Captivity and the co-diversification of great ape microbiomes

AbstractWild great apes harbor clades of gut bacteria that are restricted to each host species. Previous research shows the evolutionary relationships among several host-restricted clades mirror those of great-ape species. However, processes such as geographic separation, host-shift speciation, and host-filtering based on diet or gut physiology can generate host-restricted bacterial clades and mimic patterns of co-diversification across host species. To gain insight into the distribution of host-restricted taxa, we examine captive great apes living under conditions where sharing of bacterial strains is readily possible. Here, we show that increased sampling of wild and captive apes identifies additional host-restricted lineages whose relationships are not concordant with the host phylogeny. Moreover, the gut microbiomes of captive apes converge through the displacement of strains that are restricted to their wild conspecifics by human-restricted strains. We demonstrate that host-restricted and co-diversifying bacterial strains in wild apes lack persistence and fidelity in captive environments.

Download Full-text

Genomes of gut bacteria from Nasonia wasps shed light on phylosymbiosis and microbe-assisted hybrid breakdown

10.1101/2021.02.13.431100 ◽

2021 ◽

Author(s):

Karissa L. Cross ◽

Brittany A. Leigh ◽

E. Anne Hatmaker ◽

Aram Mikaelyan ◽

Asia K. Miller ◽

...

Keyword(s):

Proteus Mirabilis ◽

Host Species ◽

Parental Species ◽

Parasitoid Wasp ◽

Gut Bacteria ◽

Hybrid Breakdown ◽

Bacterial Genomes ◽

Providencia Rettgeri ◽

Host Phylogeny

ABSTRACTPhylosymbiosis is a cross-system trend whereby microbial community relationships recapitulate the host phylogeny. In Nasonia parasitoid wasps, phylosymbiosis occurs throughout development, is distinguishable between sexes, and benefits host development and survival. Moreover, the microbiome shifts in hybrids as a rare Proteus bacteria in the microbiome becomes dominant. The larval hybrids then catastrophically succumb to bacterial-assisted lethality and reproductive isolation between the species. Two important questions for understanding phylosymbiosis and bacterial-assisted lethality in hybrids are: (i) Do the Nasonia bacterial genomes differ from other animal isolates and (ii) Are the hybrid bacterial genomes the same as those in the parental species? Here we report the cultivation, whole genome sequencing, and comparative analyses of the most abundant gut bacteria in Nasonia larvae, Providencia rettgeri and Proteus mirabilis. Characterization of new isolates shows Proteus mirabilis forms a more robust biofilm than Providencia rettgeri and when grown in co-culture, Proteus mirabilis significantly outcompetes Providencia rettgeri. Providencia rettgeri genomes from Nasonia are similar to each other and more divergent to pathogenic, human-associates strains. Proteus mirabilis from N. vitripennis, N. giraulti, and their hybrid offspring are nearly identical and relatively distinct from human isolates. These results indicate that members of the larval gut microbiome within Nasonia are most similar to each other, and the strain of the dominant Proteus mirabilis in hybrids is resident in parental species. Holobiont interactions between shared, resident members of the wasp microbiome and the host underpin phylosymbiosis and hybrid breakdown.IMPORTANCEAnimal and plant hosts often establish intimate relationships with their microbiomes. In varied environments, closely-related host species share more similar microbiomes, a pattern termed phylosymbiosis. When phylosymbiosis is functionally significant and beneficial, microbial transplants between host species or host hybridization can have detrimental consequences on host biology. In the Nasonia parasitoid wasp genus that contains a phylosymbiotic gut community, both effects occur and provide evidence for selective pressures on the holobiont. Here, we show that bacterial genomes in Nasonia differ from other environments and harbor genes with unique functions that may regulate phylosymbiotic relationships. Furthermore, the bacteria in hybrids are identical to parental species, thus supporting a hologenomic tenet that the same members of the microbiome and the host genome impact phylosymbiosis, hybrid breakdown, and speciation.

Download Full-text

Genomes of Gut Bacteria from Nasonia Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown

mSystems ◽

10.1128/msystems.01342-20 ◽

2021 ◽

Vol 6 (2) ◽

Author(s):

Karissa L. Cross ◽

Brittany A. Leigh ◽

E. Anne Hatmaker ◽

Aram Mikaelyan ◽

Asia K. Miller ◽

...

