Host Phylogeny Research Articles

Functional host-specific adaptation of the intestinal microbiome in hominids

Fine-scale knowledge of the changes in composition and function of the human gut microbiome compared that of our closest relatives is critical for understanding the evolutionary processes underlying its developmental trajectory. To infer taxonomic and functional changes in the gut microbiome across hominids at different timescales, we perform high-resolution metagenomic-based analyzes of the fecal microbiome from over two hundred samples including diverse human populations, as well as wild-living chimpanzees, bonobos, and gorillas. We find human-associated taxa depleted within non-human apes and patterns of host-specific gut microbiota, suggesting the widespread acquisition of novel microbial clades along the evolutionary divergence of hosts. In contrast, we reveal multiple lines of evidence for a pervasive loss of diversity in human populations in correlation with a high Human Development Index, including evolutionarily conserved clades. Similarly, patterns of co-phylogeny between microbes and hosts are found to be disrupted in humans. Together with identifying individual microbial taxa and functional adaptations that correlate to host phylogeny, these findings offer insights into specific candidates playing a role in the diverging trajectories of the gut microbiome of hominids. We find that repeated horizontal gene transfer and gene loss, as well as the adaptation to transient microaerobic conditions appear to have played a role in the evolution of the human gut microbiome.

Gut diazotrophs in lagomorphs are associated with season but not altitude and host phylogeny.

Invertebrates such as termites feeding on nutrient-poor substrate receive essential nitrogen by biological nitrogen fixation of gut diazotrophs. However, the diversity and composition of gut diazotrophs of vertebrates such as Plateau pikas living in nutrient-poor Qinghai-Tibet Plateau remain unknown. To fill this knowledge gap, we studied gut diazotrophs of Plateau pikas (Ochotona curzoniae) and its related species, Daurian pikas (Ochotona daurica), Hares (Lepus europaeus) and Rabbits (Oryctolagus cuniculus) by high-throughput amplicon sequencing methods. We analyzed whether the gut diazotrophs of Plateau pikas are affected by season, altitude, and species, and explored the relationship between gut diazotrophs and whole gut microbiomes. Our study showed that Firmicutes, Spirochaetes, and Euryarchaeota were the dominant gut diazotrophs of Plateau pikas. The beta diversity of gut diazotrophs of Plateau pikas was significantly different from the other three lagomorphs, but the alpha diversity did not show a significant difference among the four lagomorphs. The gut diazotrophs of Plateau pikas were the most similarly to that of Rabbits, followed by Daurian pikas and Hares, which was inconsistent with gut microbiomes or animal phylogeny. The dominant gut diazotrophs of the four lagomorphs may reflect their living environment and dietary habits. Season significantly affected the alpha diversity and abundance of dominant gut diazotrophs. Altitude had no significant effect on the gut diazotrophs of Plateau pikas. In addition, the congruence between gut microbiomes and gut diazotrophs was low. Our results proved that the gut of Plateau pikas was rich in gut diazotrophs, which is of great significance for the study of ecology and evolution of lagomorphs.

Molecular Characterisation of Faecal Bacterial Assemblages Among Four Species of Syntopic Odonates

Factors such as host species, phylogeny, diet, and both timing and location of sampling are thought to influence the composition of gut-associated bacteria in insects. In this study, we compared the faecal-associated bacterial taxa for three Coenagrion and one Enallagma damselfly species. We expected high overlap in representation of bacterial taxa due to the shared ecology and diet of these species. Using metabarcoding based on the 16S rRNA gene, we identified 1513 sequence variants, representing distinct bacterial ‘taxa’. Intriguingly, the damselfly species showed somewhat different magnitudes of richness of ZOTUs, ranging from 480 to 914 ZOTUs. In total, 921 (or 60.8% of the 1513) distinct ZOTUs were non-shared, each found only in one species, and then most often in only a single individual. There was a surfeit of these non-shared incidental ZOTUs in the Enallagma species accounting for it showing the highest bacterial richness and accounting for a sample-wide pattern of more single-species ZOTUs than expected, based on comparisons to the null model. Future studies should address the extent to which faecal bacteria represent non-incidental gut bacteria and whether abundant and shared taxa are true gut symbionts.Graphical Pictures of odonates adopted from Norske Art databank under Creative Commons License (CC BY 4.0).

