Luke J. Matthews

How does cognition evolve? Phylogenetic comparative psychology

Now more than ever animal studies have the potential to test hypotheses regarding how cognition evolves. Comparative psychologists have developed new techniques to probe the cognitive mechanisms underlying animal behavior, and they have become increasingly skillful at adapting methodologies to test multiple species. Meanwhile, evolutionary biologists have generated quantitative approaches to investigate the phylogenetic distribution and function of phenotypic traits, including cognition. In particular, phylogenetic methods can quantitatively (1) test whether specific cognitive abilities are correlated with life history (e.g., lifespan), morphology (e.g., brain size), or socio-ecological variables (e.g., social system), (2) measure how strongly phylogenetic relatedness predicts the distribution of cognitive skills across species, and (3) estimate the ancestral state of a given cognitive trait using measures of cognitive performance from extant species. Phylogenetic methods can also be used to guide the selection of species comparisons that offer the strongest tests of a priori predictions of cognitive evolutionary hypotheses (i.e., phylogenetic targeting). Here, we explain how an integration of comparative psychology and evolutionary biology will answer a host of questions regarding the phylogenetic distribution and history of cognitive traits, as well as the evolutionary processes that drove their evolution.

Novelty‐seeking DRD4 polymorphisms are associated with human migration distance out‐of‐Africa after controlling for neutral population gene structure

Numerous lines of evidence suggest that Homo sapiens evolved as a distinct species in Africa by 150,000 years before the present (BP) and began major migrations out-of-Africa ∼50,000 BP. By 20,000 BP, our species had effectively colonized the entire Old World, and by 12,000 BP H. sapiens had a global distribution. We propose that this rapid migration into new habitats selected for individuals with low reactivity to novel stressors. Certain dopamine receptor D4 (DRD4) polymorphisms are associated with low neuronal reactivity and increased exploratory behavior, novelty seeking, and risk taking, collectively considered novelty-seeking trait (NS). One previous report (Chen et al.: Evol Hum Behav 20 (1999) 309-324) demonstrated a correlation between migratory distance and the seven-repeat (7R) VNTR DRD4 allele at exon 3 for human populations. This study, however, failed to account for neutral genetic processes (drift and admixture) that might create such a correlation in the absence of natural selection. Furthermore, additional loci surrounding DRD4 are now recognized to influence NS. Herein we account for neutral genetic structure by modeling the nonindependence of neutral allele frequencies between human populations. We retest the DRD4 exon 3 alleles, and also test two other loci near DRD4 that are associated with NS. We conclude there is an association between migratory distance and DRD4 exon 3 2R and 7R alleles that cannot be accounted for by neutral genetic processes alone.

Simulating trait evolution for cross-cultural comparison

Cross-cultural anthropologists have increasingly used phylogenetic methods to study cultural variation. Because cultural behaviours can be transmitted horizontally among socially defined groups, however, it is important to assess whether phylogeny-based methods—which were developed to study vertically transmitted traits among biological taxa—are appropriate for studying group-level cultural variation. Here, we describe a spatially explicit simulation model that can be used to generate data with known degrees of horizontal donation. We review previous results from this model showing that horizontal transmission increases the type I error rate of phylogenetically independent contrasts in studies of correlated evolution. These conclusions apply to cases in which two traits are transmitted as a pair, but horizontal transmission may be less problematic when traits are unlinked. We also use the simulation model to investigate whether measures of homology (the consistency index and the retention index) can detect horizontal transmission of cultural traits. Higher rates of evolutionary change have a stronger depressive impact on measures of homology than higher rates of horizontal transmission; thus, low consistency or retention indices are not necessarily indicative of ‘ethnogenesis’. Collectively, these studies demonstrate the importance of using simulations to assess the validity of methods in cross-cultural research.

