Jason M. Kamilar

Phylogenetic signal in primate behaviour, ecology and life history.

Examining biological diversity in an explicitly evolutionary context has been the subject of research for several decades, yet relatively recent advances in analytical techniques and the increasing availability of species-level phylogenies, have enabled scientists to ask new questions. One such approach is to quantify phylogenetic signal to determine how trait variation is correlated with the phylogenetic relatedness of species. When phylogenetic signal is high, closely related species exhibit similar traits, and this biological similarity decreases as the evolutionary distance between species increases. Here, we first review the concept of phylogenetic signal and suggest how to measure and interpret phylogenetic signal in species traits. Second, we quantified phylogenetic signal in primates for 31 variables, including body mass, brain size, life-history, sexual selection, social organization, diet, activity budget, ranging patterns and climatic variables. We found that phylogenetic signal varies extensively across and even within trait categories. The highest values are exhibited by brain size and body mass, moderate values are found in the degree of territoriality and canine size dimorphism, while low values are displayed by most of the remaining variables. Our results have important implications for the evolution of behaviour and ecology in primates and other vertebrates.

Environmental and phylogenetic correlates of Eulemur behavior and ecology (Primates: Lemuridae)

The extent of diversity within closely related taxa may be a function of their shared evolutionary history or of selective forces causing adaptive changes. Examining variation among taxa within a single genus may help to identify flexibility in trait variation because recently diverged populations are more likely living in the environment of adaptation. This study examines correlates of diversity in Eulemur, a genus that has a wide distribution in a variety of habitat types throughout Madagascar. Previously published data were gathered from 11 long-term studies of Eulemur populations. Variables were categorized into multiple datasets: (1) environmental characteristics, (2) social organization, and (3) ecology, which included subsets for ranging behavior, diet, and activity budget. Molecular phylogenies from the literature were used to create the fourth and final dataset, a dissimilarity matrix of evolutionary distance among the 12 species and subspecies. Principal components and cluster analyses were implemented to examine the overall ecological similarity among Eulemur populations and to determine which variables contribute most to the variation among taxa. Partial Mantel tests were conducted to test for correlations among the dataset matrices. The results suggest ecological flexibility for the genus, in particular, populations in similar environments displayed similar activity patterns. In contrast, social organization showed no relationship with environment but was correlated with phylogenetic distance among populations. While Eulemur seems to demonstrate some flexibility for ecological adaptations, characteristics related to group size and sex ratio more closely track phylogeny and thus may be less flexible.

Eye shape and the nocturnal bottleneck of mammals

Most vertebrate groups exhibit eye shapes that vary predictably with activity pattern. Nocturnal vertebrates typically have large corneas relative to eye size as an adaptation for increased visual sensitivity. Conversely, diurnal vertebrates generally demonstrate smaller corneas relative to eye size as an adaptation for increased visual acuity. By contrast, several studies have concluded that many mammals exhibit typical nocturnal eye shapes, regardless of activity pattern. However, a recent study has argued that new statistical methods allow eye shape to accurately predict activity patterns of mammals, including cathemeral species (animals that are equally likely to be awake and active at any time of day or night). Here, we conduct a detailed analysis of eye shape and activity pattern in mammals, using a broad comparative sample of 266 species. We find that the eye shapes of cathemeral mammals completely overlap with nocturnal and diurnal species. Additionally, most diurnal and cathemeral mammals have eye shapes that are most similar to those of nocturnal birds and lizards. The only mammalian clade that diverges from this pattern is anthropoids, which have convergently evolved eye shapes similar to those of diurnal birds and lizards. Our results provide additional evidence for a nocturnal ‘bottleneck’ in the early evolution of crown mammals.

Environmental and geographic correlates of the taxonomic structure of primate communities

Previous research has shown that both environmental and historical factors influence the taxonomic structure of animal communities; yet, the relative importance of these effects is not known for primates. Environmental characteristics shape the possible niches in a community, providing suitable habitats for some species and not others. Therefore, communities found in similar environments should display similar species compositions. Additionally, geography may be viewed as a surrogate for historical processes. For instance, as the geographic distance between communities increases, dispersal between sites is more limited, and the probability of historical vicariance increases. Therefore, communities in close proximity to each other should exhibit similar species compositions. The geographic location, environmental characteristics, and species composition of 168 primate communities were gathered from the literature. Canonical correspondence analyses were conducted to examine the relative effects of geographic distance and environmental variables on the taxonomic structure of communities. In addition, UPGMA cluster analyses were conducted to better visualize the taxonomic similarity of communities. Spatial variables were significant predictors of community structure in all regions. Rainfall patterns explained African, Malagasy, and Neotropical community structure. In addition, maximum temperature was also correlated with community structure in Madagascar and the Neotropics. No climatic variables predicted Asian community structure. These results demonstrate that both historical and environmental factors play a significant role in structuring modern primate communities; yet, the importance of environmental factors depend on the region in question.