Evaluation of Genetic Diversity in Quill Mites of the Genus Syringophiloidus Kethley, 1970 (Prostigmata: Syringophilidae) with Six New-to-Science Species.

Quill mites (Acariformes: Syringophilidae) are poorly explored bird parasites. Syringophiloidus Kethley, 1970, is the most specious and widespread genus in this family. It is believed to contain mono-, steno- and poly-xenous parasites and thus seems to be an exemplary for studies on biodiversity and host associations. In this work, we applied the DNA barcode marker (mitochondrial cytochrome c oxidase subunit I gene fragment, COI) to analyze the species composition and host specificity of representatives of fifteen Syringophiloidus populations parasitizing fifteen bird species. The neighbor joining analyses distinguished thirteen monophyletic lineages, almost completely corresponding to seven previously known species recognized based on morphological features, and six new-to-science species. The only exception is S. amazilia Skoracki, 2017, which is most likely conspecific with Syringophiloidus stawarczyki Skoracki, 2004. The intraspecific distances of all species were not higher than 0.9%, whilst the interspecific diversity ranged from 5.9% to 19.2% and 6.3-22.4%, inferred as the distances p and K2P, respectively. Although all putative species (except S. amazilia) are highly supported, the relationships between them have not been fully resolved and only faintly indicate that both host phylogeny and distributions influence the phylogenetic structure of quill mite taxa.

Foliar endophyte diversity in Eastern Asian-Eastern North American disjunct tree species - influences of host identity, environment, phylogeny, and geographic isolation.

The well-known eastern Asian (EA) and eastern North American (ENA) floristic disjunction provides a unique system for biogeographic and evolutionary studies. Despite considerable interest in the disjunction, few studies have investigated the patterns and their underlying drivers of allopatric divergence in sister species or lineages isolated in the two areas. Endophyte diversity and assembly in disjunct sister taxa, as an ecological trait, may have played an important role in the processes of allopatric evolution, but no studies have examined endophytes in these lineages. Here we compared foliar endophytic fungi and bacteria-archaea (FEF and FEB) in 17 EA-ENA disjunct species or clade pairs from genera representing conifers and 10 orders of five major groups of angiosperms and 23 species of Cornus from EA and North America. Metagenomic sequencing of fungal ITS and bacterial-archaeal 16S rDNA was used to capture the foliar endophytic communities. Alpha and beta diversity of fungi and bacteria were compared at multiple scales and dimensions to gain insights into the relative roles of historical geographic isolation, host identity, phylogeny, and environment from samples at different sites in shaping endophytic diversity patterns. We found that beta diversity of endophytes varied greatly among plant individuals within species and between species among genera at the same sampling site, and among three sampling sites, but little variation between region-of-origin of all plant species (EA vs ENA) and between EA-ENA disjunct counterparts within genera. Various numbers of indicator fungal species differing in abundance were identified for each plant genus and Cornus species. An overall significant correlation between endophyte community dissimilarity and phylogenetic distance of plants was detected among the disjunct genera but not among species of Cornus. However, significant correlations between beta diversities at different taxonomic scales of endophytes and phylogenetic distances of Cornus species were observed. Our results suggest important roles of host identity and environment (sampling sites), and a likely minor role of phylogenetic divergence and historical biogeographic isolation in shaping the pattern of foliar endophyte diversity and assembly in the EA-ENA disjunct genera and Cornus. The results lead to a hypothesis that the sister taxa in EA and ENA likely differ in FEF and FEB when growing in native habitats due to differences in local environments, which may potentially drive allopatric divergence of the functional features of species.

The effects of host ecology and phylogeny on gut microbiota (non)parallelism across birds and mammals.

