Diversity and temporal dynamics of primate milk microbiomes

Milk is inhabited by a community of bacteria and is one of the first postnatal sources of microbial exposure for mammalian young. Bacteria in breast milk may enhance immune development, improve intestinal health, and stimulate the gut‐brain axis for infants. Variation in milk microbiome structure (e.g., operational taxonomic unit [OTU] diversity, community composition) may lead to different infant developmental outcomes. Milk microbiome structure may depend on evolutionary processes acting at the host species level and ecological processes occurring over lactation time, among others. We quantified milk microbiomes using 16S rRNA high‐throughput sequencing for nine primate species and for six primate mothers sampled over lactation. Our data set included humans (Homo sapiens, Philippines and USA) and eight nonhuman primate species living in captivity (bonobo [Pan paniscus], chimpanzee [Pan troglodytes], western lowland gorilla [Gorilla gorilla gorilla], Bornean orangutan [Pongo pygmaeus], Sumatran orangutan [Pongo abelii], rhesus macaque [Macaca mulatta], owl monkey [Aotus nancymaae]) and in the wild (mantled howler monkey [Alouatta palliata]). For a subset of the data, we paired microbiome data with nutrient and hormone assay results to quantify the effect of milk chemistry on milk microbiomes. We detected a core primate milk microbiome of seven bacterial OTUs indicating a robust relationship between these bacteria and primate species. Milk microbiomes differed among primate species with rhesus macaques, humans and mantled howler monkeys having notably distinct milk microbiomes. Gross energy in milk from protein and fat explained some of the variations in microbiome composition among species. Microbiome composition changed in a predictable manner for three primate mothers over lactation time, suggesting that different bacterial communities may be selected for as the infant ages. Our results contribute to understanding ecological and evolutionary relationships between bacteria and primate hosts, which can have applied benefits for humans and endangered primates in our care.     

Gut microbiomes of sympatric Amazonian wood‐eating catfishes (Loricariidae) reflect host identity and little role in wood digestion

Neotropical wood‐eating catfishes (family Loricariidae) can occur in diverse assemblages with multiple genera and species feeding on the same woody detritus. As such, they present an intriguing system in which to examine the influence of host species identity on the vertebrate gut microbiome as well as to determine the potential role of gut bacteria in wood digestion. We characterized the gut microbiome of two co‐occurring catfish genera and four species: Panaqolus albomaculatus, Panaqolus gnomus, Panaqolus nocturnus, and Panaque bathyphilus, as well as that of submerged wood on which they feed. The gut bacterial community did not significantly vary across three gut regions (proximal, mid, distal) for any catfish species, although interspecific variation in the gut microbiome was significant, with magnitude of interspecific difference generally reflecting host phylogenetic proximity. Further, the gut microbiome of each species was significantly different to that present on the submerged wood. Inferring the genomic potential of the gut microbiome revealed that the majority of wood digesting pathways were at best equivalent to and more often depleted or nonexistent within the catfish gut compared to the submerged wood, suggesting a minimal role for the gut microbiome in wood digestion. Rather, these fishes are more likely reliant on fiber degradation performed by microbes in the environment, with their gut microbiome determined more by host identity and phylogenetic history.     

The role of gut microbes in satisfying the nutritional demands of adult and juvenile wild,black howler monkeys (Alouatta pigra)

In all mammals, growth, development, pregnancy, and lactation increase nutritional demands. Although primate field studies tend to focus on shifts in activity and diet as mechanisms to compensate for these demands, differences in digestive efficiency also are likely to be important. Because the gut microbiota can impact host digestive efficiency, we examined differences in activity budget, diet, and the gut microbial community among adult male (N = 4), adult female (N = 4), and juvenile (N = 5) wild black howler monkeys (Alouatta pigra) across a ten‐month period in Palenque National Park, Mexico to determine how adult females and juveniles compensate for increased nutritional demands. Results indicate that adult females and juveniles consumed more protein and energy than adult males. Adult males, adult females, and juveniles also possessed distinct gut microbial communities, unrelated to diet. Juveniles exhibited a gut microbiota characterized by bacteria from the phylum Firmicutes, such as Roseburia and Ruminococcus, and demonstrated high fecal volatile fatty acid content, suggesting increased microbial contributions to host energy balances. Adult females possessed a higher Firmicutes to Bacteroidetes ratio, also suggesting increased energy production, and their gut microbiota was characterized by Lactococcus, which has been associated with folate biosynthesis. On the basis of these patterns, it appears that the gut microbiota differentially contributes to howler monkey nutrition during reproduction and growth. Determining the nutritional and energetic importance of shifts in activity, diet, and the gut microbiota in other nonhuman primate taxa, as well as humans, will transform our understanding of these life history processes and the role of host‐microbe relationships in primate evolution. Am J Phys Anthropol 155:652–664, 2014. © 2014 Wiley Periodicals, Inc.     

