Cospeciation of gut microbiota with hominids Moeller, Andrew H.; Caro-Quintero, Alejandro; Mjungu, Deus ...
Science (American Association for the Advancement of Science),
07/2016, Volume:
353, Issue:
6297
Journal Article
Peer reviewed
Open access
The evolutionary origins of the bacterial lineages that populate the human gut are unknown. Here we show that multiple lineages of the predominant bacterial taxa in the gut arose via cospeciation ...with humans, chimpanzees, bonobos, and gorillas over the past 15 million years. Analyses of strain-level bacterial diversity within hominid gut microbiomes revealed that clades of Bacteroidaceae and Bifidobacteriaceae have been maintained exclusively within host lineages across hundreds of thousands of host generations. Divergence times of these cospeciating gut bacteria are congruent with those of hominids, indicating that nuclear, mitochondrial, and gut bacterial genomes diversified in concert during hominid evolution. This study identifies human gut bacteria descended from ancient symbionts that speciated simultaneously with humans and the African apes.
Plasmodium falciparum is the most prevalent and lethal of the malaria parasites infecting humans, yet the origin and evolutionary history of this important pathogen remain controversial. Here we ...develop a single-genome amplification strategy to identify and characterize Plasmodium spp. DNA sequences in faecal samples from wild-living apes. Among nearly 3,000 specimens collected from field sites throughout central Africa, we found Plasmodium infection in chimpanzees (Pan troglodytes) and western gorillas (Gorilla gorilla), but not in eastern gorillas (Gorilla beringei) or bonobos (Pan paniscus). Ape plasmodial infections were highly prevalent, widely distributed and almost always made up of mixed parasite species. Analysis of more than 1,100 mitochondrial, apicoplast and nuclear gene sequences from chimpanzees and gorillas revealed that 99% grouped within one of six host-specific lineages representing distinct Plasmodium species within the subgenus Laverania. One of these from western gorillas comprised parasites that were nearly identical to P. falciparum. In phylogenetic analyses of full-length mitochondrial sequences, human P. falciparum formed a monophyletic lineage within the gorilla parasite radiation. These findings indicate that P. falciparum is of gorilla origin and not of chimpanzee, bonobo or ancient human origin.
Immune defenses provide resistance against infectious disease that is critical to survival. But immune defenses are costly, and limited resources allocated to immunity are not available for other ...physiological or developmental processes. We propose a framework for explaining variation in patterns of investment in two important subsystems of anti-pathogen defense: innate (non-specific) and acquired (specific) immunity. The developmental costs of acquired immunity are high, but the costs of maintenance and activation are relatively low. Innate immunity imposes lower upfront developmental costs, but higher operating costs. Innate defenses are mobilized quickly and are effective against novel pathogens. Acquired responses are less effective against novel exposures, but more effective against secondary exposures due to immunological memory. Based on their distinct profiles of costs and effectiveness, we propose that the balance of investment in innate versus acquired immunity is variable, and that this balance is optimized in response to local ecological conditions early in development. Nutritional abundance, high pathogen exposure and low signals of extrinsic mortality risk during sensitive periods of immune development should all favor relatively higher levels of investment in acquired immunity. Undernutrition, low pathogen exposure, and high mortality risk should favor innate immune defenses. The hypothesis provides a framework for organizing prior empirical research on the impact of developmental environments on innate and acquired immunity, and suggests promising directions for future research in human ecological immunology.
Malaria parasites, though widespread among wild chimpanzees and gorillas, have not been detected in bonobos. Here, we show that wild-living bonobos are endemically Plasmodium infected in the ...eastern-most part of their range. Testing 1556 faecal samples from 11 field sites, we identify high prevalence Laverania infections in the Tshuapa-Lomami-Lualaba (TL2) area, but not at other locations across the Congo. TL2 bonobos harbour P. gaboni, formerly only found in chimpanzees, as well as a potential new species, Plasmodium lomamiensis sp. nov. Rare co-infections with non-Laverania parasites were also observed. Phylogenetic relationships among Laverania species are consistent with co-divergence with their gorilla, chimpanzee and bonobo hosts, suggesting a timescale for their evolution. The absence of Plasmodium from most field sites could not be explained by parasite seasonality, nor by bonobo population structure, diet or gut microbiota. Thus, the geographic restriction of bonobo Plasmodium reflects still unidentified factors that likely influence parasite transmission.
