Randi H. Griffin

Community Structure and the Spread of Infectious Disease in Primate Social Networks

Living in a large social group is thought to increase disease risk in wild animal populations, but comparative studies have provided mixed support for this prediction. Here, we take a social network perspective to investigate whether patterns of social contact within groups influence parasite risk. Specifically, increased modularity (i.e. sub-grouping) in larger groups could offset the increased disease risk associated with living in a large group. We simulated the spread of a contagious pathogen in random social networks to generate theoretically grounded predictions concerning the relationship between social network connectivity and the success of socially transmitted pathogens. Simulations yielded the prediction that community modularity (Q) negatively impacts parasite success. No clear predictions emerged for a second network metric we considered, the eigenvector centralization index (C), as the relationship between this measure and parasite success depended on the transmission probability of parasites. We then tested the prediction that Q reduces parasite success in a phylogenetic comparative analysis of social network modularity and parasite richness across 19 primate species. Using a Bayesian implementation of phylogenetic generalized least squares and controlling for sampling effort, we found that primates living in larger groups exhibited higher Q, and as predicted by our simulations, higher Q was associated with lower richness of socially transmitted parasites. This suggests that increased modularity mediates the elevated risk of parasitism associated with living in larger groups, which could contribute to the inconsistent findings of empirical studies on the association between group size and parasite risk. Our results indicate that social networks may play a role in mediating pressure from socially transmitted parasites, particularly in large groups where opportunities for transmitting communicable diseases are abundant. We propose that parasite pressure in gregarious primates may have favored the evolution of behaviors that increase social network modularity, especially in large social groups.

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.

Genetic basis for a rare floral mutant in an Andean species of Solanaceae

PREMISE OF THE STUDY White forms of typically pigmented flowers are one of the most common polymorphisms in flowering plants. Although the range of genetic changes that give rise to white phenotypes is well known from model systems, few studies have identified causative mutations in natural populations. METHODS Here we combine genetic studies, in vitro enzyme assays, and biochemical analyses to identify the mechanism underlying the loss of anthocyanin pigment production in the naturally occurring white-flowered morph of Iochroma calycinum (Solanaceae). KEY RESULTS Comparison of anthocyanin gene sequences revealed a putative loss-of-function mutation, an 11 amino-acid deletion in dihydroflavonol 4-reductase (DFR), in the white morph. Functional assays of Dfr alleles from blue and white morphs demonstrated that this deletion results in a loss of enzymatic activity, indicating that the deletion could be solely responsible for the lack of pigment production. Consistent with this hypothesis, quantitative PCR showed no significant differences in expression of anthocyanin genes between the morphs. Also, thin layer chromatography confirmed that the white morph continues to accumulate compounds upstream of the DFR enzyme. CONCLUSIONS Collectively, these experiments indicate that the structural mutation at Dfr underlies the rare white flower morph of I. calycinum. This study is one of only a few examples where a flower color polymorphism is due to a loss-of-function mutation in the coding region of an anthocyanin enzyme. The rarity of such mutations in nature suggests that negative consequences prevent fixation across populations.

The Independent Evolution Method Is Not a Viable Phylogenetic Comparative Method.

Phylogenetic comparative methods (PCMs) use data on species traits and phylogenetic relationships to shed light on evolutionary questions. Recently, Smaers and Vinicius suggested a new PCM, Independent Evolution (IE), which purportedly employs a novel model of evolution based on Felsenstein’s Adaptive Peak Model. The authors found that IE improves upon previous PCMs by producing more accurate estimates of ancestral states, as well as separate estimates of evolutionary rates for each branch of a phylogenetic tree. Here, we document substantial theoretical and computational issues with IE. When data are simulated under a simple Brownian motion model of evolution, IE produces severely biased estimates of ancestral states and changes along individual branches. We show that these branch-specific changes are essentially ancestor-descendant or “directional” contrasts, and draw parallels between IE and previous PCMs such as “minimum evolution”. Additionally, while comparisons of branch-specific changes between variables have been interpreted as reflecting the relative strength of selection on those traits, we demonstrate through simulations that regressing IE estimated branch-specific changes against one another gives a biased estimate of the scaling relationship between these variables, and provides no advantages or insights beyond established PCMs such as phylogenetically independent contrasts. In light of our findings, we discuss the results of previous papers that employed IE. We conclude that Independent Evolution is not a viable PCM, and should not be used in comparative analyses.

