The degree and pattern of phylogenetic signal in primate long-bone structure

Interspecific scaling is a fundamental tool for comparative studies of primate long-bone structure and adaptation. However, scaling analyses based on conventional statistical methods can lead to false positives regarding adaptive relationships when traits exhibit strong phylogenetic signal. This problem can be addressed through the use of phylogenetic comparative methods (PCMs). To date, PCMs have not been incorporated into comparative studies of primate long-bone structure because it has been assumed that long-bone structure is free of phylogenetic signal once appropriately scaled. To test this assumption, we evaluated the degree of phylogenetic signal in three types of long-bone structural traits (bone length, articular surface areas, and cross-sectional geometric properties) from 17 quadrupedal primate species. We compared the pattern of phylogenetic signal in raw trait values and residual trait values after regression against body mass, bone length, and the product of body mass x bone length. Our results show that significant phylogenetic signal is present in all traits before scaling, due in part to their strong covariance with body mass. After scaling, bone length still exhibits strong phylogenetic signal, but articular surface areas do not, and cross-sectional properties exhibit different levels of signal depending on the variable used to scale the data. These results suggest that PCMs should be incorporated into interspecific studies of bone length and perhaps cross-sectional geometric properties. Our results also demonstrate that tests for phylogenetic signal prior to implementing a PCM should focus on residual variance, not individual traits.     

The 10kTrees website: A new online resource for primate phylogeny

The comparative method plays a central role in efforts to uncover the adaptive basis for primate behaviors, morphological traits, and cognitive abilities. 1 - 4 The comparative method has been used, for example, to infer that living in a larger group selects for a larger neocortex, 5 , 6 that primate territoriality favors a longer day range relative to home range size, 7 and that sperm competition can account for the evolution of primate testes size. 8 , 9 Comparison is fundamental for reconstructing behavioral traits in the fossil record, for example, in studies of locomotion and diet. 10 - 13 Recent advances in comparative methods require phylogenetic information, 2 , 14 - 16 but our knowledge of phylogenetic information is imperfect. In the face of uncertainty about evolutionary relationships, which phylogeny should one use? Here we provide a new resource for comparative studies of primates that enables users to run comparative analyses on multiple primate phylogenies Importantly, the 10,000 trees that we provide are not random, but instead use recent systematic methods to create a plausible set of topologies that reflect our certainty about some nodes on the tree and uncertainty about other nodes, given the dataset. The trees also reflect uncertainty about branch lengths.     

The gray mouse lemur (Microcebus murinus) as a model for early primate brain evolution

The gray mouse lemur (Microcebus murinus), one of the world’s smallest primates, is thought to share a similar ecological niche and many anatomical traits with early euprimates. As a result, it has been considered a suitable model system for early primate physiology and behavior. Moreover, recent studies have demonstrated that mouse lemurs have comparable cognitive abilities and cortical functional organization as haplorhines. Finally, the small brain size of mouse lemurs provides us with actual lower limits for miniaturization of functional brain circuits within the primate clade. Considering its phylogenetic position and early primate-like traits, the mouse lemurs are a perfect model species to study the early evolution of primate brains.     

Behavioral Flexibility and the Evolution of Primate Social States

Comparative approaches to the evolution of primate social behavior have typically involved two distinct lines of inquiry. One has focused on phylogenetic analyses that treat social traits as static, species-specific characteristics; the other has focused on understanding the behavioral flexibility of particular populations or species in response to local ecological or demographic variables. Here, we combine these approaches by distinguishing between constraining traits such as dispersal regimes (male, female, or bi-sexual), which are relatively invariant, and responding traits such as grouping patterns (stable, fission-fusion, sometimes fission-fusion), which can reflect rapid adjustments to current conditions. Using long-term and cross-sectional data from 29 studies of 22 species of wild primates, we confirm that dispersal regime exhibits a strong phylogenetic signal in our sample. We then show that primate species with high variation in group size and adult sex ratios exhibit variability in grouping pattern (i.e., sometimes fission-fusion) with dispersal regime constraining the grouping response. When assessing demographic variation, we found a strong positive relationship between the variability in group size over time and the number of observation years, which further illustrates the importance of long-term demographic data to interpretations of social behavior. Our approach complements other comparative efforts to understand the role of behavioral flexibility by distinguishing between constraining and responding traits, and incorporating these distinctions into analyses of social states over evolutionary and ecological time.     