Explaining intraspecific variation in reproductive tactics hinges on measuring associated costs and benefits. Yet, this is difficult if alternative (purportedly less optimal) tactics remain ...unobserved. We describe a rare alpha-position take-over by an immigrant male rhesus macaque in a population where males typically gain rank via succession. Unusually, male aggressiveness after the take-over correlated with rank and mating success. The new alpha achieved the highest mating and reproductive success. Nevertheless, he sired only 4 infants due to high extra-group paternity (59.3%). The costs of his immigration tactic were high: after the mating season ended, unable to deter coalitionary attacks by resident males, he was overthrown. The following year he had the highest relative annual weight loss and levels of immune activation among males in the group. Succession-based rank-acquisition in large, provisioned groups of macaques thus appears to be actively maintained by resident males, who impose high costs on challengers.
Many animals have been shown to eat fungi and most truffle-like fungi depend on animals for spore dispersal via mycophagy. Although these interactions are widespread, they are understudied in many ...habitats. In this study, we show that bonobos (Pan paniscus) forage and feed on an undescribed truffle species in the rainforests of the Democratic Republic of Congo. Based on morphological and molecular assessment of collections, we show that the species eaten by bonobos is a previously undescribed taxon described here as Hysterangium bonobo. This species is known in the local Bantu language (Bongando) as simbokilo and is used for baiting traps to catch several species of small mammals. Our findings highlight the need for further research into mycophagy and systematics of sequestrate fungi in Africa.
Lay Summary How does male quality relate to rank and mating success in rhesus macaques? We measured innate immune function and oxidative status as indicators of male quality in free-ranging rhesus ...macaques. Higher-ranking males had more robust innate immune functionality, lower oxidative damage, and higher mating success. Rank showed stronger association with mating success than measures of physiological quality. Whether high-quality males are sexually attractive to females independently of rank remains to be established.In social mammals, condition and health are important determinants of the ability of males to achieve high dominance rank. Measures of individual condition are also predicted to affect male fitness via female preference for high-quality mates. We examined intermale variation in phenotypic quality (immune function and oxidative stress) in relation to male dominance status and mating success in a species with prominent female choice and a lack of male-female sexual coercion, the rhesus macaque (Macaca mulatta). We quantified immunity via 2 functional assays of innate immune response (bacteria killing assay and hemolytic complement assay) and measured oxidative stress via a lipid peroxidation assay in 15 adult males from 1 social group of macaques on Cayo Santiago, Puerto Rico. We then observed these males throughout the mating season to test the prediction that males in better condition achieved higher mating success. Males with more robust innate immune response and lower oxidative damage mated with a greater number of potentially fertile females. Male dominance rank, however, also correlated with our measures of quality. Higher-ranking males had more robust functional innate immune response and lower levels of oxidative damage. After accounting for rank, male quality was no longer correlated with mating success. These results demonstrate a potentially important role of male phenotypic quality in the mating system of a long-lived, group-living primate. What are the exact behavioral mechanisms via which sexual selection may operate on traits related to immunocompetence and resistance to oxidative damage in this species, however, remains an open question.
Exaggerated male traits can evolve under intra- or intersexual selection, but it remains less clear how often both mechanisms act together on trait evolution. While the males of many anthropoid ...primate species exhibit colorful signals that appear to be badges of status under intrasexual selection, the red facial coloration of male rhesus macaques (
) appears to have evolved primarily under intersexual selection and female mate choice. Nonetheless, experiments show that red color is salient to males, raising the question of whether the signal may also be under intrasexual selection. Here, we examine whether males express this signal more strongly in competitive contexts. Facial images were collected on all 15 adult males of a free-ranging social group during the peak of the mating season, and coloration was quantified using visual models. Results show that males more similar in facial redness were more likely to interact aggressively than more dissimilar ones, suggesting that color may be involved in the assessment of rivals. Furthermore, males exhibited darker coloration on days they were observed copulating, and dominance rank predicted facial redness only on copulating days, suggesting that coloration may also advertise motivation to defend a mate. Male rhesus macaque facial coloration may thus mediate agonistic interactions with rivals during competition over reproductive opportunities, such that it is under both inter- and intrasexual selection. However, color differences were small, raising perceptibility questions. It remains possible that color variation reflects differences in male condition, which in turn alter investment towards male-male competition and mating effort.
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