High mortality associated with tapeworm parasitism in geladas (Theropithecus gelada) in the Simien Mountains National Park, Ethiopia

Despite increasing appreciation for parasitism as an important component of primate ecology and evolution, surprisingly few studies have demonstrated the costs of helminth parasitism in primates. Detecting parasite‐related costs in primates is particularly difficult because it requires detailed, long‐term data on individual host reproductive success, survival, and parasitism. The identification of the larval tapeworm Taenia serialis in geladas under intensive long‐term study in the Ethiopian Highlands (Nguyen et al. [2015] American Journal of Primatology, 77:579–594; Schneider‐Crease et al. [2013] Veterinary Parasitology 198:240–243) provides an opportunity to examine how an endemic parasite impacts host reproductive success and survival. We used survival analyses to assess the mortality risk associated with protuberant larval cysts characteristic of T. serialis using a decade of data from a gelada population in the Simien Mountains National Park (SMNP), Ethiopia. We demonstrated strikingly high mortality associated with T. serialis cysts in adult females, particularly for younger adults. The estimated effect of cysts on male mortality was similar, although the effect was not statistically significant, likely owing to the smaller sample size. Additionally, the offspring of mothers with cysts experienced increased mortality, which was driven almost entirely by maternal death. Mothers with cysts had such high mortality that they rarely completed an interbirth interval. Comparison with a study of this parasite in another gelada population on the Guassa Plateau (Nguyen et al. [2015] American Journal of Primatology, 77:579–594) revealed lower cyst prevalence in the SMNP and similar cyst‐associated mortality. However, many more females with cysts completed interbirth intervals at Guassa than in the SMNP, suggesting that T. serialis cysts may kill hosts more rapidly in the SMNP. Our results point toward the underlying causes of individual and population‐level heterogeneity in T. serialis‐associated mortality as important areas for future research.

Identifying wildlife reservoirs of neglected taeniid tapeworms: Non-invasive diagnosis of endemic Taenia serialis infection in a wild primate population

Despite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that includes geladas (Theropithecus gelada), primates endemic to Ethiopia. Geladas exhibit protuberant larval cysts indicative of advanced T. serialis infection that are associated with high mortality. However, non-protuberant larvae can develop in deep tissue or the abdominal cavity, leading to underestimates of prevalence based solely on observable cysts. We adapted a non-invasive monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) to detect circulating Taenia spp. antigen in dried gelada urine. Analysis revealed that this assay was highly accurate in detecting Taenia antigen, with 98.4% specificity, 98.5% sensitivity, and an area under the curve of 0.99. We used this assay to investigate the prevalence of T. serialis infection in a wild gelada population, finding that infection is substantially more widespread than the occurrence of visible T. serialis cysts (16.4% tested positive at least once, while only 6% of the same population exhibited cysts). We examined whether age or sex predicted T. serialis infection as indicated by external cysts and antigen presence. Contrary to the female-bias observed in many Taenia-host systems, we found no significant sex bias in either cyst presence or antigen presence. Age, on the other hand, predicted cyst presence (older individuals were more likely to show cysts) but not antigen presence. We interpret this finding to indicate that T. serialis may infect individuals early in life but only result in visible disease later in life. This is the first application of an antigen ELISA to the study of larval Taenia infection in wildlife, opening the doors to the identification and description of infection dynamics in reservoir populations.

Comment on Smaers et al. (2016): A nonviable phylogenetic comparative method hampered by circularity, inaccuracy, and bias

Smaers, Mongle & Kandler (2016) (Biological Journal of the Linnean Society, 118: 78-94) introduced a new phylogenetic comparative method, multiple variance Brownian motion (mvBM), for reconstructing ancestral states given a phylogenetic tree and continuous trait data. The authors conducted a simulation study and argued that mvBM outperforms constant variance Brownian motion (BM) when rates of evolution vary across the phylogeny. In this comment, we argue that mvBM is not a viable statistical method because it is fundamentally a circular analysis that overfits phylogenetic branch lengths to the data. We further argue that the comparison of mvBM to BM under conditions where the assumptions of BM are clearly violated is not an informative performance analysis, and that the simulation study of Smaers et al. (2016) exaggerates the performance of mvBM by focusing on a narrow range of simulation conditions and reporting aggregated accuracy metrics that obscure severe inaccuracy and bias in its ancestral state estimates. Our arguments are supported by simulation results. We conclude that mvBM is not a viable phylogenetic comparative method.