The Hologenomic Basis of Speciation: Gut Bacteria Cause Hybrid Lethality in the Genus Nasonia

@article{Brucker2013TheHB,
  title={The Hologenomic Basis of Speciation: Gut Bacteria Cause Hybrid Lethality in the Genus Nasonia},
  author={Robert M. Brucker and Seth R. Bordenstein},
  journal={Science},
  year={2013},
  volume={341},
  pages={667 - 669}
}
Microbes → Host Speciation? No living organism is an individual—an individual's microbiota can outnumber the host's somatic cells. Working in parasitoid wasps, Brucker and Bordenstein (p. 667, published online 18 July) now suggest that the gut microbiota can play a crucial role in speciation and hybrid lethality. In a clade of parasitoid wasps, interspecies hybrids survived when reared on antibiotic-treated sterile food (thus eliminating gut microbiota), but experienced high mortality when… 
Evolution: Speciation meets microbiomes
TLDR
The authors showed that the microbiomes of F2 hybrids just before lethality are distinct from those of either parental species, and when parents and hybrids were reared in a way that eliminated gut microorganisms, hybrid lethality was rescued.
Analysis of intestinal microbiota in hybrid house mice reveals evolutionary divergence in a vertebrate hologenome
TLDR
Analysis of the gut microbiota of two house mice subspecies reveals genetic incompatibilities, aberrant immune gene expression and increased intestinal pathology associated with altered community structure among hybrids, providing unique insight into the consequences of evolutionary divergence in a vertebrate ‘hologenome’.
Genomes of Gut Bacteria from Nasonia Wasps Shed Light on Phylosymbiosis and Microbe-Assisted Hybrid Breakdown
TLDR
It is shown that bacterial genomes in Nasonia differ from other environments and harbor genes with unique functions that may regulate phylosymbiotic relationships, thus supporting a hologenomic tenet that the same members of the microbiome and the host genome impact phylosYmbiosis, hybrid breakdown, and speciation.
The native microbiome of the nematode Caenorhabditis elegans: gateway to a new host-microbiome model
TLDR
This first systematic analysis of the nematode’s native microbiome reveals a species-rich bacterial community to be associated with C. elegans, which is likely of central importance for the understanding of the worm's biology.
Host determinants of among-species variation in microbiome composition in drosophilid flies
TLDR
It is concluded that drosophilid flies display robust among-host species variation in host controls over microbiota composition that has diversified in response to selection pressures which are not tracked by host phylogeny.
Genomes of gut bacteria from Nasonia wasps shed light on phylosymbiosis and microbe-assisted hybrid breakdown
TLDR
It is shown that bacterial genomes in Nasonia differ from other environments and harbor genes with unique functions that may regulate phylosymbiotic relationships, and 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.
Disentangling a Holobiont – Recent Advances and Perspectives in Nasonia Wasps
TLDR
This review presents the Nasonia species complex as a model system to experimentally investigate questions regarding the impact of different microbes, including heritable endosymbionts, on the extended phenotype of the holobiont and the establishment and regulation of a species-specific microbiota.
Comparative Gut Microbiota of 59 Neotropical Bird Species
TLDR
It is suggested that microbial sampling during field collection of organisms would propel biological understanding of evolutionary history and ecological significance of host-associated microbiota.
Invasive freshwater snails form novel microbial relationships
TLDR
Comparison of New Zealand and European populations of the freshwater snail Potamopyrgus antipodarum found that while invaders do carry over some core microbial taxa from New Zealand, most of their microbial community is distinct, highlighting that invasions can result in the formation of novel symbioses.
A globally ubiquitous symbiont can drive experimental host evolution
TLDR
It is shown that across geographically distant locations (South Africa, France, Cape Verde), Leucobacter isolates vary substantially in their virulence to an associated animal host, Caenorhabditis nematodes, which combined with natural variation in virulence provides real‐world potential for LeUCobacter community composition to influence host fitness.
...
...

References

SHOWING 1-10 OF 29 REFERENCES
THE ROLES OF HOST EVOLUTIONARY RELATIONSHIPS (GENUS: NASONIA) AND DEVELOPMENT IN STRUCTURING MICROBIAL COMMUNITIES
TLDR
The results indicate that all three species of the parasitoid wasp genus Nasonia share simple larval microbiotas dominated by the γ‐proteobacteria class; however, bacterial species diversity increases as Nasonia develop into pupae and adults, which suggests that the structure of an animal's microbial community is closely allied with divergence of host genes.
Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution.
TLDR
The hologenome theory of evolution considers the holobiont (the animal or plant with all of its associated microorganisms) as a unit of selection in evolution and fits within the framework of the 'superorganism' proposed by Wilson and Sober.
Speciation by symbiosis.
Functional and Evolutionary Insights from the Genomes of Three Parasitoid Nasonia Species
TLDR
Key findings include the identification of a functional DNA methylation tool kit; hymenopteran-specific genes including diverse venoms; lateral gene transfers among Pox viruses, Wolbachia, and Nasonia; and the rapid evolution of genes involved in nuclear-mitochondrial interactions that are implicated in speciation.
GENETIC AND DEVELOPMENTAL BASIS OF F2 HYBRID BREAKDOWN IN NASONIA PARASITOID WASPS
TLDR
It is shown that hybrid larvae that carry the incompatible allele on chromosome 5 halt growth early in their development and that ∼98% die before they reach adulthood, suggesting that the incompatible mitochondrial locus is one of the six mitochondrial‐encoded NADH genes.
Characterization of the Active Microbiotas Associated with Honey Bees Reveals Healthier and Broader Communities when Colonies are Genetically Diverse
TLDR
Colonies with genetically diverse populations of workers, a result of the highly promiscuous mating behavior of queens, benefited from greater microbial diversity, reduced pathogen loads, and increased abundance of putatively helpful bacteria, particularly species from the potentially probiotic genus Bifidobacterium.
Wolbachia-induced incompatibility precedes other hybrid incompatibilities in Nasonia
TLDR
The results indicate that Wolbachia-induced reproductive isolation occurred in the early stages of speciation in this system, before the evolution of other postmating isolating mechanisms (for example, hybrid inviability and hybrid sterility).
HYBRID BREAKDOWN BETWEEN TWO HAPLODIPLOID SPECIES: THE ROLE OF NUCLEAR AND CYTOPLASMIC GENES.
TLDR
Experiments clearly demonstrate that the latter incompatibility is not due to maternal-effect genes, but to cytoplasmically inherited elements, supporting the view that hybrid lethality genes tend to be recessive.
Temperature stress increases hybrid incompatibilities in the parasitic wasp genus Nasonia
TLDR
Investigation of the effect of developmental temperature in Nasonia hybrids shows that extreme temperatures strongly affect both hybrid sterility and mortality, and underline the sensitivity of hybrid incompatibilities to environmental factors and the effects of unstable epistasis.
Hybrid incompatibilities in the parasitic wasp genus Nasonia: negative effects of hemizygosity and the identification of transmission ratio distortion loci
TLDR
The data show that diploid F1 hybrid females suffer less from hybridization than haploid F2 hybrid males, and accentuate the need to broaden the view of Haldane's rule to include species with haplodiploid sex determination, consistent with the original definition.
...
...