Host Evolutionary History Research Articles

Host diet and evolutionary history explain different aspects of gut microbiome diversity among vertebrate clades

Multiple factors modulate microbial community assembly in the vertebrate gut, though studies disagree as to their relative contribution. One cause may be a reliance on captive animals, which can have very different gut microbiomes compared to their wild counterparts. To resolve this disagreement, we analyze a new, large, and highly diverse animal distal gut 16 S rRNA microbiome dataset, which comprises 80% wild animals and includes members of Mammalia, Aves, Reptilia, Amphibia, and Actinopterygii. We decouple the effects of host evolutionary history and diet on gut microbiome diversity and show that each factor modulates different aspects of diversity. Moreover, we resolve particular microbial taxa associated with host phylogeny or diet and show that Mammalia have a stronger signal of cophylogeny. Finally, we find that environmental filtering and microbe-microbe interactions differ among host clades. These findings provide a robust assessment of the processes driving microbial community assembly in the vertebrate intestine.

Terrestriality and bacterial transfer: a comparative study of gut microbiomes in sympatric Malagasy mammals

The gut microbiomes of mammals appear to mirror their hosts’ phylogeny, suggesting host-driven microbial community assembly. Yet, much of this evidence stems from comparative studies of distinct wild or captive populations that lack data for disentangling the relative influences of shared phylogeny and environment. Here, we present phylogenetic and multivariate analyses of gut microbiomes from six sympatric (i.e., co-occurring) mammal species inhabiting a 1-km2 area in western Madagascar—three lemur and three non-primate species—that consider genetic, dietary, and ecological predictors of microbiome functionality and composition. Host evolutionary history, indeed, appears to shape gut microbial patterns among both closely and distantly related species. However, we also find that diet—reliance on leaves versus fruit—is the best predictor of microbiome similarity among closely related lemur species, and that host substrate use—ground versus tree—constrains horizontal transmission via incidental contact with feces, with arboreal species harboring far more distinct communities than those of their terrestrial and semi-terrestrial counterparts.

Dynamic microbiome evolution in social bees.

The highly social (eusocial) corbiculate bees, comprising the honey bees, bumble bees, and stingless bees, are ubiquitous insect pollinators that fulfill critical roles in ecosystem services and human agriculture. Here, we conduct wide sampling across the phylogeny of these corbiculate bees and reveal a dynamic evolutionary history behind their microbiota, marked by multiple gains and losses of gut associates, the presence of generalist as well as host-specific strains, and patterns of diversification driven, in part, by host ecology (for example, colony size). Across four continents, we found that different host species have distinct gut communities, largely independent of geography or sympatry. Nonetheless, their microbiota has a shared heritage: The emergence of the eusocial corbiculate bees from solitary ancestors appears to coincide with the acquisition of five core gut bacterial lineages, supporting the hypothesis that host sociality facilitates the development and maintenance of specialized microbiomes.

Coprological survey of parasites of free-ranging jaguar (Panthera onca) and puma (Puma concolor) inhabiting 2 types of tropical forests in Mexico

This study presents a coproparasitological survey of free-ranging jaguars (Panthera onca) and pumas (Puma concolor) inhabiting 2 types of tropical forest in southeastern Mexico. We examined 167 fecal samples (68=jaguar; 33=puma; 66=unidentified large felids), and identified 16 parasitic taxa, 56% of which were nematodes. We compared parasite community composition and prevalence between host species and forest types, and found that parasitic communities of jaguar and puma were more similar between host species in the same forest type than among conspecific hosts inhabiting different forest types. Possible determinants for the observed patterns could include ecosystem differences and host evolutionary history, as well as disparate diet and habitat use of these 2 felines. Further studies are needed for a more accurate estimation of the parasitic community composition of these felines, and for a better comprehension of the effects that habitat perturbation could have on the ecology and transmission of parasitic diseases, and the related consequences for the conservation of wild felines.

