The changing ecology of primate parasites: Insights from wild-captive comparisons.

Host movements, including migrations or range expansions, are known to influence parasite communities. Transitions to captivity-a rarely studied yet widespread human-driven host movement-can also change parasite communities, in some cases leading to pathogen spillover among wildlife species, or between wildlife and human hosts. We compared parasite species richness between wild and captive populations of 22 primate species, including macro- (helminths and arthropods) and micro-parasites (viruses, protozoa, bacteria, and fungi). We predicted that captive primates would have only a subset of their native parasite community, and would possess fewer parasites with complex life cycles requiring intermediate hosts or vectors. We further predicted that captive primates would have parasites transmitted by close contact and environmentally-including those shared with humans and other animals, such as commensals and pests. We found that the composition of primate parasite communities shifted in captive populations, especially because of turnover (parasites detected in captivity but not reported in the wild), but with some evidence of nestedness (holdovers from the wild). Because of the high degree of turnover, we found no significant difference in overall parasite richness between captive and wild primates. Vector-borne parasites were less likely to be found in captivity, whereas parasites transmitted through either close or non-close contact, including through fecal-oral transmission, were more likely to be newly detected in captivity. These findings identify parasites that require monitoring in captivity and raise concerns about the introduction of novel parasites to potentially susceptible wildlife populations during reintroduction programs.

Quaternary climate change and social behavior shaped the genetic differentiation of an endangered montane primate from the southern edge of the Tibetan Plateau.

Multiple factors, including climate change, dispersal barriers, and social behavior influence the genetic structure of natural populations. While the effects of extrinsic factors such as historical climatic change and habitat topography have been well studied, mostly in temperate habitats, the simultaneous effects of intrinsic factors such as social behavior on genetic structure have rarely been explored. Such simultaneous effect, however, may particularly be common in social mammals such as many primates. Consequently, we studied the population structure of a rare and endangered social primate, the Arunachal macaque Macaca munzala, endemic to the northeastern Indian state of Arunachal Pradesh, located on the subtropical southern edge of the Tibetan Plateau and forming part of the Eastern Himalayan biodiversity hotspot. We studied a 534 bp-long mitochondrial DNA sequence and 22 autosomal microsatellite loci in individuals from three populations, Tawang, Upper Subansiri, and West Siang. The mtDNA data revealed three major divergence events: that between the Arunachal and bonnet macaques (ca. 1.61 mya), the founding of the West Siang population and the ancestral population of the present-day bonnet macaques (ca. 1.32 mya), and the divergence between the Tawang and Upper Subansiri populations (ca. 0.80 mya) that coincided with the major glacial events in the region. Comparing mitochondrial DNA with autosomal microsatellites, we also found evidence for female philopatry and male-driven long-distance gene flow. Arunachal macaques thus appear to be characterized by groups of philopatric females separated by geographical barriers and harsh climate but with dispersing males exerting a homogenizing effect on the nuclear gene pool. Given that severe population differentiation is of major concern in species conservation, we suggest that our study populations represent significant conservation units of this rare, endangered primate but, more importantly, emphasize the complex interplay of extrinsic and intrinsic factors in shaping the population structure of a social mammalian species.

Phylodynamic analysis of the highly pathogenic avian influenza H5N8 epidemic in France, 2016-2017.

In 2016-2017, France experienced a devastating epidemic of highly pathogenic avian influenza (HPAI) H5N8, with more than 400 outbreaks reported in poultry farms. We analyzed the spatiotemporal dynamics of the epidemic using a structured-coalescent-based phylodynamic approach that combined viral genomic data (n = 196; one viral genome per farm) and epidemiological data. In the process, we estimated viral migration rates between départements (French administrative regions) and the temporal dynamics of the effective viral population size (Ne) in each département. Viral migration rates quantify viral spread between départements and Ne is a population genetic measure of the epidemic size and, in turn, is indicative of the within-département transmission intensity. We extended the phylodynamic analysis with a generalized linear model to assess the impact of multiple factors-including large-scale preventive culling and live-duck movement bans-on viral migration rates and Ne. We showed that the large-scale culling of ducks that was initiated on 4 January 2017 significantly reduced the viral spread between départements. No relationship was found between the viral spread and duck movements between départements. The within-département transmission intensity was found to be weakly associated with the intensity of duck movements within départements. Together, these results indicated that the virus spread in short distances, either between adjacent départements or within départements. Results also suggested that the restrictions on duck transport within départements might not have stopped the viral spread completely. Overall, we demonstrated the usefulness of phylodynamics in characterizing the dynamics of a HPAI epidemic and assessing control measures. This method can be adapted to investigate other epidemics of fast-evolving livestock pathogens.

What leads to parallel evolution?

The repeated emergence of similar variants of influenza virus is linked to interactions between the virus's RNA segments.