What are the roles of determinism and contingency in evolution? The paleontologist and evolutionary biologist Stephen J. Gould raised this question in his famous thought experiment of "replaying life's tape." Settings where independent lineages have repeatedly adapted to similar ecological niches (i.e., parallel evolution) are well suited to address this question. Here, we quantified whether repeated ecological shifts across 53 mammalian and 50 avian host species are associated with parallel gut microbiota changes. Our results indicate that parallel shifts in host diet are associated with greater gut microbiota parallelism (i.e., more deterministic). While further research will be necessary to obtain a comprehensive picture of the circumstances under which deterministic gut microbiota changes might be expected, our study can be instrumental in motivating the use of more quantitative methods in microbiota research. This, in turn, can help us better understand microbiota dynamics during adaptive evolution of their hosts.

Patterns of host-parasite associations between marine meiofaunal flatworms (Platyhelminthes) and rhytidocystids (Apicomplexa)

Microturbellarians are abundant and ubiquitous members of marine meiofaunal communities around the world. Because of their small body size, these microscopic animals are rarely considered as hosts for parasitic organisms. Indeed, many protists, both free-living and parasitic ones, equal or surpass meiofaunal animals in size. Despite several anecdotal records of “gregarines”, “sporozoans”, and “apicomplexans” parasitizing microturbellarians in the literature—some of them dating back to the nineteenth century—these single-celled parasites have never been identified and characterized. More recently, the sequencing of eukaryotic microbiomes in microscopic invertebrates have revealed a hidden diversity of protist parasites infecting microturbellarians and other meiofaunal animals. Here we show that apicomplexans isolated from twelve taxonomically diverse rhabdocoel taxa and one species of proseriate collected in four geographically distinct areas around the Pacific Ocean (Okinawa, Hokkaido, and British Columbia) and the Caribbean Sea (Curaçao) all belong to the apicomplexan genus Rhytidocystis. Based on comprehensive molecular phylogenies of Rhabdocoela and Proseriata inferred from both 18S and 28S rDNA sequences, as well as a molecular phylogeny of Marosporida inferred from 18S rDNA sequences, we determine the phylogenetic positions of the microturbellarian hosts and their parasites. Multiple lines of evidence, including morphological and molecular data, show that at least nine new species of Rhytidocystis infect the microturbellarian hosts collected in this study, more than doubling the number of previously recognized species of Rhytidocystis, all of which infect polychaete hosts. A cophylogenetic analysis examining patterns of phylosymbiosis between hosts and parasites suggests a complex picture of overall incongruence between host and parasite phylogenies, and varying degrees of geographic signals and taxon specificity.

Host species and habitat shape fish-associated bacterial communities: phylosymbiosis between fish and their microbiome

BackgroundWhile many studies have reported that the structure of the gut and skin microbiota is driven by both species-specific and habitat-specific factors, the relative importance of host-specific versus environmental factors in wild vertebrates remains poorly understood. The aim of this study was to determine the diversity and composition of fish skin, gut, and surrounding water bacterial communities (hereafter referred to as microbiota) and assess the extent to which host habitat and phylogeny predict microbiota similarity. Skin swabs and gut samples from 334 fish belonging to 17 species were sampled in three Laurentian Great Lakes (LGLs) habitats (Detroit River, Lake Erie, Lake Ontario). We also collected and filtered water samples at the time of fish collection. We analyzed bacterial community composition using 16S metabarcoding and tested for community variation.ResultsWe found that the water microbiota was distinct from the fish microbiota, although the skin microbiota more closely resembled the water microbiota. We also found that environmental (sample location), habitat, fish diet, and host species factors shape and promote divergence or convergence of the fish microbiota. Since host species significantly affected both gut and skin microbiota (separately from host species effects), we tested for phylosymbiosis using pairwise host species phylogenetic distance versus bacterial community dissimilarity. We found significant phylogenetic effects on bacterial community dissimilarity, consistent with phylosymbiosis for both the fish skin and gut microbiota, perhaps reflecting the longstanding co-evolutionary relationship between the host species and their microbiomes.ConclusionsAnalyzing the gut and skin mucus microbiota across diverse fish species in complex natural ecosystems such as the LGLs provides insights into the potential for habitat and species-specific effects on the microbiome, and ultimately the health, of the host.13rgRWqcw5pvG7aonCbZg2Video