Phylosymbiosis: Relationships and Functional Effects of Microbial Communities across Host Evolutionary History.

Phylosymbiosis was recently proposed to describe the eco-evolutionary pattern, whereby the ecological relatedness of host-associated microbial communities parallels the phylogeny of related host species. Here, we test the prevalence of phylosymbiosis and its functional significance under highly controlled conditions by characterizing the microbiota of 24 animal species from four different groups (Peromyscus deer mice, Drosophila flies, mosquitoes, and Nasonia wasps), and we reevaluate the phylosymbiotic relationships of seven species of wild hominids. We demonstrate three key findings. First, intraspecific microbiota variation is consistently less than interspecific microbiota variation, and microbiota-based models predict host species origin with high accuracy across the dataset. Interestingly, the age of host clade divergence positively associates with the degree of microbial community distinguishability between species within the host clades, spanning recent host speciation events (~1 million y ago) to more distantly related host genera (~108 million y ago). Second, topological congruence analyses of each group's complete phylogeny and microbiota dendrogram reveal significant degrees of phylosymbiosis, irrespective of host clade age or taxonomy. Third, consistent with selection on host–microbiota interactions driving phylosymbiosis, there are survival and performance reductions when interspecific microbiota transplants are conducted between closely related and divergent host species pairs. Overall, these findings indicate that the composition and functional effects of an animal's microbial community can be closely allied with host evolution, even across wide-ranging timescales and diverse animal systems reared under controlled conditions.

Metagenome Sequencing of the Hadza Hunter-Gatherer Gut Microbiota

Through human microbiome sequencing, we can better understand how host evolutionary and ontogenetic history is reflected in the microbial function. However, there has been no information on the gut metagenome configuration in hunter-gatherer populations, posing a gap in our knowledge of gut microbiota (GM)-host mutualism arising from a lifestyle that describes over 90% of human evolutionary history. Here, we present the first metagenomic analysis of GM from Hadza hunter-gatherers of Tanzania, showing a unique enrichment in metabolic pathways that aligns with the dietary and environmental factors characteristic of their foraging lifestyle. We found that the Hadza GM is adapted for broad-spectrum carbohydrate metabolism, reflecting the complex polysaccharides in their diet. Furthermore, the Hadza GM is equipped for branched-chain amino acid degradation and aromatic amino acid biosynthesis. Resistome functionality demonstrates the existence of antibiotic resistance genes in a population with little antibiotic exposure, indicating the ubiquitous presence of environmentally derived resistances. Our results demonstrate how the functional specificity of the GM correlates with certain environment and lifestyle factors and how complexity from the exogenous environment can be balanced by endogenous homeostasis. The Hadza gut metagenome structure allows us to appreciate the co-adaptive functional role of the GM in complementing the human physiology, providing a better understanding of the versatility of human life and subsistence.

Parasite diversity declines with host evolutionary distinctiveness: a global analysis of carnivores.

Evolutionarily distinctive host lineages might harbor fewer parasite species because they have fewer opportunities for parasite sharing than hosts having extant close relatives, or because diverse parasite assemblages promote host diversification. We evaluate these hypotheses using data from 930 species of parasites reported to infect free-living carnivores. We applied nonparametric richness estimators to estimate parasite diversity among well-sampled carnivore species and assessed how well host evolutionary distinctiveness, relative to other biological and environmental factors, explained variation in estimated parasite diversity. Species richness estimates indicate that the current published literature captures less than 50% of the true parasite diversity for most carnivores. Parasite species richness declined with evolutionary distinctiveness of carnivore hosts (i.e., length of terminal ranches of the phylogeny) and increased with host species body mass and geographic range area. We found no support for the hypothesis that hosts from more diverse lineages support a higher number of generalist parasites, but we did find evidence that parasite assemblages might have driven host lineage diversification through mechanisms linked to sexual selection. Collectively, this work provides strong support for host evolutionary history being an essential predictor of parasite diversity, and offers a simple model for predicting parasite diversity in understudied carnivore species.