Effects of host extinction and vector preferences on vector-borne disease risk in phylogenetically structured host-hector communities.

Anthropogenic disturbance impacts the phylogenetic composition and diversity of ecological communities. While changes in diversity are known to dramatically change species interactions and alter disease dynamics, the effects of phylogenetic changes in host and vector communities on disease have been relatively poorly studied. Using a theoretical model, we investigated how phylogeny and extinction influence network structural characteristics relevant to disease transmission in disturbed environments. We modelled a multi-host, multi-vector community as a bipartite ecological network, where nodes represent host and vector species and edges represent connections among them through vector feeding, and we simulated vector preferences and threat status on host and parasite phylogenies. We then simulated loss of hosts, including phylogenetically clustered losses, to investigate how extinction influences network structure. We compared effects of phylogeny and extinction to those of host specificity, which we predicted to strongly increase network modularity and reduce disease prevalence. The simulations revealed that extinction often increased modularity, with higher modularity as species loss increased, although not as much as increasing host specificity did. These results suggest that extinction itself, all else being equal, may reduce disease prevalence in disturbed communities. However, in real communities, systematic patterns in species loss (e.g. favoring high competence species) or changes in abundance may counteract these effects. Unexpectedly, we found that effects of phylogenetic signal in host and vector traits were relatively weak, and only important when phylogenetic signal of host and vector traits were similar, or when these traits both varied.

Inferring within-flock transmission dynamics of highly pathogenic avian influenza H5N8 virus in France, 2020.

Following the emergence of highly pathogenic avian influenza (H5N8) in France in early December 2020, we used duck mortality data from the index farm to investigate within-flock transmission dynamics. A stochastic epidemic model was fitted to the daily mortality data and model parameters were estimated using an approximate Bayesian computation sequential Monte Carlo (ABC-SMC) algorithm. The model predicted that the first bird in the flock was infected 5 days (95% credible interval, CI: 3-6) prior to the day of suspicion and that the transmission rate was 4.1 new infections per day (95% CI: 2.8-5.8). On average, ducks became infectious 4.1 h (95% CI: 0.7-9.1) after infection and remained infectious for 4.3 days (95% CI: 2.8-5.7). The model also predicted that 34% (50% prediction interval: 8%-76%) of birds would already be infectious by the day of suspicion, emphasizing the substantial latent threat this virus could pose to other poultry farms and to neighbouring wild birds. This study illustrates how mechanistic models can help provide rapid relevant insights that contribute to the management of infectious disease outbreaks of farmed animals. These methods can be applied to future outbreaks and the resulting parameter estimates made available to veterinary services within a few hours.

Genetic polymorphism in the serotonin transporter promoter region and ecological success in macaques.

A well-characterised sequence length polymorphism in the serotonin transporter promoter region (5-HTTLPR) influences individual behavioural traits and cognitive abilities in humans and rhesus macaques. Macaques have been classified into four continuous grades on the basis of their behavioural attributes, ranging from highly hierarchical and nepotistic species to the most egalitarian and tolerant ones. A comparative study of several species that spanned these grades revealed only rhesus macaques to be polymorphic at the 5-HTTLPR and concluded that the polymorphism was responsible for their despotic and aggressive behaviour (Wendland et al., Behav Genet 36:163-172, 2006). We studied wild populations of three other species and found that the egalitarian and tolerant bonnet and Arunachal macaques are also polymorphic while liontailed macaques, although belonging to the same group, are monomorphic. We thus reject a role for this particular polymorphism in interspecific behavioural variability and show that polymorphic species enjoy greater ecological success possibly due to their higher intraspecific variability in individual behavioural traits.

Land Use Change Increases Wildlife Parasite Diversity in Anamalai Hills, Western Ghats, India.

Anthropogenic landscape changes such as land use change and habitat fragmentation are known to alter wildlife diversity. Since host and parasite diversities are strongly connected, landscape changes are also likely to change wildlife parasite diversity with implication for wildlife health. However, research linking anthropogenic landscape change and wildlife parasite diversity is limited, especially comparing effects of land use change and habitat fragmentation, which often cooccur but may affect parasite diversity substantially differently. Here, we assessed how anthropogenic land use change (presence of plantation, livestock foraging and human settlement) and habitat fragmentation may change the gastrointestinal parasite diversity of wild mammalian host species (n = 23) in Anamalai hills, India. We found that presence of plantations, and potentially livestock, significantly increased parasite diversity due possibly to spillover of parasites from livestock to wildlife. However, effect of habitat fragmentation on parasite diversity was not significant. Together, our results showed how human activities may increase wildlife parasite diversity within human-dominated landscape and highlighted the complex pattern of parasite diversity distribution as a result of cooccurrence of multiple anthropogenic landscape changes.

Prevalence of Gastrointestinal Parasites in Civets of Fragmented Rainforest Patches in Anamalai Hills, Western Ghats, India.