Species diversity and relative abundance of lactic acid bacteria in the milk of rhesus monkeys (Macaca mulatta)

Background Mother’s milk is a source of bacteria that influences the development of the infant commensal gut microbiota. To date, the species diversity and relative abundance of lactic acid bacteria in the milk of non‐human primates have not been described. Methods Milk samples were aseptically obtained from 54 female rhesus monkeys (Macaca mulatta) at peak lactation. Following GM17 and MRS agar plating, single bacterial colonies were isolated based on difference in morphotypes, then grouped based on whole‐cell protein profiles on SDS–PAGE. Bacterial DNA was isolated and the sequence the 16S rRNA gene was analyzed. Results A total of 106 strains of 19 distinct bacterial species, belonging to five genera, Bacillus, Enterococcus, Lactobacillus, Pediococcus, and Streptococcus, were identified. Conclusions Maternal gut and oral commensal bacteria may be translocated to the mammary gland during lactation and present in milk. This pathway can be an important source of commensal bacteria to the infant gut and oral cavity.     

Microbiome maturation during a unique developmental window

Shortly after birth, mammals are colonized by a multitude of microbes derived from the mother and the environment. Studies in model organisms have demonstrated that the structure and composition of the gut microbiome of offspring steadily mature with increasing diversity during nursing and weaning (Sommer & Bäckhed, 2013). This period of microbiome assembly is critical for young mammals because the gut microbes they acquire will help train their immune system (Lathrop et al., 2011) with potential long‐lasting effects on their health (Cox et al., 2014). In an article in this issue of Molecular Ecology, Stoffel et al. (2020) investigated the gut microbiota of northern elephant seals (Mirounga angustirostris) during a key developmental window. A month after giving birth, elephant seal mothers stop nursing their pups and return to the sea. As a consequence, their pups go from a diet of milk rich in fat to abruptly enter a post weaning fasting period which lasts for about two months while they remain with the colony. This particular life‐history trait therefore offered the authors a unique and exciting opportunity to evaluate intrinsic factors contributing to gut microbiota development in a wild marine mammal.     

A genetic linkage map of the vervet monkey (Chlorocebus aethiops sabaeus)

The spectacular progress in genomics increasingly highlights the importance of comparative biology in biomedical research. In particular, nonhuman primates, as model systems, provide a crucial intermediate between humans and mice. The close similarities between humans and other primates are stimulating primate studies in virtually every area of biomedical research, including development, anatomy, physiology, immunology, and behavior. The vervet monkey (Chlorocebus aethiops sabaeus) is an important model for studying human diseases and complex traits, especially behavior. We have developed a vervet genetic linkage map to enable mapping complex traits in this model organism and facilitate comparative genomic analysis between vervet and other primates. Here we report construction of an initial genetic map built with about 360 human orthologous short tandem repeats (STRs) that were genotyped in 434 members of an extended vervet pedigree. The map includes 226 markers mapped in a unique order with a resolution of 9.8 Kosambi centimorgans (cM) in the vervet monkey genome, and with a total length (including all 360 markers) of 2726 cM. At least one complex and 11 simple rearrangements in marker order distinguish vervet chromosomes from human homologs. While inversions and insertions can explain a similar number of changes in marker order between vervet and rhesus homologs, mostly inversions are observed when vervet chromosome organization is compared to that in human and chimpanzee. Our results support the notion that large inversions played a less prominent role in the evolution within the group of the Old World monkeys compared to the human and chimpanzee lineages. Electronic supplementary material The online version of this article (doi: ) contains supplementary material, which is available to authorized users.     

