Genetic regulation of parasite infection: empirical evidence of the functional significance of an IL4 gene SNP on nematode infections in wild primates

Background Susceptibility to parasite infection affects fitness-related processes, such as mate choice and survival, yet its genetic regulation remains poorly understood. Interleukin-4 (IL4) plays a central role in the humoral immune defence against nematode parasite infections, inducing IgE switch and regulation of worm expulsion from the intestines. The evolutionary and functional significance of single nucleotide polymorphisms (SNPs) in IL4-genes is known, yet empirical information on the effect of IL4 SNPs on gastro-intestinal infections is lacking. Using samples from a population of wild red-fronted lemurs (Eulemur fulvus rufus, Primates: Lemuridae), from western Madagascar, we explored the association of IL4-gene promoter polymorphisms with nematode infections and investigated a possible functional role of the IL4 polymorphism on male reproductive success. Results Using sequence analyses of lemur DNA we detected a new SNP in the IL4 gene promoter area. Carriers of the genotype T/T showed higher nematode infection intensities than individuals of genotypes C/T and C/C. Genetic population analyses using data from more than 10 years, suggested higher reproductive success of T/T males than expected. Conclusions Our results suggest a regulatory effect of an IL4 gene promoter polymorphism on the intensity of parasite infections in a natural population of red-fronted lemurs, with a seemingly disadvantageous genotype represented in low frequencies. Long-term population analyses, however, point in the direction of a negative frequency-dependent association, giving a fitness advantage to the rare genotype. Due to low frequencies of the genotype in question conclusive evidence of a functional role of IL4 polymorphism cannot be drawn here; still, we suggest the use of IL4 polymorphism as a new molecular tool for quick assessment of individual genetic constitution with regard to nematode infection intensities, contributing to a better understanding of the actual components of the immune response that mediate protection against gastro-intestinal parasites

Catalyzing Transitions to Sociality: Ecology Builds on Parental Care

In the context of social evolution research, great emphasis on kin-selected benefits has led to an understanding of parental care as one of the activities that helpers can perform in extended cooperative families. Nevertheless, this perspective might have precluded a deeper understanding of the implications of parental care for social evolution. We argue that parental care is a broader set of processes playing a key role both before and during the emergence of sociality. The care system of a species may be understood as the result of long coevolutionary processes with environmental pressures during pre-social stages that impact transitions to sociality. We evaluate the present framework against evidence on the evolution of parental care and transitions toward sociality in subsocial and parasocial vertebrate and invertebrate species. Moreover, following previous evidence for the importance of modes of foraging and resting, we structure our inquiry by classifying societies into three types. Our results suggest that in “central place foragers” and “fortress defenders”, ecological factors promoting the evolution of parental care foster a set of coevolutionary feedback loops resulting in increases in parental effort and offspring needs. Offspring needs alone or in combination with limited breeding options enhance the relative benefits of positive social interactions, catalyzing transitions to sociality. In “itinerant foragers”, sociality is associated with colonizing new niches. Changes in predation pressure entail changes in the modes of care or selection for certain types of care already present in solitary ancestors. Further changes in the form of collective defense may be needed for permanent sociality to evolve. We conclude that there is evidence that social transitions to different types of societies are the result of long coevolutionary processes between environmental pressures and the care systems in a wide variety of taxa. Therefore, advances in the study of the origins of sociality may require further investigation of parental care evolution in solitary ancestors of today's social species

The Behavioral Ecology of the Tibetan Macaque

This open access book summarizes the multi-disciplinary results of one of China’s main primatological research projects on the endemic Tibetan macaque (Macaca thibetana), which had continued for over 30 years, but which had never been reported on systematically. Dedicated to this exceptional Old World monkey, this book makes the work of Chinese primatologists on the social behavior, cooperation, culture, cognition, group dynamics, and emerging technologies in primate research accessible to the international scientific community