: Parasitism, driven by anthropogenic habitat modifications, is being increasingly recognized as a major threat to wildlife. Unfortunately, even baseline parasite data for most wildlife species are lacking in India, including the civets, which are particularly vulnerable due to their proximity to human habitations. Civet fecal samples were collected from 10 forest fragments that vary in size and disturbance level in Anamalai Hills, Western Ghats, India. These samples were screened for the presence of gastrointestinal parasites using fecal floatation and fecal sedimentation techniques. From a total of 180 civet fecal samples, 15 gastrointestinal parasite taxa were recovered, and these species are also known to infect domesticated animals. Additionally, small, disturbed forest fragments recorded higher mean gastrointestinal parasite taxa and greater prevalence when compared to large, undisturbed forest fragments, indicating a potential relationship between anthropogenic activities and gastrointestinal parasitism of civets in the Anamalai Hills.

Mammalian gastrointestinal parasites in rainforest remnants of Anamalai Hills, Western Ghats, India.

Habitat fragmentation is postulated to be a major factor influencing infectious disease dynamics in wildlife populations and may also be responsible, at least in part, for the recent spurt in the emergence, or re-emergence, of infectious diseases in humans. The mechanism behind these relationships are poorly understood due to the lack of insights into the interacting local factors and insufficient baseline data in ecological parasitology of wildlife. Here, we studied the gastrointestinal parasites of nonhuman mammalian hosts living in 10 rainforest patches of the Anamalai Tiger Reserve, India. We examined 349 faecal samples of 17 mammalian species and successfully identified 24 gastrointestinal parasite taxa including 1 protozoan, 2 trematode, 3 cestode and 18 nematode taxa. Twenty of these parasites are known parasites of humans. We also found that as much as 73% of all infected samples were infected by multiple parasites. In addition, the smallest and most fragmented forest patches recorded the highest parasite richness; the pattern across fragments, however, seemed to be less straightforward, suggesting potential interplay of local factors.

Mixed fortunes: ancient expansion and recent decline in population size of a subtropical montane primate, the Arunachal macaque Macaca munzala.

Quaternary glacial oscillations are known to have caused population size fluctuations in many temperate species. Species from subtropical and tropical regions are, however, considerably less studied, despite representing most of the biodiversity hotspots in the world including many highly threatened by anthropogenic activities such as hunting. These regions, consequently, pose a significant knowledge gap in terms of how their fauna have typically responded to past climatic changes. We studied an endangered primate, the Arunachal macaque Macaca munzala, from the subtropical southern edge of the Tibetan plateau, a part of the Eastern Himalaya biodiversity hotspot, also known to be highly threatened due to rampant hunting. We employed a 534 bp-long mitochondrial DNA sequence and 22 autosomal microsatellite loci to investigate the factors that have potentially shaped the demographic history of the species. Analysing the genetic data with traditional statistical methods and advance Bayesian inferential approaches, we demonstrate a limited effect of past glacial fluctuations on the demographic history of the species before the last glacial maximum, approximately 20,000 years ago. This was, however, immediately followed by a significant population expansion possibly due to warmer climatic conditions, approximately 15,000 years ago. These changes may thus represent an apparent balance between that displayed by the relatively climatically stable tropics and those of the more severe, temperate environments of the past. This study also draws attention to the possibility that a cold-tolerant species like the Arunachal macaque, which could withstand historical climate fluctuations and grow once the climate became conducive, may actually be extremely vulnerable to anthropogenic exploitation, as is perhaps indicated by its Holocene ca. 30-fold population decline, approximately 3,500 years ago. Our study thus provides a quantitative appraisal of these demographically important events, emphasising the ability to potentially infer the occurrence of two separate historical events from contemporary genetic data.

Phylogenetic relationships and morphometric affinities of the Arunachal macaque Macaca munzala, a newly described primate from Arunachal Pradesh, northeastern India.

A new species of primate, the Arunachal macaque Macaca munzala, belonging to the sinica species-group of the genus, was described from northeastern India in 2005, and, based on its appearance and distribution, hypothesised to be closely related to M. assamensis and M. thibetana. We subsequently obtained an entire adult male specimen and tissue remains from two other M. munzala individuals. Molecular analyses establish the distinct identity of the species and indicate a time of origin of c. 0.48 mya for it. The species also shows close phylogenetic affinities with the allopatric M. radiata and with the geographically closer M. assamensis and M. thibetana, possibly mediated by male introgression from an ancestral M. assamensis-M. thibetana stock into an ancestral M. munzala stock. Morphometric analyses, on the other hand, reiterate its close similarity only with M. assamensis and M. thibetana, presumably resulting from convergent evolution under similar ecological conditions and along a latitudinal gradient, as predicted by Bergmann's and Allen's rules.