability of speciation. We conclude that chance factors have not played a dominant role in producing dramatic changes in standing diversity within speciose higher taxa.
Phylogenies that are reconstructed without fossil material often contain approximate dates for lineage splitting. For example, particular nodes on molecular phylogenies may be dated by known geographic events that caused lineages to split, thereby calibrating a molecular clock that is used to date other nodes. On the one hand, such phylogenies contain no information about lineages that have become extinct. On the other hand, they do provide a potentially useful testing ground for ideas about evolutionary processes. Here we first ask what such reconstructed phylogenies should be expected to look like under a birth-death process in which the birth and death parameters of lineages remain constant through time. We show that it is possible to estimate both the birth and death rates of lineages from the reconstructed phylogenies, even though they contain no explicit information about extinct lineages. We also show how such phylogenies can reveal mass extinctions and how their characteristic footprint can be distinguished from similar ones produced by density-dependent cladogenesis.
Hollow curve distributions (HCDs) of taxonomic diversity are common in nature and are a result of assemblages being dominated by one or a few very diverse taxa. Models of random extinction and speciation can produce HCDs; however, the similarity between real and simulated HCDs has been examined previously only qualitatively. We compare quantitatively dominance observed in 85 real taxonomic assemblages to dominance predicted by five null models (1. Poisson; 2. Raup et al.'s [1973] simulation model; 3. Anderson and Anderson's [1975] simulation model; 4. simultaneous broken-stick; and 5. canonical lognormal distributions). Real assemblages were dominated to a significantly greater extent by one unit than predicted by all null models. This dominance is compounded as one proceeds down the taxonomic hierarchy. We demonstrate that overdominance is common whether phylogenetic or traditional classification schemes are used to assemble taxa. We propose that overdominance reflects real differences in the evolutionary success of units within an assemblage.
Equilibrium models in population biology have demonstrated that accurate predictions of species diversity can be made without reference to particular taxa. We have extended the use of equilibrium models to examine patterns of phyletic diversification in the fossil record. We assume that (1) regions become saturated with respect to the number of taxa that can coexist; and (2) after that limit is reached, rates of speciation and extinction are very similar. Using these minimal constraints, and the standard precepts of evolutionary taxonomy (monophyly), we have generated evolutionary trees by stochastic simulation and classified their lineages into clades. Random processes with minimal constraints yield phyletic trees similar to those based upon the fossil record. Of particular interest are the patterns of clade origination and extinction and of intraclade diversity. For comparison with computer simulations, we present actual clades for the Reptilia. The similarities are striking, but some patterns of the fossil record are not simulated by random processes. For example, the late Cretaceous extinction may represent a fundamentally different type of evolutionary event. The simulation program and its comparison with the real world permits a clearer separation of stochastic and deterministic elements in the evolutionary record.