Refuge sharing network predicts ectoparasite load in a lizard

Living in social groups facilitates cross-infection by parasites. However, empirical studies on indirect transmission within wildlife populations are scarce. We investigated whether asynchronous overnight refuge sharing among neighboring sleepy lizards, Tiliqua rugosa, facilitates indirect transmission of its ectoparasitic tick, Amblyomma limbatum. We fitted 18 neighboring lizards with GPS recorders, observed their overnight refuge use each night over 3 months, and counted their ticks every fortnight. We constructed a transmission network to estimate the cross-infection risk based on asynchronous refuge sharing frequencies among all lizards and the life history traits of the tick. Although self-infection was possible, the network provided a powerful predictor of measured tick loads. Highly connected lizards that frequently used their neighbors’ refuges were characterized by higher tick loads. Thus, indirect contact had a major influence on transmission pathways and parasite loads. Furthermore, lizards that used many different refuges had lower cross- and self-infection risks and lower tick loads than individuals that used relatively fewer refuges. Increasing the number of refuges used by a lizard may be an important defense mechanism against ectoparasite transmission in this species. Our study provides important empirical data to further understand how indirectly transmitted parasites move through host populations and influence individual parasite loads

Interrelationship among spatial cohesion, aggression rate, counter-aggression and female dominance in three lemur species

Abstract: How social and ecological factors are associated with variation in dominance style across species of animals has been studied frequently, but the underlying processes are often not addressed. Theoretical research indicates that stronger spatial cohesion among individuals in a group causes a higher frequency of fighting and, thus, through the self-reinforcing effects of winning and losing fights, a stronger differentiation of the dominance hierarchy and dominance of females over more males. Our aim in the present paper is to study whether the same interrelationship among processes may underlie differences in dominance style among three species of lemur that differ in their degree of despotism: Lemur catta, Propithecus verreauxi and Eulemur rufifrons. We investigated their agonistic interactions and spatial cohesion based on 2752 h of observational data of 20 wild groups of these three species. We determined dominance style using the proportion of counter-aggression, with a lower proportion indicating a more despotic dominance style. We found that stronger spatial cohesion among individuals is associated with a higher rate of aggression, stronger despotism and dominance of females over more males. The results of our study emphasise the general importance of spatial cohesion in determining dominance style. Significance statement: Theoretical studies have shown that the spatial configuration of individuals in a group influences the dominance style. In an agent-based model, DomWorld, individuals are guided by simple rules of grouping and fighting and emergent patterns of behaviour switch between resembling those of despotic or egalitarian primates depending on the degree of cohesion in groups. Yet this link has seldom been studied empirically. We, therefore, examine the relevance of spatial cohesion on patterns of behaviour of individuals in groups of three species of lemur. We confirm the predictions from the model and show that stronger spatial cohesion results in more frequent aggression, a more despotic dominance style and stronger female dominance over males. In light of this, we urge future research of animal dominance to include measures of cohesion

Editorial: Sex and gender effects on power, status, dominance, and leadership – an interdisciplinary look at human and other mammalian societies

In human societies, men tend to have more power, status, dominance, and occupy leadership positions more often than women; similarly, in animal societies, power and dominance are often unequally distributed between males and females. Despite these similarities across societies of humans and animals, the scientific study of power, status, dominance, and leadership have (for the most part) progressed in isolation, with little cross-disciplinary exchange or fertilization between the natural and social sciences

Corrigendum: Editorial: Sex and gender effects on power, status, dominance, and leadership – an interdisciplinary look at human and other mammalian societies

In the published article, there was an error in Research investigating sex effects in non-human mammals, paragraph 5. We omitted a few words in two places of the same sentence. The sentence previously stated: “Several papers in this Research Topic investigated whether the degree of dominance of females over males depends on morphological, demographic or ecological factors such as relative body size, adult sex ratio, sexual maturity or mating season.” The corrected sentence appears below: “Several papers in this Research Topic investigated whether the degree of dominance of females over males depends on morphological, demographic, ecological or social factors such as relative body size, adult sex ratio, sexual maturity, mating season or social support.” In the published article, there was an error in Research investigating sex effects in non-human mammals, paragraph 7. We omitted a full sentence citing the results of one study of the Research Topic. This sentence previously stated: “Conversely, Koenig et al. show in wild gray langurs that male dominance appears inflexible across contexts, and that the rare events of female aggression toward males are aimed at infant protection, while most male aggression towards females occur in a feeding context. This work suggests that intersexual feeding competition may contribute to shaping male-female relationships.” The corrected sentence appears below: “Conversely, Koenig et al. show in wild gray langurs that male dominance appears inflexible across contexts, and that the rare events of female aggression toward males are aimed at infant protection, while most male aggression towards females occur in a feeding context. This work suggests that intersexual feeding competition may contribute to shaping male-female relationships. Moreover, McCormick et al. report support for the idea that sex differences in agonistic behavior as well as in social support both mediate female dominance over males in clans of spotted hyenas, even though adult females can often dominate immigrant males without any support.” In the published article, there was an error in Research investigating sex effects in non-human mammals, paragraph 8. A couple of words need to be changed to the following sentence to avoid repeats arising from the inserted sentence. This sentence previously stated: “Finally, in the female-dominated society of spotted hyenas, East et. al., show that male fitness is substantially affected by the loss of offspring due to infanticide by females.” The corrected sentence appears below: “Finally, also in spotted hyenas, East et al. show that male fitness is substantially affected by the loss of offspring due to infanticide by females.” The authors apologize for this error and state that this does not change the scientific conclusions of the article in any way. The original article has been updated.</p