The Influence of Phylogeny on the Social Behaviour of Macaques (Primates: Cercopithecidae, genus Macaca)

The macaques are the most geographically widespread and behaviourally diverse primate genus. Many of the diversified features of social behaviour and organization in this genus have been attributed to socio-ecological differences. However, some core aspects of social behaviour and organization appear to be highly conservative, suggesting a high degree of phylogenetic inertia. A recently derived classification of macaque social organization, as well as a large range of social and physical traits, were analysed for 16 species to ascertain the role of phylogeny in explaining the distribution of these traits within the genus Macaca . These traits were mapped onto two alternative phylogenies. The pattern of social organization, based on the degree of asymmetry in social relations, exhibited a high and significant level of phylogenetic inertia, as did seven of the 22 individual traits compared. A profile constructed of the most likely ancestral state for this character matrix showed that it most closely resembles the pattern present in the Barbary macaque ( M. sylvanus ), which, based on both molecular and morphological data, most closely resembles the ancestral macaque.     

THE QUANTITATIVE ASSESSMENT OF PHYLOGENETIC CONSTRAINTS IN COMPARATIVE ANALYSES: SEXUAL DIMORPHISM IN BODY WEIGHT AMONG PRIMATES

We have presented a formal model for the quantitative analysis of phylogenetic and specific effects on the distribution of trait values among species. Total trait values are divided into phylogenetic values, inherited from an ancestral species, and specific values, the result of independent evolution. This allows a quantitative assessment of the strength of the phylogenetic inertia, or burden, displayed by a character in a lineage, so that questions concerning the relative importance of phylogenetic constraints in evolution can be answered. The separation of phylogenetic from specific effects proposed here also allows phylogenetic factors to be explicitly included in cross-species comparative analyses of adaptation. This solves a long-standing problem in evolutionary comparative studies. Only species' specific values can provide information concerning the independent evolution of characters in a set of related species. Therefore, only correlations among specific values for traits may be used as evidence for adaptation in cross-species comparative analyses. The phylogenetic autocorrelation model was applied to a comparative analysis of the determinants of sexual dimorphism in weight among 44 primate species. In addition to sexual dimorphism in weight, mating system, habitat, diet, and size (weight itself) were included in the analysis. All of the traits, except diet, were substantially influenced by phylogenetic inertia. The comparative analysis of the determinants of sexual dimorphism in weight indicates that 50% of the variation among primate species is due to phylogeny. Size, or scaling, could account for a total of 36% of the variance, making it almost as important as phylogeny in determining the level of dimorphism displayed by a species. Habitat, mating system, and diet follow, accounting for minor amounts of variation. Thus, in attempting to explain why a particular modern primate species is very dimorphic compared to other primates, we would say first because its ancestor was more dimorphic than average, second because it is a relatively large species, and third because it is terrestrial, polygynous, and folivorous.     

Linking the investigations of character evolution and species diversification

Variation in diversification rates is often studied by investigating traits related to species' ecology and life history. Often, however, it is unknown whether these traits evolve gradually or in punctuated bursts during speciation. Using phylogenetic data and species' present-day trait information, we present a novel approach to assessing the mode of character change while accounting for trait-dependent speciation and extinction. Our model, "Binary-State Speciation and Extinction-node enhanced state shift" (BiSSE-ness), estimates both the rate of change occurring along lineages and the probability of change occurring during speciation, as well as independent speciation and extinction rates for each character state. Using simulations, we found that BiSSE-ness is able to distinguish along-lineage and speciational change and accurately estimate the parameters associated with character change and diversification rates. We applied BiSSE-ness to an empirical primate data set and found evidence for along-lineage changes in primate mating systems and social behaviors, whereas shifts in habitat were associated with speciation. In cases where trait changes may be linked to the speciation process itself (e.g., niche-related traits), BiSSE-ness provides a suitable framework with which to simultaneously address questions regarding species diversification and character change.     