Characterization of the soil resistome and mobilome in Namib Desert soils

The study of the soil resistome is important in understanding the evolution of antibiotic resistance and its dissemination between the clinic and the environment. However, very little is known about the soil resistome, especially of those from deserts. Here, we characterize the bacterial communities, using targeted sequencing of the 16S rRNA genes, and both the resistome and the mobilome in Namib Desert soils, using shotgun metagenomics. We detected a variety of antibiotic resistance genes (ARGs) that conferred resistance to antibiotics such as elfamycin, rifampicin, and fluoroquinolones, metal/biocide resistance genes (MRGs/BRGs) conferring resistance to metals such as arsenic and copper, and mobile genetic elements (MGEs) such as the ColE1-like plasmid. The presence of metal/biocide resistance genes in close proximity to ARGs indicated a potential for co-selection of resistance to antibiotics and metals/biocides. The co-existence of MGEs and horizontally acquired ARGs most likely contributed to a decoupling between bacterial community composition and ARG profiles. Overall, this study indicates that soil bacterial communities in Namib Desert soils host a diversity of resistance elements and that horizontal gene transfer, rather than host phylogeny, plays an essential role in their dynamics.

Influence of social lifestyles on host-microbe symbioses in the bees.

Microbiomes are increasingly recognised as critical for the health of an organism. In eusocial insect societies, frequent social interactions allow for high-fidelity transmission of microbes across generations, leading to closer host-microbe coevolution. The microbial communities of bees with other social lifestyles are less studied, and few comparisons have been made between taxa that vary in social structure. To address this gap, we leveraged a cloud-computing resource and publicly available transcriptomic data to conduct a survey of microbial diversity in bee samples from a variety of social lifestyles and taxa. We consistently recover the core microbes of well-studied corbiculate bees, supporting this method's ability to accurately characterise microbial communities. We find that the bacterial communities of bees are influenced by host location, phylogeny and social lifestyle, although no clear effect was found for fungal or viral microbial communities. Bee genera with more complex societies tend to harbour more diverse microbes, with Wolbachia detected more commonly in solitary tribes. We present a description of the microbiota of Euglossine bees and find that they do not share the "corbiculate core" microbiome. Notably, we find that bacteria with known anti-pathogenic properties are present across social bee genera, suggesting that symbioses that enhance host immunity are important with higher sociality. Our approach provides an inexpensive means of exploring microbiomes of a given taxa and identifying avenues for further research. These findings contribute to our understanding of the relationships between bees and their associated microbial communities, highlighting the importance of considering microbiome dynamics in investigations of bee health.

Phylosymbiosis: The Eco-Evolutionary Pattern of Insect-Symbiont Interactions.

Insects harbor diverse assemblages of bacterial and fungal symbionts, which play crucial roles in host life history. Insects and their various symbionts represent a good model for studying host-microbe interactions. Phylosymbiosis is used to describe an eco-evolutionary pattern, providing a new cross-system trend in the research of host-associated microbiota. The phylosymbiosis pattern is characterized by a significant positive correlation between the host phylogeny and microbial community dissimilarities. Although host-symbiont interactions have been demonstrated in many insect groups, our knowledge of the prevalence and mechanisms of phylosymbiosis in insects is still limited. Here, we provide an order-by-order summary of the phylosymbiosis patterns in insects, including Blattodea, Coleoptera, Diptera, Hemiptera, Hymenoptera, and Lepidoptera. Then, we highlight the potential contributions of stochastic effects, evolutionary processes, and ecological filtering in shaping phylosymbiotic microbiota. Phylosymbiosis in insects can arise from a combination of stochastic and deterministic mechanisms, such as the dispersal limitations of microbes, codiversification between symbionts and hosts, and the filtering of phylogenetically conserved host traits (incl., host immune system, diet, and physiological characteristics).