Root microbiome relates to plant host evolution in maize and other Poaceae

Prokaryote-eukaryote interactions are primordial, but host selection of its bacterial community remains poorly understood. Because eukaryote evolution affects numerous traits shaping the ecology of their microbiome, we can expect that many evolutionary changes in the former will have the potential to impact on the composition of the latter. Consequently, the more phylogenetically distant the eukaryotic hosts, the more distinct their associated bacterial communities should be. We tested this with plants, by comparing the bacterial communities associated with maize genotypes or other Poaceae. 16S rRNA taxonomic microarray analysis showed that the genetic distance between rhizobacterial communities correlated significantly with the phylogenetic distance (derived from chloroplastic sequences) between Poaceae genotypes. This correlation was also significant when considering specific bacterial populations from all main bacterial divisions, instead of the whole rhizobacterial community. These results indicate that eukaryotic host's evolutionary history can be a significant factor shaping directly the assembly and composition of its associated bacterial compartment.

The Population History of Endogenous Retroviruses in Mule Deer (Odocoileus hemionus)

Mobile elements are powerful agents of genomic evolution and can be exceptionally informative markers for investigating species and population-level evolutionary history. While several studies have utilized retrotransposon-based insertional polymorphisms to resolve phylogenies, few population studies exist outside of humans. Endogenous retroviruses are LTR-retrotransposons derived from retroviruses that have become stably integrated in the host genome during past infections and transmitted vertically to subsequent generations. They offer valuable insight into host-virus co-evolution and a unique perspective on host evolutionary history because they integrate into the genome at a discrete point in time. We examined the evolutionary history of a cervid endogenous gammaretrovirus (CrERVγ) in mule deer (Odocoileus hemionus). We sequenced 14 CrERV proviruses (CrERV-in1 to -in14), and examined the prevalence and distribution of 13 proviruses in 262 deer among 15 populations from Montana, Wyoming, and Utah. CrERV absence in white-tailed deer (O. virginianus), identical 5' and 3' long terminal repeat (LTR) sequences, insertional polymorphism, and CrERV divergence time estimates indicated that most endogenization events occurred within the last 200000 years. Population structure inferred from CrERVs (F ST = 0.008) and microsatellites (θ = 0.01) was low, but significant, with Utah, northwestern Montana, and a Helena herd being particularly differentiated. Clustering analyses indicated regional structuring, and non-contiguous clustering could often be explained by known translocations. Cluster ensemble results indicated spatial localization of viruses, specifically in deer from northeastern and western Montana. This study demonstrates the utility of endogenous retroviruses to elucidate and provide novel insight into both ERV evolutionary history and the history of contemporary host populations.

Phylogenetically related and ecologically similar carnivores harbour similar parasite assemblages

Most parasites infect multiple hosts, but what factors determine the range of hosts a given parasite can infect? Understanding the broad scale determinants of parasite distributions across host lineages is important for predicting pathogen emergence in new hosts and for estimating pathogen diversity in understudied host species. In this study, we used a new data set on 793 parasite species reported from free-ranging populations of 64 carnivore species to examine the factors that influence parasite sharing between host species. Our results showed that parasites are more commonly shared between phylogenetically related host species pairs. Additionally, host species with higher similarity in biological traits and greater geographic range overlap were also more likely to share parasite species. Of three measures of phylogenetic relatedness considered here, the number divergence events that separated host species pairs most strongly influenced the likelihood of parasite sharing. We also showed that viruses and helminths tend to infect carnivore hosts within more restricted phylogenetic ranges than expected by chance. Overall, our results underscore the importance of host evolutionary history in determining parasite host range, even when simultaneously considering other factors such as host ecology and geographic distribution.