Activation of nuclear factor kappa B in mammary epithelium promotes milk loss during mammary development and infection

We investigated whether nuclear factor kappa B (NF‐κB), which exhibits a regulated pattern of activity during murine mammary gland development, plays an important role during lactation and involution, when milk production ceases and the gland undergoes apoptosis and re‐modeling. We generated a doxycycline inducible transgenic mouse model to activate NF‐κB specifically in the mammary epithelium through expression of a constitutively active form of IKK2, the upstream kinase in the classical NF‐κB signaling cascade. We found that activation of NF‐κB during involution resulted in a more rapid reduction in milk levels and increased cleavage of caspase‐3, an indicator of apoptosis. We also found that activation of NF‐κB during lactation with no additional involution signals had a similar effect. The observation that NF‐κB is a key regulator of milk production led us to investigate the role of NF‐κB during mastitis, an infection of the mammary gland in which milk loss is observed. Mammary gland injection of E. coli LPS resulted in activation of NF‐κB and milk loss during lactation. This milk loss was decreased by selective inhibition of NF‐κB in mammary epithelium. Together, our data reveal that activation of NF‐κB leads to milk clearance in the lactating mammary gland. Therefore, targeting of NF‐κB signaling may prove therapeutic during mastitis in humans and could be beneficial for the dairy industry, where such infections have a major economic impact. J. Cell. Physiol. 222:73–81, 2010. © 2009 Wiley‐Liss, Inc.     

Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach,Diploptera punctata

The vertical transmission of microbes from mother to offspring is critical to the survival, development, and health of animals. Invertebrate systems offer unique opportunities to conduct studies on microbiome‐development‐reproduction dynamics since reproductive modes ranging from oviparity to multiple types of viviparity are found in these animals. One such invertebrate is the live‐bearing cockroach, Diploptera punctata. Females carry embryos in their brood sac, which acts as the functional equivalent of the uterus and placenta. In our study, 16S rRNA sequencing was used to characterize maternal and embryonic microbiomes as well as the development of the whole‐body microbiome across nymphal development. We identified 50 phyla and 121 classes overall and found that mothers and their developing embryos had significantly different microbial communities. Of particular interest is the notable lack of diversity in the embryonic microbiome, which is comprised exclusively of Blattabacteria, indicating microbial transmission of only this symbiont during gestation. Our analysis of postnatal development reveals that significant amounts of non‐Blattabacteria species are not able to colonize newborn D. punctata until melanization, after which the microbial community rapidly and dynamically diversifies. While the role of these microbes during development has not been characterized, Blattabacteria must serve a critical role providing specific micronutrients lacking in milk secretions to the embryos during gestation. This research provides insight into the microbiome development, specifically with relation to viviparity, provisioning of milk‐like secretions, and mother–offspring interactions during pregnancy.     

Small to modest impact of social group on the gut microbiome of wild Costa Rican capuchins in a seasonal forest

The horizontal transmission of pathogenic and beneficial microbes has implications for health and development of socially living animals. Social group is repeatedly implicated as an important predictor of gut microbiome structure among primates, with individuals in neighboring social groups exhibiting distinct microbiomes. Here we examine whether group membership is a predictor of gut microbiome structure and diversity across three groups of white‐faced capuchins (Cebus capucinus imitator) inhabiting a seasonal Costa Rican forest. We collected 62 fecal samples from 18 adult females during four sampling bouts. Sampling bouts spanned the dry‐to‐wet‐to‐dry seasonal transitions. To investigate gut microbial composition, we sequenced the V4 region of the 16S rRNA gene. We used the DADA2 pipeline to assign amplicon sequence variants and the RDP database to classify taxa. Our findings are: 1) gut microbiomes of capuchins clustered by social group in the late dry season, but this pattern was less evident in other sampling bouts; 2) social group was a significant variable in a PERMANOVA test of beta diversity, but it accounted for less variation than season; 3) social group was not an important predictor of abundance for the ten most abundant microbial taxa in capuchins; 4) when examining log2‐fold abundances of microbes between social groups, there were significant differences in some pairwise comparisons. While this is suggestive of group‐wide differences, individual variation may have a strong impact and should be assessed in future studies. Overall, we found a minor impact of social group membership on the gut microbiota of wild white‐faced capuchins. Future research including home range overlap and resource use, as well as fine‐scale investigation of individual variation, will further elucidate patterns of socially structured microbes.     