Microclimate shapes the phylosymbiosis of rodent gut microbiota in Jordan’s Great Rift Valley

Host phylogeny and the environment play vital roles in shaping animal microbiomes. However, the effects of these variables on the diversity and richness of the gut microbiome in different bioclimatic zones remain underexplored. In this study, we investigated the effects of host phylogeny and bioclimatic zone on the diversity and composition of the gut microbiota of two heterospecific rodent species, the spiny mouse Acomys cahirinus and the house mouse Mus musculus, in three bioclimatic zones of the African Great Rift Valley (GRV). We confirmed host phylogeny using the D-loop sequencing method and analyzed the influence of host phylogeny and bioclimatic zone parameters on the rodent gut microbiome using high-throughput amplicon sequencing of 16S rRNA gene fragments. Phylogenetic analysis supported the morphological identification of the rodents and revealed a marked genetic difference between the two heterospecific species. We found that bioclimatic zone had a significant effect on the gut microbiota composition while host phylogeny did not. Microbial alpha diversity of heterospecific hosts was highest in the Mediterranean forest bioclimatic zone, followed by the Irano–Turanian shrubland, and was lowest in the Sudanian savanna tropical zone. The beta diversity of the two rodent species showed significant differences across the Mediterranean, Irano–Turanian, and Sudanian regions. The phyla Firmicutes and Bacteroidetes were highly abundant, and Deferribacterota, Cyanobacteria and Proteobacteria were also prominent. Amplicon sequence variants (ASVs) were identified that were unique to the Sudanian bioclimatic zone. The core microbiota families recovered in this study were consistent among heterospecific hosts. However, diversity decreased in conspecific host populations found at lower altitudes in Sudanian bioclimatic zone. The composition of the gut microbiota is linked to the adaptation of the host to its environment, and this study underscores the importance of incorporating climatic factors such as elevation and ambient temperature, in empirical microbiome research and is the first to describe the rodent gut microbiome from the GRV.

The functional traits of host fish can act as good predictors for parasite composition in a neotropical floodplain.

Parasite diversity can be influenced by the interaction of environmental factors and host traits, but understanding which traits can be decisive for the establishment of the parasite may provide subsidies fora better understanding of the host-parasite relationship. In this study, we investigated whether functional traits, diet, and host phylogeny can predict the similarity of the endoparasite composition of a fish assemblage in a Brazilian floodplain. Of the three evaluated components, the host's diet was the factor that showed the greatest influence on the composition and similarity of endoparasites, demonstrating the highest value of the explanation. The functional traits and phylogeny, despite presenting significant values (unique effect and global effect), showed low explainability in the composition of the endoparasites. When analyzing the joint effects, all components showed significant influence. Hosts that live in the same environment that are phylogenetically related and have a similar ecology have a certain degree of homogeneity in their parasite assemblages and, because they are endoparasites (which are acquired trophically along the chain), diet is the main driver of parasite richness and similarity. Overall, host traits can be one of the main determinants of parasite composition, so studies that address the functional traits of the host provide a representation of local diversity and define the possible patterns of these parasite communities.

Conserved, yet disruption-prone, gut microbiomes in neotropical bumblebees.

Social bees are an important model for the ecology and evolution of gut microbiomes. These bees harbor ancient, specific, and beneficial gut microbiomes and are crucial pollinators. However, most of the research has concentrated on managed honeybees and bumblebees in the temperate zone. Here we used 16S rRNA gene sequencing to characterize gut microbiomes in wild neotropical bumblebee communities from Colombia. We also analyzed drivers of microbiome structure across our data and previously published data from temperate bumblebees. Our results show that lineages of neotropical bumblebees not only retained their ancient gut bacterial symbionts during dispersal from North America but also are prone to major disruption, a shift that is strongly associated with parasite infection. Finally, we also found that microbiomes are much more strongly structured by host phylogeny than by geography, despite the very different environmental conditions and plant communities in the two regions.