Host specificity and coevolution of Flavobacteriaceae endosymbionts within the siphonous green seaweed Bryopsis

The siphonous green seaweed Bryopsis harbors complex intracellular bacterial communities. Previous studies demonstrated that certain species form close, obligate associations with Flavobacteriaceae. A predominant imprint of host evolutionary history on the presence of these bacteria suggests a highly specialized association. In this study we elaborate on previous results by expanding the taxon sampling and testing for host–symbiont coevolution Therefore, we optimized a PCR protocol to directly and specifically amplify Flavobacteriaceae endosymbiont 16S rRNA gene sequences, which allowed us to screen a large number of algal samples without the need for cultivation or surface sterilization. We analyzed 146 Bryopsis samples, and 92 additional samples belonging to the Bryopsidales and other orders within the class Ulvophyceae. Results indicate that the Flavobacteriaceae endosymbionts are restricted to Bryopsis, and only occur within specific, warm-temperate and tropical clades of the genus. Statistical analyses (AMOVA) demonstrate a significant non-random host–symbiont association. Comparison of bacterial 16S rRNA and Bryopsis rbcL phylogenies, however, reveal complex host–symbiont evolutionary associations, whereby closely related hosts predominantly harbor genetically similar endosymbionts. Bacterial genotypes are rarely confined to a single Bryopsis species and most Bryopsis species harbored several Flavobacteriaceae, obscuring a clear pattern of coevolution.

Permanent residents or temporary lodgers: characterizing intracellular bacterial communities in the siphonous green algaBryopsis

The ecological success of giant celled, siphonous green algae in coastal habitats has repeatedly been linked to endophytic bacteria living within the cytoplasm of the hosts. Yet, very little is known about the relative importance of evolutionary and ecological factors controlling the intracellular bacterial flora of these seaweeds. Using the marine alga Bryopsis (Bryopsidales, Chlorophyta) as a model, we explore the diversity of the intracellular bacterial communities and investigate whether their composition is controlled by ecological and biogeographic factors rather than the evolutionary history of the host. Using a combination of 16S rDNA clone libraries and denaturing gradient gel electrophoresis analyses, we show that Bryopsis harbours a mixture of relatively few but phylogenetically diverse bacterial species. Variation partitioning analyses show a strong impact of local environmental factors on the presence of Rickettsia and Mycoplasma in their association with Bryopsis. The presence of Flavobacteriaceae and Bacteroidetes, on the other hand, reflects a predominant imprint of host evolutionary history, suggesting that these bacteria are more specialized in their association. The results highlight the importance of interpreting the presence of individual bacterial phylotypes in the light of ecological and evolutionary principles such as phylogenetic niche conservatism to understand complex endobiotic communities and the parameters shaping them.

Phylogenetic congruence between Mollitrichosiphum (Aphididae: Greenideinae) and Buchnera indicates insect–bacteria parallel evolution

We wanted to test whether Mollitrichosiphum, an aphid genus with life cycles on subtropical woody host plants, and Buchnera, the primary endosymbiont of aphids, evolve in parallel. We used three aphid genes (mitochondrial COI, cytochrome oxidase subunit I and Cytb, cytochrome b; nuclear EF1α, translation elongation factor 1 alpha) and two Buchnera genes (16S rDNA; gnd, gluconate‐6‐phosphate dehydrogenase) to reconstruct phylogenies. The congruence between the phylogenetic trees of aphids and Buchnera was then measured. The results present phylogenetic evidence for the parallel evolution of Mollitrichosiphum and Buchnera at the intraspecific as well as the interspecific levels. Our results support the possibility of using endosymbiont genes to study host evolutionary history and biogeographical patterns. We also investigated the usability of the Buchnera gnd gene as a barcoding marker for aphid identification.

Variable Microsatellite Loci for Population Genetic Analysis of Old World Monkey Lice (Pedicinus sp.)