Are you what you eat? A highly transient and prey‐influenced gut microbiome in the grey house spider Badumna longinqua

Stable core microbial communities have been described in numerous animal species and are commonly associated with fitness benefits for their hosts. Recent research, however, highlights examples of species whose microbiota are transient and environmentally derived. Here, we test the effect of diet on gut microbial community assembly in the spider Badumna longinqua. Using 16S rRNA gene amplicon sequencing combined with quantitative PCR, we analyzed diversity and abundance of the spider's gut microbes, and simultaneously characterized its prey communities using nuclear rRNA markers. We found a clear correlation between community similarity of the spider's insect prey and gut microbial DNA, suggesting that microbiome assembly is primarily diet‐driven. This assumption is supported by a feeding experiment, in which two types of prey—crickets and fruit flies—both substantially altered microbial diversity and community similarity between spiders, but did so in different ways. After cricket consumption, numerous cricket‐derived microbes appeared in the spider's gut, resulting in a rapid homogenization of microbial communities among spiders. In contrast, few prey‐associated bacteria were detected after consumption of fruit flies; instead, the microbial community was remodelled by environmentally sourced microbes, or abundance shifts of rare taxa in the spider's gut. The reshaping of the microbiota by both prey taxa mimicked a stable core microbiome in the spiders for several weeks post feeding. Our results suggest that the spider's gut microbiome undergoes pronounced temporal fluctuations, that its assembly is dictated by the consumed prey, and that different prey taxa may remodel the microbiota in drastically different ways.     

Bacterial microbiome of Coptotermes curvignathus (Isoptera: Rhinotermitidae) reflects the coevolution of species and dietary pattern

Coptotermes curvignathus Holmgren is capable of feeding on living trees. This ability is attributed to their effective digestive system that is furnished by the termite's own cellulolytic enzymes and cooperative enzymes produced by their gut microbes. In this study, the identity of an array of diverse microbes residing in the gut of C. curvignathus was revealed by sequencing the near‐full‐length 16S rRNA genes. A total of 154 bacterial phylotypes were found. The Bacteroidetes was the most abundant phylum and accounted for about 65% of the gut microbial profile. This is followed by Firmicutes, Actinobacteria, Spirochetes, Proteobacteria, TM7, Deferribacteres, Planctomycetes, Verrucomicrobia, and Termite Group 1. Based on the phylogenetic study, this symbiosis can be a result of long coevolution of gut enterotypes with the phylogenic distribution, strong selection pressure in the gut, and other speculative pressures that determine bacterial biome to follow. The phylogenetic distribution of cloned rRNA genes in the bacterial domain that was considerably different from other termite reflects the strong selection pressures in the gut where a proportional composition of gut microbiome of C. curvignathus has established. The selection pressures could be linked to the unique diet preference of C. curvignathus that profoundly feeds on living trees. The delicate gut microbiome composition may provide available nutrients to the host as well as potential protection against opportunistic pathogen.     

The conflict between vervet monkeys and farmers at the forest edge in Entebbe, Uganda

Forty‐seven property owners in Entebbe, Uganda were questioned about vervet monkey activities on their property. Our main objective was to investigate the interactions between humans and vervet monkeys in an agricultural area adjacent to a forest zone. Other studies have reported that farms located within 300 m of a forested boundary probably incur the greatest risk of crop‐raiding. Two other factors that may influence susceptibility to vervet crop‐raiding were also examined: the types of crops grown and the types of direct preventative measures used. The effect of these two factors on vervet crop‐raiding is not straightforward. However, the distance a property is located from the forest edge is an important factor influencing vervet crop‐raiding. Surveyed gardens 200 m from the forest edge received significantly less crop‐raiding than farms located 100 m or 50 m (P = 0.040, < α = 0.05). We suggest that the development of nonagricultural activities on land directly adjacent to forested areas may reduce vervet crop‐raiding by deterring vervets from travelling greater distances from the forest edge due to increased obstacles or risks.     