Testing for Divergent Transmission Histories among Cultural Characters: A Study Using Bayesian Phylogenetic Methods and Iranian Tribal Textile Data

Background Archaeologists and anthropologists have long recognized that different cultural complexes may have distinct descent histories, but they have lacked analytical techniques capable of easily identifying such incongruence. Here, we show how Bayesian phylogenetic analysis can be used to identify incongruent cultural histories. We employ the approach to investigate Iranian tribal textile traditions. Methods We used Bayes factor comparisons in a phylogenetic framework to test two models of cultural evolution: the hierarchically integrated system hypothesis and the multiple coherent units hypothesis. In the hierarchically integrated system hypothesis, a core tradition of characters evolves through descent with modification and characters peripheral to the core are exchanged among contemporaneous populations. In the multiple coherent units hypothesis, a core tradition does not exist. Rather, there are several cultural units consisting of sets of characters that have different histories of descent. Results For the Iranian textiles, the Bayesian phylogenetic analyses supported the multiple coherent units hypothesis over the hierarchically integrated system hypothesis. Our analyses suggest that pile-weave designs represent a distinct cultural unit that has a different phylogenetic history compared to other textile characters. Conclusions The results from the Iranian textiles are consistent with the available ethnographic evidence, which suggests that the commercial rug market has influenced pile-rug designs but not the techniques or designs incorporated in the other textiles produced by the tribes. We anticipate that Bayesian phylogenetic tests for inferring cultural units will be of great value for researchers interested in studying the evolution of cultural traits including language, behavior, and material culture.

Primate Extinction Risk and Historical Patterns of Speciation and Extinction in Relation to Body Mass

Body mass is thought to influence diversification rates, but previous studies have produced ambiguous results. We investigated patterns of diversification across 100 trees obtained from a new Bayesian inference of primate phylogeny that sampled trees in proportion to their posterior probabilities. First, we used simulations to assess the validity of previous studies that used linear models to investigate the links between IUCN Red List status and body mass. These analyses support the use of linear models for ordinal ranked data on threat status, and phylogenetic generalized linear models revealed a significant positive correlation between current extinction risk and body mass across our tree block. We then investigated historical patterns of speciation and extinction rates using a recently developed maximum-likelihood method. Specifically, we predicted that body mass correlates positively with extinction rate because larger bodied organisms reproduce more slowly, and body mass correlates negatively with speciation rate because smaller bodied organisms are better able to partition niche space. We failed to find evidence that extinction rates covary with body mass across primate phylogeny. Similarly, the speciation rate was generally unrelated to body mass, except in some tests that indicated an increase in the speciation rate with increasing body mass. Importantly, we discovered that our data violated a key assumption of sample randomness with respect to body mass. After correcting for this bias, we found no association between diversification rates and mass.

Anointing variation across wild capuchin populations: a review of material preferences, bout frequency and anointing sociality in Cebus and Sapajus

The frequency of anointing bouts and the materials used for self‐ and social anointing vary across capuchin species in captivity, but there is little published data on capuchin anointing in the wild. Here we present previously unpublished data on anointing behaviors from capuchin monkey populations at ten different field sites and incorporate these data into a review of the anointing literature for captive and wild capuchins. Using a comparative phylogenetic framework, we test four hypotheses derived primarily from captive literature for variation in anointing between wild untufted capuchins (Cebus) and tufted capuchins (Sapajus), including that (1) the frequency of anointing is higher in Cebus, (2) Cebus uses a higher proportion of plant species to insect species for anointing compared with Sapajus, (3) anointing material diversity is higher in Cebus, and (4) social indices of anointing are higher in Cebus. We found that wild Cebus anoints more with plant parts, including fruits, whereas wild Sapajus anoints more with ants and other arthropods. Cebus capucinus in particular uses more plant species per site for anointing compared with other capuchins and may specialize in anointing as an activity independent from foraging, whereas most other capuchin species tend to eat the substances they use for anointing. In agreement with captive studies, we found evidence that wild Cebus anoints at a significantly higher frequency than Sapajus. However, contrary to the captive literature, we found no difference in the range of sociality for anointing between Cebus and Sapajus in the wild. We review anointing in the context of other Neotropical primate rubbing behaviors and consider the evidence for anointing as self‐medication; as a mechanism for enhanced sociality; and as a behavioral response to chemical stimuli. Am. J. Primatol. 74:299–314, 2012.