The climatic niche diversity of malagasy primates: a phylogenetic perspective.

Background Numerous researchers have posited that there should be a strong negative relationship between the evolutionary distance among species and their ecological similarity. Alternative evidence suggests that members of adaptive radiations should display no relationship between divergence time and ecological similarity because rapid evolution results in near-simultaneous speciation early in the clades history. In this paper, we performed the first investigation of ecological diversity in a phylogenetic context using a mammalian adaptive radiation, the Malagasy primates. Methodology/Principal Findings We collected data for 43 extant species including: 1) 1064 species by locality samples, 2) GIS climate data for each sampling locality, and 3) the phylogenetic relationships of the species. We calculated the niche space of each species by summarizing the climatic variation at localities of known occurrence. Climate data from all species occurrences at all sites were entered into a principal components analysis. We calculated the mean value of the first two PCA axes, representing rainfall and temperature diversity, for each species. We calculated the K statistic using the Physig program for Matlab to examine how well the climatic niche space of species was correlated with phylogeny. Conclusions/Significance We found that there was little relationship between the phylogenetic distance of Malagasy primates and their rainfall and temperature niche space, i.e., closely related species tend to occupy different climatic niches. Furthermore, several species from different genera converged on a similar climatic niche. These results have important implications for the evolution of ecological diversity, and the long-term survival of these endangered species.

Species co‐occurrence patterns and dietary resource competition in primates

Diamond (Assembly of species communities. In: Cody ML, Diamond JM, editors. Ecology and evolution of communities. Cambridge: Belknap. p 342-444 (1975)) argued that interspecific competition between species occupying similar niches results in a nonrandom pattern of species distributions. In particular, some species pairs may never be found in the same community due to competitive exclusion. Rigorous analytical methods have been developed to investigate the possible role that interspecific competition has on the evolution of communities. Many studies that have implemented these methods have shown support for Diamonds assembly rules, yet there are numerous exceptions. We build on this previous research by examining the co-occurrence patterns of primate species in 109 communities from across the world. We used EcoSim to calculate a checkerboard (C) score for each region. The C score provides a measure of the proportion of species pairs that do not co-occur in a set of communities. High C scores indicate that species are nonrandomly distributed throughout a region, and interspecific competition may be driving patterns of competitive exclusion. We conducted two sets of analyses. One included all primate species per region, and the second analysis assigned each species to one of four dietary guilds: frugivores, folivores, insectivores, and frugivore-insectivores. Using all species per region, we found significantly high C scores in 9 of 10 regions examined. For frugivores, we found significantly high-C scores in more than 50% of regions. In contrast, only 23% of regions exhibited significantly high-C scores for folivores. Our results suggest that communities are nonrandomly structured and may be the result of greater levels of interspecific competition between frugivores compared to folivores.

Examining the extinction risk of specialized folivores: a comparative study of Colobine monkeys.

Species extinctions are nonrandom with some taxa appearing to possess traits that increase their extinction risk. In this study, eight predictors of extinction risk were used as independent variables to predict the IUCN category of a subfamily of specialized folivorous primates, the Colobinae. All data were transformed into phylogenetically independent contrasts and were analyzed using bivariate regressions, multiple regression, and a maximum likelihood approach using Akaikes Information Criterion to assess model performance. Once an outlier was removed from the data set, species that devote a smaller proportion of their diet to mature leaf consumption appear to be at a greater risk of extinction. Also, as female body mass increases, so does extinction risk. In contrast, as maximum latitude and the number of habitat types increase, extinction risk appears to decrease. These findings emphasize the importance of examining detailed dietary variation for predicting extinction risk at a relatively fine taxonomic scale and, consequently, may help improve conservation management. Am. J. Primatol. 70:816–827, 2008.

