Extensive inheritance of gut microbial communities in a superorganismal termite DOI Creative Commons
Veronica Sinotte, Justinn Renelies‐Hamilton, Sergio Andreu‐Sánchez

et al.

Research Square (Research Square), Journal Year: 2023, Volume and Issue: unknown

Published: Feb. 17, 2023

Abstract Mutualistic co-evolution can be mediated by vertical transmission of symbionts between host generations. Organisms exhibit adaptations that ensure optimal microbial inheritance, yet the extent to which this applies social insects, such as termites have co-evolved with gut microbes, is poorly resolved. Here, we document consistent across colony generations fungus-farming termites. Inherited bacteria comprise 44% microbiome, over 80 genera, and strains are specific termite pedigrees. We show superorganism, consisting reproductives workers, analogous gametes soma an organism, adapted vertically transmit a distinct community high fidelity. Microbial inheritance achieved because colony-founding endowed set non-random, environmentally-sensitive, termite-specific microbes derived from their colonies origin. Reproductives biparentally these offspring where priority effects dictate composition forming microbiome. Superorganismal gametes, reproductives, thus secure entire communities specific, critical microbiome later retained workers. Extensive aligns evolutionary patterns termite-bacterial co-diversification. This colony-level extends models individual organisms superorganisms, both demonstrate retain symbiotic fidelity mixed-mode conducive mutualism.

Language: Английский

Vertically inherited microbiota and environment modifying behaviours conceal genetic variation in dung beetle life history DOI
Patrick T. Rohner, Armin P. Moczek

Proceedings of the Royal Society B Biological Sciences, Journal Year: 2024, Volume and Issue: 291(2021)

Published: April 17, 2024

Diverse organisms actively manipulate their (sym)biotic and physical environment in ways that feed back on own development. However, the degree to which these processes affect microevolution remains poorly understood. The gazelle dung beetle both physically modifies its ontogenetic structures biotic interactions through vertical symbiont transmission. By experimentally eliminating (i) environmental modifications (ii) inheritance of microbes, we assess how modifying behaviour microbiome transmission shape heritable variation evolutionary potential. We found depriving larvae symbionts behaviours increased additive genetic variance heritability for development time but not body size. This suggests larvae's ability has potential modify facilitate accumulation cryptic variation. may become released selectable when encounter environments are less amenable organismal manipulation or restructuring. Our findings also suggest intact microbiomes, commonly thought increase hosts, instead reduce conceal More broadly, our highlight populations evolve encountering novel, stressful conditions.

Language: Английский

Citations

4

Impact of Species and Developmental Stage on the Bacterial Communities of Aphaenogaster Ants DOI

Lily A Kelleher,

Manuela O. Ramalho

Current Microbiology, Journal Year: 2025, Volume and Issue: 82(4)

Published: Feb. 26, 2025

Language: Английский

Citations

0

Challenges in the Early Ontogeny of a Mutualistic Plant: Resource Availability and Plant Defense in Juvenile Cecropia Ant‐Plants DOI

Stephanie M. Coronado,

Andrea G. Vincent,

Felix S. H. Pozos

et al.

Biotropica, Journal Year: 2025, Volume and Issue: 57(2)

Published: Feb. 24, 2025

ABSTRACT Mutualistic species often must survive periods of their development without mutualist partner, but we lack a clear understanding the ecological mechanisms that maintain mutualisms despite these gaps in partnership. In ant‐plant protection mutualisms, plants house ant colonies deter herbivores. Yet juvenile ant‐plants symbiotic and withstand herbivory pressure until they are colonized by ants. A sapling's ability to host ants or employ alternative direct defenses, such as leaf secondary metabolites, may depend on access key resources, like light, soil nutrients, water. Alternatively, receive biotic at little resource cost from generalist predators, spiders. We examined whether Cecropia trees maintained sapling chemical defenses were associated with resources. surveyed three naturally occurring across rainfall gradient northwest Costa Rica. found both defense regulated availability fertility, water saplings. Rather than trade off, larger saplings more resources likely invest strategies, whereas smaller fewer appeared have defense. also although spiders common resource‐poor, undefended saplings, did not reduce herbivory. This study highlights importance determining performance during early ontogenetic stages.