Host phylogeny and environment shape the diversity of salamander skin bacterial communities

The composition and diversity of animal-associated microbial communities are shaped by multiple ecological and evolutionary processes acting at different spatial and temporal scales. Skin microbiomes are thought to be strongly influenced by the environment due to the direct interaction of the host’s skin with the external media. As expected, the diversity of amphibian skin microbiomes is shaped by climate and host sampling habitats, whereas phylogenetic effects appear to be weak. However, the relative strength of phylogenetic and environmental effects on salamander skin microbiomes remains poorly understood. Here, we analysed sequence data from 1164 adult salamanders of 44 species to characterise and compare the diversity and composition of skin bacteria. We assessed the relative contribution of climate, host sampling habitat, and host phylogeny to the observed patterns of bacterial diversity. We found that bacterial alpha diversity was mainly associated with host sampling habitat and climate, but that bacterial beta diversity was more strongly associated with host taxonomy and phylogeny. This phylogenetic effect predominantly occurred at intermediate levels of host divergence (0–50 Mya). Our results support the importance of environmental factors shaping the diversity of salamander skin microbiota, but also support host phylogenetic history as a major factor shaping these bacterial communities.

DO PARASITIC LICE EXHIBIT ENDEMISM IN PARALLEL WITH THEIR AVIAN HOSTS? A COMPARISON ACROSS NORTHERN AMAZONIAN AREAS OF ENDEMISM.

Areas of endemism are the smallest units in biogeography and can be defined as biologically unique areas comprising taxa with common geographic limits to their distributions. High beta diversity within Amazonia is often related to turnover among these areas. For decades, evolutionary biologists have tried to comprehend the mechanisms generating and maintaining the spatial structure and high diversity of free-living Amazonian organisms, particularly birds. However, few studies have tried to analyze these patterns among their parasites. Host and parasite associations involve shared history that may allow us to better understand the fine-scale evolutionary history of the host. Here we compare the coevolutionary patterns among 2 avian host species with distinct patterns of genetic structure in northern Amazonia, Dendrocincla fuliginosa (Aves: Dendrocolaptidae) and Dixiphia pipra (Aves: Pipridae), and their ectoparasitic lice (Insecta: Phthiraptera), Furnaricola sp. ex Dendrocincla fuliginosa, Myrsidea sp. ex Dixiphia pipra, and Tyranniphilopterus sp. ex Dixiphia pipra. We obtained sequences of the mitochondrial gene cytochrome oxidase subunit I from hosts and parasites collected on opposite banks of the Negro and Japurá rivers, which delimit 3 areas of endemism in northern Amazonia: Napo, Jau, and Guiana. Our results demonstrate that the Negro River is a geographical barrier for both Furnaricola sp. and its avian host, Dendrocincla fuliginosa. Phylogenies of both hosts, Dendrocincla fuliginosa, and the parasites, Furnaricola sp., show monophyletic clades on opposite margins of the river that are not sister taxa. These clades have a mean uncorrected p-distance of 17.8% for Furnaricola sp. and 6.0% for Dendrocincla fuliginosa. Thus, these parasite clades constitute distinct evolutionary lineages and may even be distinct species. In contrast, Dixiphia pipra has no population structure associated with either river. Accordingly, data from their lice Myrsidea sp. indicate weak support for different clades on opposite margins of the Negro River, whereas data from their lice Tyranniphilopterus sp. indicate weak structure across the Japurá. This study is a first step toward understanding the effects of biogeographic history on permanent ectoparasites and suggests that host biogeographic history is to some extent a determinant of the parasite's history. Furthermore, the parasite's evolutionary history is an additional source of information about their hosts' evolution in this highly diverse region of northern Amazonia.

The microbiome of African penguins (Spheniscus demersus) under managed care resembles that of wild marine mammals and birds

Animals under managed care in zoos and aquariums are ideal surrogate study subjects for endangered species that are difficult to obtain in the wild. We compared the fecal and oral microbiomes of healthy, managed African penguins (Spheniscus demersus) to those of other domestic and wild vertebrate hosts to determine how host identity, diet, and environment shape the penguin microbiome. The African penguin oral microbiome was more similar to that of piscivorous marine mammals, suggesting that diet and a marine environment together play a strong role in shaping the oral microbiome. Conversely, the penguin cloaca/fecal microbiome was more similar to that of other birds, suggesting that host phylogeny plays a significant role in shaping the gut microbiome. Although the penguins were born under managed care, they had a gut microbiome more similar to that of wild bird species compared to domesticated (factory-farmed) birds, suggesting that the managed care environment and diet resemble those experienced by wild birds. Finally, the microbiome composition at external body sites was broadly similar to that of the habitat, suggesting sharing of microbes between animals and their environment. Future studies should link these results to microbial functional capacity and host health, which will help inform conservation efforts.