Keyword(s):

Proteus Mirabilis ◽

Host Species ◽

Parental Species ◽

Parasitoid Wasp ◽

Gut Bacteria ◽

Hybrid Breakdown ◽

Bacterial Genomes ◽

Providencia Rettgeri ◽

Content Type ◽

Host Phylogeny

ABSTRACT Phylosymbiosis is a cross-system trend whereby microbial community relationships recapitulate the host phylogeny. In Nasonia parasitoid wasps, phylosymbiosis occurs throughout development, is distinguishable between sexes, and benefits host development and survival. Moreover, the microbiome shifts in hybrids as a rare Proteus bacterium in the microbiome becomes dominant. The larval hybrids then catastrophically succumb to bacterium-assisted lethality and reproductive isolation between the species. Two important questions for understanding phylosymbiosis and bacterium-assisted lethality in hybrids are (i) do the Nasonia bacterial genomes differ from other animal isolates and (ii) are the hybrid bacterial genomes the same as those in the parental species? Here, we report the cultivation, whole-genome sequencing, and comparative analyses of the most abundant gut bacteria in Nasonia larvae, Providencia rettgeri and Proteus mirabilis. Characterization of new isolates shows Proteus mirabilis forms a more robust biofilm than Providencia rettgeri and that, when grown in coculture, Proteus mirabilis significantly outcompetes Providencia rettgeri. Providencia rettgeri genomes from Nasonia are similar to each other and more divergent from pathogenic, human associates. Proteus mirabilis from Nasonia vitripennis, Nasonia giraulti, and their hybrid offspring are nearly identical and relatively distinct from human isolates. These results indicate that members of the larval gut microbiome within Nasonia are most similar to each other, and the strain of the dominant Proteus mirabilis in hybrids is resident in parental species. Holobiont interactions between shared, resident members of the wasp microbiome and the host underpin phylosymbiosis and hybrid breakdown. IMPORTANCE Animal and plant hosts often establish intimate relationships with their microbiomes. In varied environments, closely related host species share more similar microbiomes, a pattern termed phylosymbiosis. When phylosymbiosis is functionally significant and beneficial, microbial transplants between host species and host hybridization can have detrimental consequences on host biology. In the Nasonia parasitoid wasp genus, which contains a phylosymbiotic gut community, both effects occur and provide evidence for selective pressures on the holobiont. Here, we show that bacterial genomes in Nasonia differ from other environments and harbor genes with unique functions that may regulate phylosymbiotic relationships. Furthermore, the bacteria in hybrids are identical to those in parental species, thus supporting a hologenomic tenet that the same members of the microbiome and the host genome impact phylosymbiosis, hybrid breakdown, and speciation.

Download Full-text

Using Great Ape Phylogeny to Teach Evolutionary Thinking

The American Biology Teacher ◽

10.1525/abt.2016.78.3.263 ◽

2016 ◽

Vol 78 (3) ◽

pp. 263-265

Author(s):

Susan Offner

Keyword(s):

Phylogenetic Tree ◽

Phylogenetic Trees ◽

Great Apes ◽

Evolutionary Relationships ◽

Great Ape ◽

General Skill

A simple phylogenetic tree of the great apes provides many important teaching opportunities, both in the general skill of reading phylogenetic trees and in using them to explore evolutionary relationships.

Download Full-text

Drug resistant gut bacteria mimic a host mechanism for anticancer drug clearance

10.1101/820084 ◽

2019 ◽

Author(s):

Peter Spanogiannopoulos ◽

Patrick H. Bradley ◽

Jonathan Melamed ◽

Ysabella Noelle Amora Malig ◽

Kathy N. Lam ◽

...