Parasitic lice have been valuable informants of their host's evolutionary history because they complete their entire life cycle on the host and move between hosts primarily through direct host-to-host contact. Therefore, lice are confined to their hosts both in ecological and evolutionary time. Lice on great apes have been studied to examine details of their host's evolutionary history; however, species of Pedicinus, which parasitize the Old World monkeys, are less well known. We sampled lice from 2 groups of red colobus (Procolobus spp.) in Kibale National Park in Uganda and from red colobus and black and white colobus (Procolobus polycomos) in Taï National Park in Côte d'Ivoire. We used next-generation sequencing data analysis and the human body louse (Pediculus humanus humanus) genome to search for microsatellites for population genetic studies of Pedicinus lice. The 96 primer sets for microsatellite loci designed from the human body louse genome failed to amplify microsatellites in Pedicinus sp., perhaps due to the fast rate of evolution in parasitic lice. Of 63 microsatellites identified by next-generation sequencing data analysis of Pedicinus sp., 12 were variable among populations and 9 were variable within a single population. Our results suggest that these loci will be useful across the genus Pedicinus. We found that the lice in Uganda are not structured according to their hosts' social group; rather, 2 non-interbreeding populations of lice were found on both groups of red colobus. Because direct host-to-host contact is usually required for lice to move among hosts, these lice could be useful for identification and study of behavioral interactions between primate species.

Phylogeny of European Bat Lyssavirus 1 in Eptesicus isabellinus Bats, Spain

To better understand the epidemiology of European bat lyssavirus 1 (EBLV-1) in Europe, we phylogenetically characterized Lyssavirus from Eptesicus isabellinus bats in Spain. An independent cluster of EBLV-1 possibly resulted from geographic isolation and association with a different reservoir from other European strains. EBLV-1 phylogeny is complex and probably associated with host evolutionary history.

Phylogeny of European Bat Lyssavirus 1 inEptesicus isabellinusBats, Spain

To better understand the epidemiology of European bat lyssavirus 1 (EBLV-1) in Europe, we phylogenetically characterized Lyssavirus from Eptesicus isabellinus bats in Spain. An independent cluster of EBLV-1 possibly resulted from geographic isolation and association with a different reservoir from other European strains. EBLV-1 phylogeny is complex and probably associated with host evolutionary history.

Phylogeny and coevolutionary associations of makialgine mites (Acari, Psoroptidae, Makialginae) provide insight into evolutionary history of their hosts, strepsirrhine primates

Phylogeny of the mite subfamily Makialginae, permanent and highly specialized ectoparasites of strepsirrhine primates distributed in Madagascar and tropical Africa, was inferred based on morphology under maximum parsimony: Galagalges (Cheirogalalges (Makialges (Daubentonialges (Lemuralges, Gaudalges)))). Historical associations were reconstructed by fitting the mite tree onto alternative host topologies. Results of coevolutionary analyses highlight the disparity between morphological and molecular hypotheses on the host evolutionary history. Although phylogenetic relationships of strepsirrhine primates based on the morphological hypothesis returned significant fits to our parasite tree, the most recent molecular hypothesis of host phylogeny resulted in no coevolutionary scenario being different from random. Based on the former reconstructions, we hypothesize that present associations of Daubentoniidae, the earliest derivative extant family of Malagasy primates, acquired the present mite species via extinction of their original parasites and subsequent re-colonization by parasites from derived lemuriform families. Our data suggest that extant associations between Malagasy lemurs and their mites resulted from a single ancient codispersal to Madagascar from Africa. However, because of the host switch in Daubentoniidae, alternative, but less parsimonious, scenarios are possible. Our analyses indirectly support the hypothesis of the monophyletic origin of the infraorder Lemuriformes, the superfamily Lemuroidea, and the sister-group relationships between the families Lemuridae and Indriidae.