Effect of altitude and spatial heterogeneity on the host-parasite relationship in anurans from a remnant humid forest in the brazilian semiarid.

In the present study, we investigated the effect of habitat heterogeneity, elevation gradient, and phylogenetic distance of host species on the abundance and richness of anuran endoparasites, assuming that parasites follow the distribution of their hosts independently of environmental variation. We collected 192 anurans distributed in three altitude ranges: 100-200m, 400-500m, and 700-800m. We performed discriminant principal component analysis to analyze the interrelationships between environmental heterogeneity and the distribution of parasite and host species in the formation of species groups in each altitude range. We estimated the niche width and parasite overlap, using host species as a variable, and assessed whether parasite abundance is more influenced by historical (distance host phylogeny) or ecological effects in each altitude category and overall. Finally, we use network analyses to understand how interactions between parasites and hosts are formed along the altitude gradient. We found 22 parasite species, and the overall prevalence of infection was 74%. In our study, we did not identify environmental (altitude gradients and heterogeneity) or phylogenetic effects acting on the parasite species diversity. Overall, our results suggest that the parasites are distributed following the dispersal of their hosts and are dispersed among most anuran species.

Host phylogeny shapes viral transmission networks in an island ecosystem

Virus transmission between host species underpins disease emergence. Both host phylogenetic relatedness and aspects of their ecology, such as species interactions and predator–prey relationships, may govern rates and patterns of cross-species virus transmission and hence zoonotic risk. To address the impact of host phylogeny and ecology on virus diversity and evolution, we characterized the virome structure of a relatively isolated island ecological community in Fiordland, New Zealand, that are linked through a food web. We show that phylogenetic barriers that inhibited cross-species virus transmission occurred at the level of host phyla (between the Chordata, Arthropoda and Streptophyta) as well as at lower taxonomic levels. By contrast, host ecology, manifest as predator–prey interactions and diet, had a smaller influence on virome composition, especially at higher taxonomic levels. The virus–host community comprised a ‘small world’ network, in which hosts with a high diversity of viruses were more likely to acquire new viruses, and generalist viruses that infect multiple hosts were more likely to infect additional species compared to host specialist viruses. Such a highly connected ecological community increases the likelihood of cross-species virus transmission, particularly among closely related species, and suggests that host generalist viruses present the greatest risk of disease emergence.

Reservoir host immunology and life history shape virulence evolution in zoonotic viruses.

The management of future pandemic risk requires a better understanding of the mechanisms that determine the virulence of emerging zoonotic viruses. Meta-analyses suggest that the virulence of emerging zoonoses is correlated with but not completely predictable from reservoir host phylogeny, indicating that specific characteristics of reservoir host immunology and life history may drive the evolution of viral traits responsible for cross-species virulence. In particular, bats host viruses that cause higher case fatality rates upon spillover to humans than those derived from any other mammal, a phenomenon that cannot be explained by phylogenetic distance alone. In order to disentangle the fundamental drivers of these patterns, we develop a nested modeling framework that highlights mechanisms that underpin the evolution of viral traits in reservoir hosts that cause virulence following cross-species emergence. We apply this framework to generate virulence predictions for viral zoonoses derived from diverse mammalian reservoirs, recapturing trends in virus-induced human mortality rates reported in the literature. Notably, our work offers a mechanistic hypothesis to explain the extreme virulence of bat-borne zoonoses and, more generally, demonstrates how key differences in reservoir host longevity, viral tolerance, and constitutive immunity impact the evolution of viral traits that cause virulence following spillover to humans. Our theoretical framework offers a series of testable questions and predictions designed to stimulate future work comparing cross-species virulence evolution in zoonotic viruses derived from diverse mammalian hosts.