Keyword(s):

Mammalian Cells ◽

Drug Disposition ◽

Transcriptional Profiling ◽

Drug Efficacy ◽

Drug Clearance ◽

Gut Bacteria ◽

Resistant Bacteria ◽

Drug Resistant ◽

Bacterial Strains

Microbiome surveys indicate that pharmaceuticals are the top predictor of inter-individual variations in gut microbial community structure1, consistent with in vitro evidence that non-antibiotic (i.e. host-targeted) drugs inhibit gut bacterial growth2and are subject to extensive metabolism by the gut microbiome3,4. In oncology, bacterial metabolism has been implicated in both drug efficacy5,6and toxicity7,8; however, the degree to which bacterial sensitivity and metabolism can be driven by conserved pathways also found in mammalian cells remains poorly understood. Here, we show that anticancer fluoropyrimidine drugs broadly inhibit the growth of diverse gut bacterial strains. Media supplementation, transcriptional profiling (RNA-seq), and bacterial genetics implicated pyrimidine metabolism as a key target in bacteria, as in mammalian cells. Drug resistant bacteria metabolized 5FU to its inactive metabolite dihydrofluorouracil (DHFU) mimicking the major host pathway for drug clearance. Functional orthologs of the bacterial operon responsible (preTA) are widespread across human gut bacteria from the Firmicutes and Proteobacteria phyla. The observed conservation of both the targets and pathways for metabolism of therapeutics across domains highlights the need to distinguish the relative contributions of human and microbial cells to drug disposition9, efficacy, and side effect profiles.

Download Full-text

Rapid divergence in independent aspects of the compatibility phenotype in the Spiroplasma/Drosophila interaction

10.1101/2021.02.03.429608 ◽

2021 ◽

Author(s):

Joanne S. Griffin ◽

Michael Gerth ◽

Gregory D. D. Hurst

Keyword(s):

Vertical Transmission ◽

Host Species ◽

High Efficiency ◽

Host Shift ◽

Direct Selection ◽

New Host ◽

Host Shifts ◽

Species Pairs ◽

Novel Host ◽

Rapid Divergence

AbstractHeritable symbionts represent important components of host biology, both as antagonistic reproductive parasites and as beneficial protective partners. An important component of heritable microbes’ biology is their ability to establish in new host species, a process equivalent to a host shift for an infectiously transmitted parasite or pathogen. For a host shift to occur, the symbiont must be compatible with the host: it must not cause excess pathology, must have good vertical transmission, and possess a drive phenotype that enables spread. Classically, compatibility has been considered a declining function of genetic distance between novel and ancestral host species. Here we investigate the evolutionary lability of compatibility to heritable microbes by comparing the capacity for a symbiont to establish in two novel host species equally related to the ancestral host. Compatibility of the protective Spiroplasma from D. hydei with D. simulans and D. melanogaster was tested. The Spiroplasma had contrasting compatibility in these two host species. The transinfection showed pathology and low vertical transmission in D. melanogaster but was asymptomatic and transmitted with high efficiency in D. simulans. These results were not affected by the presence/absence of Wolbachia in either of the two species. The pattern of protection was not congruent with that for pathology/transmission, with protection being weaker in the D. simulans, the host in which Spiroplasma was asymptomatic and transmitted well. Further work indicated pathological interactions occurred in D. sechellia and D. yakuba, indicating that D. simulans was unusual in being able to carry the symbiont without damage. The differing compatibility of the symbiont with these closely related host species emphasises first the rapidity with which host-symbiont compatibility evolves despite compatibility itself not being subject to direct selection, and second the independence of the different components of compatibility (pathology, transmission, protection). This requirement to fit three different independently evolving aspects of compatibility, if commonly observed, is likely to be a major feature limiting the rate of host shifts. Moving forward, the variation between sibling species pairs observed above provides an opportunity to identify the mechanisms behind variable compatibility between closely related host species, which will drive hypotheses as to the evolutionary drivers of compatibility variation.

Download Full-text

Wild African great apes as natural hosts of malaria parasites: current knowledge and research perspectives

Primate Biology ◽

10.5194/pb-4-47-2017 ◽

2017 ◽

Vol 4 (1) ◽

pp. 47-59 ◽

Cited By ~ 2

Author(s):

Hélène Marie De Nys ◽

Therese Löhrich ◽

Doris Wu ◽

Sébastien Calvignac-Spencer ◽

Fabian Hubertus Leendertz

Keyword(s):