Primate Fruit Color: Useful Concept or Alluring Myth?

While the importance of frugivorous primates as seed dispersers is well established, the question of the extent to which they exert selective pressure on fruit color phenotypes is contested. Numerous studies have identified suites of primate fruit colors, but the lack of agreement among them illustrates the difficulty of identifying the match between primate foraging behavior and the extent of primate–plant coevolution. This may indicate that primates do not shape fruit traits, at least in a consistent direction, or that the evolution of fruit color is affected by a complex array of selection pressures in which primates play only a part. Here, we review the role of primates in shaping fruit color in the context of primate color vision phenotypes, and fruit phenotypic constraints and selective pressures. To test the hypothesis that fruit color is subjected to selection pressures by primates, we offer six testable predictions aimed at disentangling the complex array of factors that can contribute to fruit color phenotypes, including animal mutualists, animal antagonists, and developmental and phylogenetic constraints of fruits. We conclude that identifying the importance of primate seed dispersers in shaping fruit visual traits is possible, but more complex than previously thought.     

Effects of the distribution of female primates on the number of males

The spatiotemporal distribution of females is thought to drive variation in mating systems, and hence plays a central role in understanding animal behavior, ecology and evolution. Previous research has focused on investigating the links between female spatiotemporal distribution and the number of males in haplorhine primates. However, important questions remain concerning the importance of spatial cohesion, the generality of the pattern across haplorhine and strepsirrhine primates, and the consistency of previous findings given phylogenetic uncertainty. To address these issues, we examined how the spatiotemporal distribution of females influences the number of males in primate groups using an expanded comparative dataset and recent advances in bayesian phylogenetic and statistical methods. Specifically, we investigated the effect of female distributional factors (female number, spatial cohesion, estrous synchrony, breeding season duration and breeding seasonality) on the number of males in primate groups. Using bayesian approaches to control for uncertainty in phylogeny and the model of trait evolution, we found that the number of females exerted a strong influence on the number of males in primate groups. In a multiple regression model that controlled for female number, we found support for temporal effects, particularly involving female estrous synchrony: the number of males increases when females are more synchronously receptive. Similarly, the number of males increases in species with shorter birth seasons, suggesting that greater breeding seasonality makes defense of females more difficult for male primates. When comparing primate suborders, we found only weak evidence for differences in traits between haplorhines and strepsirrhines, and including suborder in the statistical models did not affect our conclusions or give compelling evidence for different effects in haplorhines and strepsirrhines. Collectively, these results demonstrate that male monopolization is driven primarily by the number of females in groups, and secondarily by synchrony of female reproduction within groups.     

Primate phylogeny: molecular evidence from retroposons

In these postgenomic times where aspects of functional genetics and character evolution form a focal point of human-mouse comparative research, primate phylogenetic research gained a widespread interest in evolutionary biology. Nevertheless, it also remains a controversial subject. Despite the surge in available primate sequences and corresponding phylogenetic interpretations, primate origins as well as several branching events in primate divergence are far from settled. The analysis of SINEs - short interspersed elements - as molecular cladistic markers represents a particularly interesting complement to sequence data. The following summarizes and discusses potential applications of this new approach in molecular phylogeny and outlines main results obtained with SINEs in the context of primate evolutionary research. Another molecular cladistic marker linking the tarsier with the anthropoid primates is also presented. This eliminates any possibility of confounding phylogenetic interpretations through lineage sorting phenomena and makes use of a new point of view in settling the phylogenetic relationships of the primate infraorders.     