Species delimitation in lemurs: multiple genetic loci reveal low levels of species diversity in the genus Cheirogaleus

<p>Abstract</p> <p>Background</p> <p>Species are viewed as the fundamental unit in most subdisciplines of biology. To conservationists this unit represents the currency for global biodiversity assessments. Even though Madagascar belongs to one of the top eight biodiversity hotspots of the world, the taxonomy of its charismatic lemuriform primates is not stable. Within the last 25 years, the number of described lemur species has more than doubled, with many newly described species identified among the nocturnal and small-bodied cheirogaleids. Here, we characterize the diversity of the dwarf lemurs (genus <it>Cheirogaleus</it>) and assess the status of the seven described species, based on phylogenetic and population genetic analysis of mtDNA (<it>cytb </it>+ <it>cox2</it>) and three nuclear markers (<it>adora3</it>, <it>fiba </it>and <it>vWF</it>).</p> <p>Results</p> <p>This study identified three distinct evolutionary lineages within the genus <it>Cheirogaleus</it>. Population genetic cluster analyses revealed a further layer of population divergence with six distinct genotypic clusters.</p> <p>Conclusion</p> <p>Based on the general metapopulation lineage concept and multiple concordant data sets, we identify three exclusive groups of dwarf lemur populations that correspond to three of the seven named species: <it>C. major</it>, <it>C. medius </it>and <it>C. crossleyi</it>. These three species were found to be genealogically exclusive in both mtDNA and nDNA loci and are morphologically distinguishable. The molecular and morphometric data indicate that <it>C. adipicaudatus </it>and <it>C. ravus </it>are synonymous with <it>C. medius </it>and <it>C. major</it>, respectively. <it>Cheirogaleus sibreei </it>falls into the <it>C. medius </it>mtDNA clade, but in morphological analyses the membership is not clearly resolved. We do not have sufficient data to assess the status of <it>C. minusculus</it>. Although additional patterns of population differentiation are evident, there are no clear subdivisions that would warrant additional specific status. We propose that ecological and more geographic data should be collected to confirm these results.</p

Concatenation and Concordance in the Reconstruction of Mouse Lemur Phylogeny: An Empirical Demonstration of the Effect of Allele Sampling in Phylogenetics

The systematics and speciation literature is rich with discussion relating to the potential for gene tree/species tree discordance. Numerous mechanisms have been proposed to generate discordance, including differential selection, longbranch attraction, gene duplication, genetic introgression, and/or incomplete lineage sorting. For speciose clades in which divergence has occurred recently and rapidly, recovering the true species tree can be particularly problematic due to incomplete lineage sorting. Unfortunately, the availability of multilocus or “phylogenomic” data sets does not simply solve the problem, particularly when the data are analyzed with standard concatenation techniques. In our study, we conduct a phylogenetic study for a nearly complete species sample of the dwarf and mouse lemur clade, Cheirogaleidae. Mouse lemurs (genus, Microcebus) have been intensively studied over the past decade for reasons relating to their high level of cryptic species diversity, and although there has been emerging consensus regarding the evolutionary diversity contained within the genus, there is no agreement as to the inter-specific relationships within the group. We attempt to resolve cheirogaleid phylogeny, focusing especially on the mouse lemurs, by employing a large multilocus data set. We compare the results of Bayesian concordance methods with those of standard gene concatenation, finding that though concatenation yields the strongest results as measured by statistical support, these results are found to be highly misleading. By employing an approach where individual alleles are treated as operational taxonomic units, we show that phylogenetic results are substantially influenced by the selection of alleles in the concatenation process. Includes supplementary materials