Evolutionary disequilibrium and activity period in primates: A bayesian phylogenetic approach

Activity period plays a central role in studies of primate origins and adaptations, yet fundamental questions remain concerning the evolutionary history of primate activity period. Lemurs are of particular interest because they display marked variation in activity period, with some species exhibiting completely nocturnal or diurnal lifestyles, and others distributing activity throughout the 24-h cycle (i.e., cathemerality). Some lines of evidence suggest that cathemerality in lemurs is a recent and transient evolutionary state (i.e., the evolutionary disequilibrium hypothesis), while other studies indicate that cathemerality is a stable evolutionary strategy with a more ancient history. Debate also surrounds activity period in early primate evolution, with some recent studies casting doubt on the traditional hypothesis that basal primates were nocturnal. Here, we used Bayesian phylogenetic methods to reconstruct activity period at key points in primate evolution. Counter to the evolutionary disequilibrium hypothesis, the most recent common ancestor of Eulemur was reconstructed as cathemeral at ∼9-13 million years ago, indicating that cathemerality in lemurs is a stable evolutionary strategy. We found strong evidence favoring a nocturnal ancestor for all primates, strepsirrhines and lemurs, which adds to previous findings based on parsimony by providing quantitative support for these reconstructions. Reconstructions for the haplorrhine ancestor were more equivocal, but diurnality was favored for simian primates. We discuss the implications of our models for the evolutionary disequilibrium hypothesis, and we identify avenues for future research that would provide new insights into the evolution of cathemerality in lemurs.

Activity Patterns, Home Range Size, and Intergroup Encounters in Cebus albifrons Support Existing Models of Capuchin Socioecology

Variation in ranging behavior, social organization, and feeding ecology among capuchins (Cebus spp.) is a classic example of how closely related species may be differentially adapted to their local environments. Marked differences in all 3 areas occur among Cebus spp. between the untufted capuchins (Cebus capucinus, C. olivaceous, and C. albifrons) and the tufted capuchins (C. apella, C. xanthosternos, C. nigritus, and C. libidinosus). The key socioecological distinction between the 2 groups has traditionally been that, compared with the tufted group, untufted capuchins eat more ripe foods, as befits their more gracile masticatory system; range more broadly in search of high-quality foods; and live in larger groups with more males and more agonistic interactions between groups. Here I assess how well the basic socioecological characteristics —activity budget, ranging— of previously unstudied Ecuadorian Cebus albifrons fit within this model. Few researchers have conducted studies on Cebus albifrons, despite its prominent role in the initial development of the model for socioecology of Cebus. The results of my 1-yr study of a single social group support the model’s general characterization of untufted capuchins in ranging and feeding behaviors, but also suggest that direct ecological and demographic effects, in addition to adaptation to local conditions, may explain additional variation in group size across species of Cebus.

Cultural inheritance or cultural diffusion of religious violence? A quantitative case study of the Radical Reformation

Abstract Religion throughout the historical record is consistently associated with large-scale cooperative activities. These cooperative activities sometimes involve coordinated acts of violence, particularly against religious out-groups. Using phylogenetic and social network analyses, we investigated whether religious violence is inherited from parent congregations or is acquired from contemporaneous purveyors of violent ideologies. We examined these questions among sixteenth-century Anabaptists, who constitute a prominent historical system with both violent and pacifist congregations. We found that ideology advocating violence was typically inherited from parent congregations, while the majority of other theological traits spread among contemporaneous groups. Violent ideology may be learned independently from most other characteristics of an overall belief system, and/or it may be determined more by congregationally inherited economic and political factors than by theology.

Variations in sexual behavior among capuchin monkeys function for conspecific mate recognition: a phylogenetic analysis and a new hypothesis for female proceptivity in tufted capuchins

Researchers of capuchin monkeys have noted stereotyped body postures, facial expressions, and vocalizations that accompany copulations in this genus. Notable variations in these sexual behaviors are observed across capuchin species. Although several hypotheses exist to explain variation in the duration and vigor of sexual behaviors across species, there is no proposed explanation for variation in the forms of these behaviors. I hypothesized that the forms of sexual behaviors function as recognition signals of conspecific mates. Such signals are adaptive when F1 hybrids exhibit reduced fitness compared with nonhybrid offspring. Recent evidence from nonprimate taxa supports the existence of species recognition signals during mating. Using newly observed sexual behaviors for Cebus albifrons and a recent phylogeny of capuchins, I found significant support for a key prediction of the conspecific mate recognition hypothesis: evolutionary changes in sexual behaviors were associated with speciation. Given the resultant best model for evolution of sexual behaviors, I reconstructed the ancestral pattern of sexual behaviors for extant capuchin species (genera Cebus and Sapajus). This reconstruction suggests that the extreme female proceptivity of tufted capuchin monkeys may function to increase female reproductive choices in the context of sperm‐limited males (genus Sapajus). Am. J. Primatol. 74:287–298, 2012.