The evolution of virulence and host specialization in malaria parasites of primates

Parasite virulence, i.e. the damage done to the host, may be a by-product of the parasite's effort to maximize its fitness. Accordingly, several life-history trade-offs may explain interspecific differences in virulence, but such constraints remain little tested in an evolutionary context. In this phylogenetic study of primate malarias, I investigated the relationship between virulence and other parasite life-history traits. I used peak parasitaemia as a proxy for virulence, because it reflected parasite reproductive success and parasite-induced mortality. Peak parasitaemia was higher in specialist than in generalist species, even when confounding life-history traits were controlled. While there was a significant phylogenetic relationship between the number of competitors per host and host specialization, peak parasitaemia was unrelated to within-host competition. Therefore, the key evolutionary factor that favours virulence is host specialization, and the evolutionary success of virulent parasites, such as Plasmodium falciparum , may be better understood when the trade-off in virulence between different hosts is considered. Such phylogenetic results may help us design better protection programmes against malaria.     

Common Ancestry Is a Poor Predictor of Competitive Traits in Freshwater Green Algae

Phytoplankton species traits have been used to successfully predict the outcome of competition, but these traits are notoriously laborious to measure. If these traits display a phylogenetic signal, phylogenetic distance (PD) can be used as a proxy for trait variation. We provide the first investigation of the degree of phylogenetic signal in traits related to competition in freshwater green phytoplankton. We measured 17 traits related to competition and tested whether they displayed a phylogenetic signal across a molecular phylogeny of 59 species of green algae. We also assessed the fit of five models of trait evolution to trait variation across the phylogeny. There was no significant phylogenetic signal for 13 out of 17 ecological traits. For 7 traits, a non-phylogenetic model provided the best fit. For another 7 traits, a phylogenetic model was selected, but parameter values indicated that trait variation evolved recently, diminishing the importance of common ancestry. This study suggests that traits related to competition in freshwater green algae are not generally well-predicted by patterns of common ancestry. We discuss the mechanisms by which the link between phylogenetic distance and phenotypic differentiation may be broken.     

Comparative histomorphology of intrinsic vibrissa musculature among primates: implications for the evolution of sensory ecology and “face touch”

Macrovibrissae are specialized tactile sensory hairs present in most mammalian orders, used in maxillary mechanoreception or “face touch.” Some mammals have highly organized vibrissae and are able to “whisk” them. Movement of vibrissae is influenced by intrinsic vibrissa musculature, striated muscle bands that attach directly to the vibrissa capsule. It is unclear if primates have organized vibrissae or intrinsic vibrissa musculature and it is uncertain if they can move their vibrissae. The present study used histomorphological techniques to compare vibrissae among 19 primates and seven non‐primate mammalian taxa. Upper lips of these mammals were sectioned and processed for histochemical analysis. While controlling for phylogenetic effects the following hypotheses were tested: 1) mammals with well‐organized vibrissae possess intrinsic vibrissa musculature and 2) intrinsic vibrissa musculature is best developed in nocturnal, arboreal taxa. Our qualitative analyses show that only arboreal, nocturnal prosimians possess intrinsic musculature. Not all taxa that possessed organized vibrissae had intrinsic vibrissa musculature. Phylogenetic comparative analyses revealed a 70% probability that stem mammals, primates, and haplorhines possessed intrinsic vibrissa musculature and well‐organized vibrissae. These two traits most likely coevolved according to a discrete phylogenetic analysis. These results indicate that nocturnal, arboreal primates have the potential to more actively use their vibrissae in spatial recognition and navigation tasks than diurnal, more terrestrial species, but there is a clear phylogenetic signal involved in the evolution of primate vibrissae and “face touch.” Am J Phys Anthropol, 2013. © 2012 Wiley Periodicals, Inc.     