Bacterial communities associated with honeybee food stores are correlated with land use

Microbial communities, associated with almost all metazoans, can be inherited from the environment. Although the honeybee (Apis mellifera L.) gut microbiome is well documented, studies of the gut focus on just a small component of the bee microbiome. Other key areas such as the comb, propolis, honey, and stored pollen (bee bread) are poorly understood. Furthermore, little is known about the relationship between the pollinator microbiome and its environment. Here we present a study of the bee bread microbiome and its relationship with land use. We estimated bacterial community composition using both Illumina MiSeq DNA sequencing and denaturing gradient gel electrophoresis (DGGE). Illumina was used to gain a deeper understanding of precise species diversity across samples. DGGE was used on a larger number of samples where the costs of MiSeq had become prohibitive and therefore allowed us to study a greater number of bee breads across broader geographical axes. The former demonstrates bee bread comprises, on average, 13 distinct bacterial phyla; Bacteroidetes, Firmicutes, Alpha‐proteobacteria, Beta‐proteobacteria, and Gamma‐proteobacteria were the five most abundant. The most common genera were Pseudomonas, Arsenophonus, Lactobacillus, Erwinia, and Acinetobacter. DGGE data show bacterial community composition and diversity varied spatially and temporally both within and between hives. Land use data were obtained from the 2007 Countryside Survey. Certain habitats, such as improved grasslands, are associated with low diversity bee breads, meaning that these environments may be poor sources of bee‐associated bacteria. Decreased bee bread bacterial diversity may result in reduced function within hives. Although the dispersal of microbes is ubiquitous, this study has demonstrated landscape‐level effects on microbial community composition.     

Daily lettuce supplements promote foraging behavior and modify the gut microbiota in captive frugivores

For captive primates, greater provisioning of leafy greens or foliage can promote natural foraging behavior while boosting fiber intake. Recalcitrant fiber, although minimally available to endogenous metabolism, is readily fermented into nutrients by gut microbes. Whereas most primates in captivity consume fiber-limited diets and harbor imbalanced gut microbiota compared to their wild conspecifics, the importance of fiber provisioning to primate gut microbiota has predominately been studied in folivores. We, therefore, determined if commercial lettuce could be used to encourage foraging behavior and modify the gut microbiota of captive frugivores. We provisioned ruffed lemurs (Varecia rubra and V. variegata) with romaine lettuce, on top of the standard dietary fare, for 10 consecutive days. Before and across the period of lettuce supplementation, we collected observational data of animal feeding and fecal samples for microbiome analysis, determined via amplicon sequencing. The ruffed lemurs and their gut microbes responded to lettuce provisioning. In particular, younger animals readily ate lettuce and showed no decline in consumption across study days. When controlling for the effects of host species and social-group membership, lettuce consumption shifted the composition of the gut microbiome away from each lemur's own baseline, an effect that became stronger as the study progressed. In the final study days, Ruminococcaceae UCG-008 and Akkermansia, microbes typically and respectively associated with fiber metabolism and host health, were significantly enriched in the consortia of lettuce-provisioned subjects. Ultimately, the routine offering of lettuce, leafy greens, or foliage to captive frugivores may benefit animal wellbeing.     

Between-partner concordance of vertically transmitted gut microbiota diminishes reproductive output in the dung beetle Onthophagus taurus

In this study, we explored the potential contribution of the gut microbiome to reproductive isolation in tunnelling dung beetles, using Onthophagus taurus (Schreber, 1759) and its sister species O. illyricus (Scopoli, 1763) as a model system (Coleoptera: Scarabaeidae: Scarabaeinae: Onthophagini). Gut microbiota play critical roles in normative development of these beetles, and are vertically inherited via a maternally derived faecal pellet called the pedestal. We first compared the developmental outcomes of individuals reared with pedestals derived from either the same or the sister species (Self and Cross inoculation treatments, respectively). We then crossed the resulting adult O. taurus in three combinations (Self female X Self male; Self female X Cross male; Cross female X Self male). We predicted that if the vertically transmitted gut microbiome plays a role in reproductive isolation by facilitating species recognition, the Self X Self line would have improved reproductive outcomes compared to the lines in which partners had mismatched gut microbiomes. Instead, we found that between-partner concordance of maternally transmitted gut microbiota resulted in fewer offspring, and that this reduction was due to partial pre-copulatory isolation as evidenced by reduced sperm transfer in the Self X Self line. This pattern is consistent either with microbiome-mediated familiarity/kin recognition, or with absence of mate choice in crosses with mismatched microbiomes. We discuss our results in the light of recent research on the influence of extracellular microbial symbionts over insects' mating preferences.     