Language: Английский

Citations

0

Inheritance or Recruitment? The Assembly Mechanisms and Functional Dynamics of Microbial Communities in the Life Cycle of a Wood‐Feeding Beetle DOI
Sixun Ge,

Yiming Niu,

Lili Ren

et al.

Molecular Ecology, Journal Year: 2025, Volume and Issue: unknown

Published: April 10, 2025

ABSTRACT Microbial partners enhance the metabolic capabilities of insects, enabling their adaptation to diverse ecological niches. Xylophagous insects have larvae that can digest lignocellulose and cope with plant secondary metabolites (PSMs). However, there is little information in terms microbiome sources, dynamics species contributions. This limits our understanding interaction between xylophagous microbiome. Monochamus saltuarius (Cerambycidae) a significant borer conifers. We used combined qPCR, host genomic metagenomic datasets, as well vitro validation experiments study associated its interactions M. . evaluated microbial metabolic/biosynthetic contributions validated related functions. Our findings revealed insect growth development altered quantity community composition bacteria fungi. The egg was particularly susceptible alteration due oviposition pits. Bacterial transmission largely persisted developmental stages, while fungal re‐acquisition primarily originated from external environment. By reconstructing pathway maps, we identified cooperative gut As transitioned phloem xylem feeding, functional role various pathways weakened. Remarkably, high‐contribution bacterial overlapped across different roles, these also showed considerable overlap feeding periods. Overall, highlights unique microbiome, which enhances ability digestion, PSMs degradation acquisition essential amino acids, vitamins.

Language: Английский

Citations

0

Cryptic community structure and metabolic interactions among the heritable facultative symbionts of the pea aphid DOI Open Access
Linyao Peng,

Jessica Hoban,

Jonah Joffe

et al.

Journal of Evolutionary Biology, Journal Year: 2023, Volume and Issue: 36(12), P. 1712 - 1730

Published: Sept. 13, 2023

Abstract Most insects harbour influential, yet non-essential heritable microbes in their hemocoel. Communities of these symbionts exhibit low diversity. But frequent multi-species nature raises intriguing questions on roles for symbiont–symbiont synergies host adaptation, and the stability symbiont communities, themselves. In this study, we build knowledge species-defined community structure across US populations pea aphid, Acyrthosiphon pisum. Through extensive genotyping, show that aphids' microbiomes can be more precisely defined at strain level, with variability shaping five out nine previously reported co-infection trends. Field data provide a mixture evidence synergistic fitness effects hitchhiking, revealing causes consequences To test whether within-host metabolic interactions predict common versus rare strain-defined leveraged high relatedness our dominant, community-defined strains vs. 12 aphid-derived Gammaproteobacteria sequenced genomes. Genomic inference, using complementarity indices, revealed potential cooperation among one pair symbionts—Serratia symbiotica Rickettsiella viridis. Applying expansion network algorithm, through additional use aphid obligate Buchnera genomes, Serratia emerged as only requiring both parties to expand holobiont metabolism. joint biotin biosynthesis pathway, may span missing gaps, creating multi-party mutualism within nutrient-limited, phloem-feeding hosts. Recent, complementary gene inactivation, pathways Rickettsiella, further origins mutualisms host–symbiont interdependencies. We genotyped seven bacterial species protein-coding loci, define ‘symbiont’ communities aphids from United States. Leveraging prior genome sequences identified strains, tested hypothesis drive ‘community structure’. found support pairing between most abundant Specifically, genome-wide analyses two commonly partnered high, reciprocal encoded by Together, enable ‘holobiont’ synthesize (vitamin B7), an important vitamin levels diet.

Language: Английский

Citations

9

Assessing co-diversification in host-associated microbiomes DOI Open Access
Andrew H. Moeller, Jon G. Sanders, Daniel D. Sprockett

et al.