Human genetic disorders, a phylogenetic perspective

When viewed from the perspective of time, human genetic disorders give new insights into their etiology and evolution. Here, we have correlated a specific set of Alu repetitive DNA elements, known to be the basis of certain genetic defects, with their phylogenetic roots in primate evolution. From a differential distribution of Alu repeats among primate species, we identify the phylogenetic roots of three human genetic diseases involving the LPL, ApoB, and HPRT genes. The different phylogenetic age of these genetic disorders could explain the different susceptibility of various primate species to genetic diseases. Our results show that LPL deficiency is the oldest and should affect humans, apes, and monkeys. ApoB deficiency should affect humans and great apes, while a disorder in the HPRT gene (leading to the Lesch-Nyhan syndrome) is unique to human, chimpanzee, and gorilla. Similar results can be obtained for cancer. We submit that de novo transpositions of Alu elements, and saltatory appearances of Alu-mediated genetic disorders, represent singularities, places where behavior changes suddenly. Alus' propensity to spread, not only increased the regulatory and developmental complexity of the primate genome, it also increased its instability and susceptibility to genetic defects and cancer. The dynamic spread not only provided markers of primate phylogeny, it must have actively shaped the course of that phylogeny.     

A tooth crown morphology framework for interpreting the diversity of primate dentitions

Variation in tooth crown morphology plays a crucial role in species diagnoses, phylogenetic inference, and the reconstruction of the evolutionary history of the primate clade. While a growing number of studies have identified developmental mechanisms linked to tooth size and cusp patterning in mammalian crown morphology, it is unclear (1) to what degree these are applicable across primates and (2) which additional developmental mechanisms should be recognized as playing important roles in odontogenesis. From detailed observations of lower molar enamel–dentine junction morphology from taxa representing the major primate clades, we outline multiple phylogenetic and developmental components responsible for crown patterning, and formulate a tooth crown morphology framework for the holistic interpretation of primate crown morphology. We suggest that adopting this framework is crucial for the characterization of tooth morphology in studies of dental development, discrete trait analysis, and systematics.     

Coevolutionary relationship between striatum size and social play in nonhuman primates

The striatum is a region of the brain specifically tied to the experience and anticipation of pleasure, reward, appropriate behavioral sequencing, cognition, learning, and social modulation. Furthermore, the striatum is connected neurologically and functionally to other brain regions associated with the exhibition of social play, such as the neocortex, cerebellum, and limbic system. For these reasons, the striatum is especially interesting to researchers of play behavior. Moreover, the caudate-putamen area of the striatum has been specifically implicated in laboratory studies of social play behavior. This study uses the phylogenetic comparative method of independent contrasts to test for an evolutionary relationship between striatum volume and a measure of social play in nonhuman primates. Relative volume of the primate striatum correlates with rate of social, but not nonsocial, play behavior across species, suggesting a coevolution of traits. The pleasurable and procedural aspects of social play behavior may be mediated in part by the striatum and further to its connection to dopaminergic pathways in the primate brain.     

A mobile element based phylogeny of Old World monkeys

SINEs (Short INterspersed Elements) are a class of non-autonomous mobile elements that are <500 bp in length and have no open reading frames. Individual SINE elements are essentially homoplasy free with known ancestral states, making them useful genetic systems for phylogenetic studies. Alu elements are the most successful SINE in primate genomes and have been utilized for resolving primate phylogenetic relationships and human population genetics. However, no Alu based phylogenetic analysis has yet been performed to resolve relationships among Old World monkeys. Using both a computational approach and polymerase chain reaction display methodology, we identified 285 new Alu insertions from sixteen Old World monkey taxa that were informative at various levels of catarrhine phylogeny. We have utilized these elements along with 12 previously reported loci to construct a phylogenetic tree of the selected taxa. Relationships among all major clades are in general agreement with other molecular and morphological data sets but have stronger statistical support.     