Host longevity and parasite species richness in mammals.

Hosts and parasites co-evolve, with each lineage exerting selective pressures on the other. Thus, parasites may influence host life-history characteristics, such as longevity, and simultaneously host life-history may influence parasite diversity. If parasite burden causes increased mortality, we expect a negative association between host longevity and parasite species richness. Alternatively, if long-lived species represent a more stable environment for parasite establishment, host longevity and parasite species richness may show a positive association. We tested these two opposing predictions in carnivores, primates and terrestrial ungulates using phylogenetic comparative methods and controlling for the potentially confounding effects of sampling effort and body mass. We also tested whether increased host longevity is associated with increased immunity, using white blood cell counts as a proxy for immune investment. Our analyses revealed weak relationships between parasite species richness and longevity. We found a significant negative relationship between longevity and parasite species richness for ungulates, but no significant associations in carnivores or primates. We also found no evidence for a relationship between immune investment and host longevity in any of our three groups. Our results suggest that greater parasite burden is linked to higher host mortality in ungulates. Thus, shorter-lived ungulates may be more vulnerable to disease outbreaks, which has implications for ungulate conservation, and may be applicable to other short-lived mammals.

Testing Bergmann's rule and the resource seasonality hypothesis in Malagasy primates using GIS-based climate data

We tested four major hypotheses on the ecological aspects of body mass variation in extant Malagasy strepsirrhines: thermoregulation, resource seasonality/scarcity, resource quality, and primary productivity. These biogeographic hypotheses focus on the ecological aspects of body mass variation, largely ignoring the role of phylogeny for explaining body mass variation within lineages. We tested the independent effects of climate and resource-related variables on variation in body mass among Malagasy primates using recently developed comparative methods that account for phylogenetic history and spatial autocorrelation. We extracted data on lemur body mass and climate variables for a total of 43 species from 39 sites. Climatic data were obtained from the WorldClim database, which is based on climate data from weather stations compiled around the world. Using generalized linear models that incorporate parameters to account for phylogenetic and spatial autocorrelation, we found that diet and climate variables were weak predictors of lemur body mass. Moreover, there was a strong phylogenetic effect relative to the effects of space on lemur body mass in all models. Thus, we failed to find support for any of the four hypotheses on patterns of geography and body mass in extant strepsirrhines. Our results indicate that body mass has been conserved since early in the evolutionary history of each genus, while species diversified into different environmental niches. Our findings are in contrast to some previous studies that have suggested resource and climate related effects on body mass, though these studies have examined this question at different taxonomic and/or geographic scales.

RUNX2 tandem repeats and the evolution of facial length in placental mammals

BackgroundWhen simple sequence repeats are integrated into functional genes, they can potentially act as evolutionary ‘tuning knobs’, supplying abundant genetic variation with minimal risk of pleiotropic deleterious effects. The genetic basis of variation in facial shape and length represents a possible example of this phenomenon. Runt-related transcription factor 2 (RUNX2), which is involved in osteoblast differentiation, contains a functionally-important tandem repeat of glutamine and alanine amino acids. The ratio of glutamines to alanines (the QA ratio) in this protein seemingly influences the regulation of bone development. Notably, in domestic breeds of dog, and in carnivorans in general, the ratio of glutamines to alanines is strongly correlated with facial length.ResultsIn this study we examine whether this correlation holds true across placental mammals, particularly those mammals for which facial length is highly variable and related to adaptive behavior and lifestyle (e.g., primates, afrotherians, xenarthrans). We obtained relative facial length measurements and RUNX2 sequences for 41 mammalian species representing 12 orders. Using both a phylogenetic generalized least squares model and a recently-developed Bayesian comparative method, we tested for a correlation between genetic and morphometric data while controlling for phylogeny, evolutionary rates, and divergence times. Non-carnivoran taxa generally had substantially lower glutamine-alanine ratios than carnivorans (primates and xenarthrans with means of 1.34 and 1.25, respectively, compared to a mean of 3.1 for carnivorans), and we found no correlation between RUNX2 sequence and face length across placental mammals.ConclusionsResults of our diverse comparative phylogenetic analyses indicate that QA ratio does not consistently correlate with face length across the 41 mammalian taxa considered. Thus, although RUNX2 might function as a ‘tuning knob’ modifying face length in carnivorans, this relationship is not conserved across mammals in general.