Journal of Evolutionary Biology, Journal Year: 2023, Volume and Issue: 36(12), P. 1659 - 1668

Published: Sept. 26, 2023

When lineages of hosts and microbial symbionts engage in intimate interactions over evolutionary timescales, they can diversify parallel (i.e., co-diversify), producing associations between the lineages' phylogenetic histories. Tests for co-diversification individual their have been developed previously, these applied to discover ancient symbioses diverse branches tree life. However, most host-microbe relationships are not binary but multipartite, that a single host-associated microbiota contain many lineages, generating challenges assessing co-diversification. Here, we review recent evidence complex microbiota, highlight limitations prior studies, outline hypothesis testing approach designed overcome some limitations. We advocate use microbiota-wide scans co-diversifying symbiont discuss tools this purpose. simple host systems be extended entire phylogenies (e.g., metagenome-assembled or isolate genomes, amplicon sequence variants) sampled from clades, thereby providing means identifying present within microbiota. The relative ages clades corroborate co-diversification, multi-level permutation tests account multiple comparisons non-independence introduced by repeated sampling species. Discovering will generate powerful opportunities interrogating molecular evolution lineage turnover ancestral, host-species specific

Language: Английский

Citations

9

Microbial symbionts are shared between ants and their associated beetles DOI Creative Commons
Catalina Valdivia,

Justin A. Newton,

Christoph von Beeren

et al.

Environmental Microbiology, Journal Year: 2023, Volume and Issue: 25(12), P. 3466 - 3483

Published: Nov. 15, 2023

The transmission of microbial symbionts across animal species could strongly affect their biology and evolution, but our understanding patterns dynamics is limited. Army ants (Formicidae: Dorylinae) hundreds closely associated insect guest (myrmecophiles) can provide unique insights into interspecific symbiont sharing. Here, we compared the microbiota workers larvae army ant Eciton burchellii with those 13 myrmecophile beetle using 16S rRNA amplicon sequencing. We found that previously characterized specialized bacterial were largely absent from myrmecophiles, whose communities usually dominated by Rickettsia, Wolbachia, Rickettsiella and/or Weissella. Strikingly, different myrmecophiles often shared identical genotypes these common bacteria. Protein-coding gene sequences confirmed close relationship Weissella strains colonizing larvae, some several species. Unexpectedly, also similar to infecting dissimilar animals inhabiting very habitats: trout whales. Together, data show interacting share much microbiota, versatile inhabit possibly transmit a diverse range hosts environments.

Language: Английский

Citations

9

Selective enrichment of founding reproductive microbiomes allows extensive vertical transmission in a fungus-farming termite DOI Creative Commons
Veronica Sinotte, Justinn Renelies‐Hamilton, Sergio Andreu‐Sánchez

et al.

Proceedings of the Royal Society B Biological Sciences, Journal Year: 2023, Volume and Issue: 290(2009)

Published: Oct. 17, 2023

Mutualistic coevolution can be mediated by vertical transmission of symbionts between host generations. Termites complex gut bacterial communities with evolutionary histories indicative mixed-mode transmission. Here, we document that strains is congruent across parent to offspring colonies in four pedigrees the fungus-farming termite Macrotermes natalensis. We show 44% colony microbiome, including more than 80 genera and pedigree-specific strains, are consistently inherited. go on demonstrate this achieved because colony-founding reproductives selectively enriched a set non-random, environmentally sensitive termite-specific microbes from their origin. These transfer workers high fidelity, after which priority effects appear influence composition establishing microbiome. Termite thus secure specific, co-evolved critical colonies. Extensive yet imperfect inheritance implies maturing benefits acquiring environmental complement combinations termite, fungus vertically transmitted microbes; mode emerging as prevailing strategy for hosts assemble adaptive microbiomes.

Language: Английский

Citations

8

Physiological and evolutionary contexts of a new symbiotic species from the nitrogen-recycling gut community of turtle ants DOI
Benoît Béchade, Christian Cabuslay, Yi Hu

et al.

The ISME Journal, Journal Year: 2023, Volume and Issue: 17(10), P. 1751 - 1764

Published: Aug. 9, 2023

Language: Английский

Citations

6

Phylosymbiosis: The Eco-Evolutionary Pattern of Insect–Symbiont Interactions DOI Open Access
Man Qin, Liyun Jiang, Gexia Qiao

et al.

International Journal of Molecular Sciences, Journal Year: 2023, Volume and Issue: 24(21), P. 15836 - 15836

Published: Oct. 31, 2023

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

Language: Английский

Citations

5