The Use (and Misuse) of Phylogenetic Trees in Comparative Behavioral Analyses

Phylogenetic comparative methods play a critical role in our understanding of the adaptive origin of primate behaviors. To incorporate evolutionary history directly into comparative behavioral research, behavioral ecologists rely on strong, well-resolved phylogenetic trees. Phylogenies provide the framework on which behaviors can be compared and homologies can be distinguished from similarities due to convergent or parallel evolution. Phylogenetic reconstructions are also of critical importance when inferring the ancestral state of behavioral patterns and when suggesting the evolutionary changes that behavior has undergone. Improvements in genome sequencing technologies have increased the amount of data available to researchers. Recently, several primate phylogenetic studies have used multiple loci to produce robust phylogenetic trees that include hundreds of primate species. These trees are now commonly used in comparative analyses and there is a perception that we have a complete picture of the primate tree. But how confident can we be in those phylogenies? And how reliable are comparative analyses based on such trees? Herein, we argue that even recent molecular phylogenies should be treated cautiously because they rely on many assumptions and have many shortcomings. Most phylogenetic studies do not model gene tree diversity and can produce misleading results, such as strong support for an incorrect species tree, especially in the case of rapid and recent radiations. We discuss implications that incorrect phylogenies can have for reconstructing the evolution of primate behaviors and we urge primatologists to be aware of the current limitations of phylogenetic reconstructions when applying phylogenetic comparative methods.     

Distribution, ecology, life history, genetic variation, and risk of extinction of nonhuman primates from Costa Rica

We examined the association between geographic distribution, ecological traits, life history, genetic diversity, and risk of extinction in nonhuman primate species from Costa Rica. All of the current nonhuman primate species from Costa Rica are included in the study; spider monkeys (Ateles geoffroyi), howling monkeys (Alouatta palliata), capuchins (Cebus capucinus), and squirrel monkeys (Saimiri oerstedii). Geographic distribution was characterized accessing existing databases. Data on ecology and life history traits were obtained through a literature review. Genetic diversity was characterized using isozyme electrophoresis. Risk of extinction was assessed from the literature. We found that species differed in all these traits. Using these data, we conducted a Pearson correlation between risk of extinction and ecological and life history traits, and genetic variation, for widely distributed species. We found a negative association between risk of extinction and population birth and growth rates; indicating that slower reproducing species had a greater risk of extinction. We found a positive association between genetic variation and risk of extinction; i.e., species showing higher genetic variation had a greater risk of extinction. The relevance of these traits for conservation efforts is discussed.     

Primate phylogenomics uncovers multiple rapid radiations and ancient interspecific introgression

Our understanding of the evolutionary history of primates is undergoing continual revision due to ongoing genome sequencing efforts. Bolstered by growing fossil evidence, these data have led to increased acceptance of once controversial hypotheses regarding phylogenetic relationships, hybridization and introgression, and the biogeographical history of primate groups. Among these findings is a pattern of recent introgression between species within all major primate groups examined to date, though little is known about introgression deeper in time. To address this and other phylogenetic questions, here, we present new reference genome assemblies for 3 Old World monkey (OWM) species: Colobus angolensis ssp. palliatus (the black and white colobus), Macaca nemestrina (southern pig-tailed macaque), and Mandrillus leucophaeus (the drill). We combine these data with 23 additional primate genomes to estimate both the species tree and individual gene trees using thousands of loci. While our species tree is largely consistent with previous phylogenetic hypotheses, the gene trees reveal high levels of genealogical discordance associated with multiple primate radiations. We use strongly asymmetric patterns of gene tree discordance around specific branches to identify multiple instances of introgression between ancestral primate lineages. In addition, we exploit recent fossil evidence to perform fossil-calibrated molecular dating analyses across the tree. Taken together, our genome-wide data help to resolve multiple contentious sets of relationships among primates, while also providing insight into the biological processes and technical artifacts that led to the disagreements in the first place.

Combining three newly sequenced primate genomes with other published genomes, this study adapts a little-known method for detecting ancient introgression to genome-scale data, revealing multiple previously unknown examples of hybridization between primate species.