Living in the suburbs: Space use by vervet monkeys (Chlorocebus pygerythrus) in an eco‐estate,South Africa

We examined vervet monkey (Chlorocebus pygerythrus) space use using GPS/UHF telemetry data from 10 vervet monkeys across six troops over 9 months within a 420 ha suburban eco‐estate. We documented a mean home range of 0.99 km² (95% MCP) and 1.07 km² (95% KDE) for females (n = 6), 1 km² (95% MCP) and 1.50 km² (95% KDE) for males (n = 4) and 0.87 km² (95% MCP) and 1.12 km² (95% KDE) for troops (n = 6), respectively, indicating that males and larger troops had larger home ranges. These relatively small home ranges included shared territorial boundaries and high home range overlap. Vervet monkey movements indicated higher morning activity levels, and habitat selection indicated significantly more use of golf course, urban residential and forest, thicket and woodland areas, and avoidance of wetland, grassland and shrub, and urban built‐up areas. Our results suggest that modified habitat use by vervet monkeys is a consequence of behavioural facilitation to access highly available food resources, thereby facilitating their persistence in green spaces in urban areas of South Africa. Conflict management is dependent on the conservation of sufficient natural habitats and food resources, to minimise their dependence on anthropogenic supplementary food resources and consequently reduce human–monkey conflict.     

Early life feeding accelerates gut microbiome maturation and suppresses acute post-weaning stress in piglets

Early life microbiome perturbations can have important effects on host development, physiology and behaviour. In this longitudinal study, we evaluated the impact of early feeding on gut microbiome colonization in neonatal piglets. Early-fed (EF) piglets had access to a customized fibrous diet from 2 days after birth until weaning in addition to mother's milk, whereas control piglets suckled mother's milk only. Rectal swabs were collected at multiple time points until 6 weeks of age to investigate microbiota development using 16S rRNA gene profiling. The dynamic pre-weaning microbiota colonization was followed by a relatively stable post-weaning microbiota, represented by Prevotella, Roseburia, Faecalibacterium, Ruminococcus, Megasphaera, Catenibacterium and Subdoligranulum. EF piglets showed an accelerated microbiota maturation, characterized by increased microbial diversity, pre-weaning emergence of post-weaning-associated microbes and a more rapid decline of typical pre-weaning microbes. Furthermore, the individual eating behaviour scores of piglets quantitatively correlated with their accelerated microbiome. Importantly, EF piglets displayed a smoother relative weight gain and tended to reach a higher relative weight gain, in addition to reduced diarrhoea scores in the first week post-weaning. Overall, these findings demonstrate the beneficial impact of early feeding on microbiota development as well as pig health and performance during the weaning transition.     

Genome shrinkage and loss of nutrient-providing potential in the obligate symbiont of the primitive termite Mastotermes darwiniensis

Beneficial microbial associations with insects are common and are classified as either one or a few intracellular species that are vertically transmitted and reside intracellularly within specialized organs or as microbial assemblages in the gut. Cockroaches and termites maintain at least one if not both beneficial associations. Blattabacterium is a flavobacterial endosymbiont of nearly all cockroaches and the termite Mastotermes darwiniensis and can use nitrogenous wastes in essential amino acid and vitamin biosynthesis. Key changes during the evolutionary divergence of termites from cockroaches are loss of Blattabacterium, diet shift to wood, acquisition of a specialized hindgut microbiota, and establishment of advanced social behavior. Termite gut microbes collaborate to fix nitrogen, degrade lignocellulose, and produce nutrients, and the absence of Blattabacterium in nearly all termites suggests that its nutrient-provisioning role has been replaced by gut microbes. M. darwiniensis is a basal, extant termite that solely retains Blattabacterium, which would show evidence of relaxed selection if it is being supplanted by the gut microbiome. This termite-associated Blattabacterium genome is ～8% smaller than cockroach-associated Blattabacterium genomes and lacks genes underlying vitamin and essential amino acid biosynthesis. Furthermore, the M. darwiniensis gut microbiome membership is more consistent between individuals and includes specialized termite gut-associated bacteria, unlike the more variable membership of cockroach gut microbiomes. The M. darwiniensis Blattabacterium genome may reflect relaxed selection for some of its encoded functions, and the loss of this endosymbiont in all remaining termite genera may result from its replacement by a functionally complementary gut microbiota.