Multigene analysis of phylogenetic relationships and divergence times of primate sucking lice (Phthiraptera: Anoplura)

Cospeciation between hosts and parasites offers a unique opportunity to use information from parasites to infer events in host evolutionary history. Although lice (Insecta: Phthiraptera) are known to cospeciate with their hosts and have frequently served as important markers to infer host evolutionary history, most molecular studies are based on only one or two markers. Resulting phylogenies may, therefore, represent gene histories (rather than species histories), and analyses of multiple molecular markers are needed to increase confidence in the results of phylogenetic analyses. Herein, we phylogenetically examine nine molecular markers in primate sucking lice (Phthiraptera: Anoplura) and we use these markers to estimate divergence times among louse lineages. Individual and combined analyses of these nine markers are, for the most part, congruent, supporting relationships hypothesized in previous studies. Only one marker, the nuclear protein-coding gene Histone 3, has a significantly different tree topology compared to the other markers. The disparate evolutionary history of this marker, however, has no significant effect on topology or nodal support in the combined phylogenetic analyses. Therefore, phylogenetic results from the combined data set likely represent a solid hypothesis of species relationships. Additionally, we find that simultaneous use of multiple markers and calibration points provides the most reliable estimates of louse divergence times, in agreement with previous studies estimating divergences among species. Estimates of phylogenies and divergence times also allow us to verify the results of [Reed, D.L., Light, J.E., Allen, J.M., Kirchman, J.J., 2007. Pair of lice lost or parasites regained: the evolutionary history of anthropoid primate lice. BMC Biol. 5, 7.]; there was probable contact between gorilla and archaic hominids roughly 3 Ma resulting in a host switch of Pthirus lice from gorillas to archaic hominids. Thus, these results provide further evidence that data from cospeciating organisms can yield important information about the evolutionary history of their hosts.

Differential impact of retrotransposon populations on the genome of allotetraploid tobacco (Nicotiana tabacum)

LTR-retrotransposons contribute substantially to the structural diversity of plant genomes. Recent models of genome evolution suggest that retrotransposon amplification is offset by removal of retrotransposon sequences, leading to a turnover of retrotransposon populations. While bursts of amplification have been documented, it is not known whether removal of retrotransposon sequences occurs continuously, or is triggered by specific stimuli over short evolutionary periods. In this work, we have characterized the evolutionary dynamics of four populations of copia-type retrotransposons in allotetraploid tobacco (Nicotiana tabacum) and its two diploid progenitors Nicotiana sylvestris and Nicotiana tomentosiformis. We have used SSAP (Sequence-Specific Amplification Polymorphism) to evaluate the contribution retrotransposons have made to the diversity of tobacco and its diploid progenitor species, to quantify the contribution each diploid progenitor has made to tobacco's retrotransposon populations, and to estimate losses or amplifications of retrotransposon sequences subsequent to tobacco's formation. Our results show that the tobacco genome derives from a turnover of retrotransposon sequences with removals concomitant with new insertions. We have detected unique behaviour specific to each retrotransposon population, with differences likely reflecting distinct evolutionary histories and activities of particular elements. Our results indicate that the retrotransposon content of a given plant species is strongly influenced by the host evolutionary history, with periods of rapid turnover of retrotransposon sequences stimulated by allopolyploidy.

Genetic Analysis of Lice Supports Direct Contact between Modern and Archaic Humans

Parasites can be used as unique markers to investigate host evolutionary history, independent of host data. Here we show that modern human head lice, Pediculus humanus, are composed of two ancient lineages, whose origin predates modern Homo sapiens by an order of magnitude (ca. 1.18 million years). One of the two louse lineages has a worldwide distribution and appears to have undergone a population bottleneck ca. 100,000 years ago along with its modern H. sapiens host. Phylogenetic and population genetic data suggest that the other lineage, found only in the New World, has remained isolated from the worldwide lineage for the last 1.18 million years. The ancient divergence between these two lice is contemporaneous with splits among early species of Homo, and cospeciation analyses suggest that the two louse lineages codiverged with a now extinct species of Homo and the lineage leading to modern H. sapiens. If these lice indeed codiverged with their hosts ca. 1.18 million years ago, then a recent host switch from an archaic species of Homo to modern H. sapiens is required to explain the occurrence of both lineages on modern H. sapiens. Such a host switch would require direct physical contact between modern and archaic forms of Homo.