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Network centrality and seasonality interact to predict lice load in a social primate.

ABSTRACT: Lice are socially-transmitted ectoparasites. Transmission depends upon their host's degree of contact with conspecifics. While grooming facilitates ectoparasite transmission via body contact, it also constrains their spread through parasite removal. We investigated relations between parasite burden and sociality in female Japanese macaques following two opposing predictions: i) central females in contact/grooming networks harbour more lice, related to their numerous contacts; ii) central females harbour fewer lice, related to receiving more grooming. We estimated lice load non-invasively using the conspicuous louse egg-picking behaviour performed by macaques during grooming. We tested for covariation in several centrality measures and lice load, controlling for season, female reproductive state and dominance rank. Results show that the interaction between degree centrality (number of partners) and seasonality predicted lice load: females interacting with more partners had fewer lice than those interacting with fewer partners in winter and summer, whereas there was no relationship between lice load and centrality in spring and fall. This is counter to the prediction that increased contact leads to greater louse burden but fits the prediction that social grooming limits louse burden. Interactions between environmental seasonality and both parasite and host biology appeared to mediate the role of social processes in louse burden.

SUBMITTER: Duboscq J

PROVIDER: S-EPMC4768153 | biostudies-literature | 2016 Feb

REPOSITORIES: biostudies-literature

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Network centrality and seasonality interact to predict lice load in a social primate.

Duboscq Julie J Romano Valeria V Sueur Cédric C MacIntosh Andrew J J AJ

Scientific reports 20160226

Lice are socially-transmitted ectoparasites. Transmission depends upon their host's degree of contact with conspecifics. While grooming facilitates ectoparasite transmission via body contact, it also constrains their spread through parasite removal. We investigated relations between parasite burden and sociality in female Japanese macaques following two opposing predictions: i) central females in contact/grooming networks harbour more lice, related to their numerous contacts; ii) central females ...[more]

PMID: 26915589

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Project description:BACKGROUND:Studies of host-parasite interactions have the potential to provide insights into the ecology of both organisms involved. We monitored the movement of sucking lice (Lemurpediculus verruculosus), parasites that require direct host-host contact to be transferred, in their host population of wild mouse lemurs (Microcebus rufus). These lemurs live in the rainforests of Madagascar, are small (40 g), arboreal, nocturnal, solitary foraging primates for which data on population-wide interactions are difficult to obtain. We developed a simple, cost effective method exploiting the intimate relationship between louse and lemur, whereby individual lice were marked, without removal from their host, with an individualized code, and tracked throughout the lemur population. We then tested the hypotheses that 1) the frequency of louse transfers, and thus interactions, would decrease with increasing distance between paired individual lemurs; 2) due to host polygynandry, social interactions and hence louse transfers would increase during the onset of the breeding season; and 3) individual mouse lemurs would vary in their contributions to the spread of lice. RESULTS:We show that louse transfers involved 43.75% of the studied lemur population, exclusively males. Louse transfers peaked during the breeding season, perhaps due to increased social interactions between lemurs. Although trap-based individual lemur ranging patterns are restricted, louse transfer rate does not correlate with the distance between lemur trapping locales, indicating wider host ranging behavior and a greater risk of rapid population-wide pathogen transmission than predicted by standard trapping data alone. Furthermore, relatively few lemur individuals contributed disproportionately to the rapid spread of lice throughout the population. CONCLUSIONS:Using a simple method, we were able to visualize exchanges of lice in a population of cryptic wild primates. This method not only provided insight into the previously unseen parasite movement between lemurs, but also allowed us to infer social interactions between them. As lice are known pathogen vectors, our method also allowed us to identify the lemurs most likely to facilitate louse-mediated epidemics. Our approach demonstrates the potential to uncover otherwise inaccessible parasite-host, and host social interaction data in any trappable species parasitized by sucking lice.

Project description:Members of a society interact using a variety of social behaviors, giving rise to a multi-faceted and complex social life. For the study of animal behavior, quantifying this complexity is critical for understanding the impact of social life on animals' health and fitness. Multilayer network approaches, where each interaction type represents a different layer of the social network, have the potential to better capture this complexity than single layer approaches. Calculating individuals' centrality within a multilayer social network can reveal keystone individuals and more fully characterize social roles. However, existing measures of multilayer centrality do not account for differences in the dynamics and functionality across interaction layers. Here we validate a new method for quantifying multiplex centrality called consensus ranking by applying this method to multiple social groups of a well-studied nonhuman primate, the rhesus macaque. Consensus ranking can suitably handle the complexities of animal social life, such as networks with different properties (sparse vs. dense) and biological meanings (competitive vs. affiliative interactions). We examined whether individuals' attributes or socio-demographic factors (sex, age, dominance rank and certainty, matriline size, rearing history) were associated with multiplex centrality. Social networks were constructed for five interaction layers (i.e., aggression, status signaling, conflict policing, grooming and huddling) for seven social groups. Consensus ranks were calculated across these five layers and analyzed with respect to individual attributes and socio-demographic factors. Generalized linear mixed models showed that consensus ranking detected known social patterns in rhesus macaques, showing that multiplex centrality was greater in high-ranking males with high certainty of rank and females from the largest families. In addition, consensus ranks also showed that females from very small families and mother-reared (compared to nursery-reared) individuals were more central, showing that consideration of multiple social domains revealed individuals whose social centrality and importance might otherwise have been missed.

Project description:BACKGROUND: The parasitic sucking lice of primates are known to have undergone at least 25 million years of coevolution with their hosts. For example, chimpanzee lice and human head/body lice last shared a common ancestor roughly six million years ago, a divergence that is contemporaneous with their hosts. In an assemblage where lice are often highly host specific, humans host two different genera of lice, one that is shared with chimpanzees and another that is shared with gorillas. In this study, we reconstruct the evolutionary history of primate lice and infer the historical events that explain the current distribution of these lice on their primate hosts. RESULTS: Phylogenetic and cophylogenetic analyses suggest that the louse genera Pediculus and Pthirus are each monophyletic, and are sister taxa to one another. The age of the most recent common ancestor of the two Pediculus species studied matches the age predicted by host divergence (ca. 6 million years), whereas the age of the ancestor of Pthirus does not. The two species of Pthirus (Pthirus gorillae and Pthirus pubis) last shared a common ancestor ca. 3-4 million years ago, which is considerably younger than the divergence between their hosts (gorillas and humans, respectively), of approximately 7 million years ago. CONCLUSION: Reconciliation analysis determines that there are two alternative explanations that account for the current distribution of anthropoid primate lice. The more parsimonious of the two solutions suggests that a Pthirus species switched from gorillas to humans. This analysis assumes that the divergence between Pediculus and Pthirus was contemporaneous with the split (i.e., a node of cospeciation) between gorillas and the lineage leading to chimpanzees and humans. Divergence date estimates, however, show that the nodes in the host and parasite trees are not contemporaneous. Rather, the shared coevolutionary history of the anthropoid primates and their lice contains a mixture of evolutionary events including cospeciation, parasite duplication, parasite extinction, and host switching. Based on these data, the coevolutionary history of primates and their lice has been anything but parsimonious.

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Network centrality and seasonality interact to predict lice load in a social primate.

Publications

Network centrality and seasonality interact to predict lice load in a social primate.

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