Current Knowledge ◽

Great Apes ◽

Future Research ◽

Human Populations ◽

Great Ape ◽

Malaria Parasites ◽

Research Perspectives ◽

Parasite Ecology ◽

Natural Hosts ◽

African Great Apes

Abstract. Humans and African great apes (AGAs) are naturally infected with several species of closely related malaria parasites. The need to understand the origins of human malaria as well as the risk of zoonotic transmissions and emergence of new malaria strains in human populations has markedly encouraged research on great ape Plasmodium parasites. Progress in the use of non-invasive methods has rendered investigations into wild ape populations possible. Present knowledge is mainly focused on parasite diversity and phylogeny, with still large gaps to fill on malaria parasite ecology. Understanding what malaria infection means in terms of great ape health is also an important, but challenging avenue of research and has been subject to relatively few research efforts so far. This paper reviews current knowledge on African great ape malaria and identifies gaps and future research perspectives.

Download Full-text

Roles of Host Species, Geographic Separation, and Isolation in the Seroprevalence of Jamestown Canyon and Snowshoe Hare Viruses in Newfoundland

Applied and Environmental Microbiology ◽

10.1128/aem.01351-12 ◽

2012 ◽

Vol 78 (18) ◽

pp. 6734-6740 ◽

Cited By ~ 11

Author(s):

Gregory Goff ◽

Hugh Whitney ◽

Michael A. Drebot

Keyword(s):

Host Species ◽

Neutralization Assay ◽

Snowshoe Hare ◽

Large Mammals ◽

Content Type ◽

Neuroinvasive Disease ◽

Snowshoe Hares ◽

Jamestown Canyon Virus ◽

Geographic Separation ◽

California Serogroup

ABSTRACTCalifornia serogroup viruses, including Jamestown Canyon virus (JCV) and snowshoe hare virus (SSHV), are mosquito-borne members of theBunyaviridaefamily and are endemic across North America. These arboviruses are potential pathogens which occasionally cause neuroinvasive disease in humans and livestock. A neutralization assay was used to document JCV and SSHV seroprevalence using blood collected from a variety of domestic and wildlife host species. These species were sampled in an island setting, Newfoundland, which contains diverse ecoregions, ecological landscapes, and habitats. Seroprevalence rates for each virus differed significantly among host species and within certain species across different geographic areas. JCV was significantly associated with large mammals, and SSHV was significantly associated with snowshoe hares. Seroprevalence rates in the 5 species of animals tested for prior exposure to JCV ranged from 0% in snowshoe hares to 64% in horses. Seroprevalence rates for SSHV ranged from less than 1% in bovines to 55% in all snowshoe hares. The seroprevalence of SSHV differed significantly (P< 0.05) among hares occupying the discrete habitats of watersheds separated by 14 to 35 km. Cattle on farms in boreal forest landscapes displayed significantly higher JCV seroprevalence (P< 0.001) than those on farms located in seacoast landscapes. Lifelong geographic isolation of cattle to insular Newfoundland was associated with significantly lower JCV seroprevalence (P< 0.01) than that for cattle which had lived off-island.

Download Full-text

Cradle Under the Canopy The Forest Origins of our Ape and Hominin Ancestors and the Tropical Forest Forays of the Genus Homo

Tropical Forests in Prehistory, History, and Modernity ◽

10.1093/oso/9780198818496.003.0007 ◽

2019 ◽

Author(s):

Patrick Roberts

Keyword(s):

Tool Use ◽

Pan Paniscus ◽

Great Apes ◽

Last Common Ancestor ◽

Great Ape ◽

Tropical Environments ◽

Genus Homo ◽

In Captivity ◽

Game Hunting ◽

The Tropics

The evolutionary proximity of the non-human great apes to us is often stressed in studies of animals, such as Kanzi, a bonobo (Pan paniscus) bred in captivity, that demonstrate their capacity to undertake tool-use and even utilize and comprehend language (Toth et al., 1993; Savage-Rumbaugh and Lewin, 1996; Schick et al., 1999). Likewise, studies of chimpanzees (Pan spp.) have highlighted the similarity of their emotional and empathetic capacities to those of humans (Parr et al., 2005; Campbell and de Waal, 2014). However, as noted by Savage- Rumbaugh and Lewin (1996), in palaeoanthropology and archaeology more broadly, the emergence of the hominin clade and, later, our species, is referenced in terms of the ‘chasm’ between ourselves and other extant great apes. Indeed, despite our genetic and behavioural proximity, extant non-human great ape taxa are often popularly characterized as living fossils of how we used to be. They are used as analogues for the subsistence and behaviour of the Last Common Ancestor (LCA) of humans and non-human great apes (Clutton-Brock and Harvey, 1977; Goodall, 1986; Foley and Lewin, 2004) and it is almost as if the fact that they still occupy the tropical environments in which these hominoids likely evolved (though see Elton, 2008) allows them to be treated as static comparisons (Figure 3.1). Since Darwin wrote the Descent of Man in 1871, the forests of the tropics, and their modern non-human great ape inhabitants, have tended to be perceived as being left behind as the hominin clade gained increasingly ‘human’ traits of tool-use, medium to large game hunting, and upright locomotion on open ‘savanna’ landscapes (Dart, 1925; Potts, 1998; Klein, 1999). From this perspective it is perhaps unsurprising that tropical forests are seen as alien to the genus Homo and its closest hominin ancestors.

Download Full-text

Pantomime and imitation in great apes

Interaction Studies ◽

10.1075/is.17028.rus ◽

2018 ◽

Vol 19 (1-2) ◽

pp. 200-215 ◽

Cited By ~ 8

Author(s):

Anne E. Russon

Keyword(s):

Data Mining ◽

Language Evolution ◽

Great Apes ◽

Great Ape ◽

Evolution Of Language ◽

Distinct Process ◽

Action Imitation ◽

Primitive Forms ◽

Communicative Abilities

Abstract This paper assesses great apes’ abilities for pantomime and action imitation, two communicative abilities proposed as key contributors to language evolution. Modern great apes, the only surviving nonhuman hominids, are important living models of the communicative platform upon which language evolved. This assessment is based on 62 great ape pantomimes identified via data mining plus published reports of great ape action imitation. Most pantomimes were simple, imperative, and scaffolded by partners’ relationship and scripts; some resemble declaratives, some were sequences of several inter-related elements. Imitation research consistently shows great apes perform action imitation at low fidelity, but also that action imitation may not represent a distinct process or function. Discussion focuses on how findings may advance reconstruction of the evolution of language, including what great apes may contribute to understanding ‘primitive’ forms of pantomime and imitation and how to improve their study.

Download Full-text

Enteroviruses from Humans and Great Apes in the Republic of Congo: Recombination within Enterovirus C Serotypes

Microorganisms ◽

10.3390/microorganisms8111779 ◽

2020 ◽

Vol 8 (11) ◽

pp. 1779 ◽

Cited By ~ 2

Author(s):

Inestin Amona ◽

Hacène Medkour ◽

Jean Akiana ◽

Bernard Davoust ◽

Mamadou Lamine Tall ◽

...

Keyword(s):

Animal Species ◽

Great Apes ◽

Great Ape ◽

Human Feces ◽

Republic Of Congo ◽

Healthy Humans ◽

The Family ◽

Severe Infections ◽

The Republic

Enteroviruses (EVs) are viruses of the family Picornaviridae that cause mild to severe infections in humans and in several animal species, including non-human primates (NHPs). We conducted a survey and characterization of enteroviruses circulating between humans and great apes in the Congo. Fecal samples (N = 24) of gorillas and chimpanzees living close to or distant from humans in three Congolese parks were collected, as well as from healthy humans (N = 38) living around and within these parks. Enteroviruses were detected in 29.4% of gorilla and 13.15% of human feces, including wild and human-habituated gorillas, local humans and eco-guards. Two identical strains were isolated from two humans coming from two remote regions. Their genomes were similar and all genes showed their close similarity to coxsackieviruses, except for the 3C, 3D and 5′-UTR regions, where they were most similar to poliovirus 1 and 2, suggesting recombination. Recombination events were found between these strains, poliovirus 1 and 2 and EV-C99. It is possible that the same EV-C species circulated in both humans and apes in different regions in the Congo, which must be confirmed in other investigations. In addition, other studies are needed to further investigate the circulation and genetic diversity of enteroviruses in the great ape population, to draw a definitive conclusion on the different species and types of enteroviruses circulating in the Republic of Congo.

Download Full-text