The far-reaching effects of the relationship between an animal and its resident gut microorganisms are becoming ever clearer. New findings suggest it can even create barriers that keep species separate.
The process of speciation, whereby one lineage splits into two independent gene pools, has at its heart the evolution of barriers to gene flow that maintain differences when populations are in contact. Gene flow can be reduced in many ways, including failure to mate, sperm–egg incompatibility, and sterility or inviability of hybrids. Writing in Science, Brucker and Bordenstein1 describe a novel source of reproductive isolation: the influence of resident gut microorganisms on hybrid survival.
The concept of microbial involvement in reproductive isolation is not new2. In the 1990s, it was recognized3 that the very low survival rates of hybrid offspring from two closely related wasp species was influenced by the presence and strain of Wolbachia bacteria in the parents. More recently, it was demonstrated that environmentally induced changes in the composition of the gut microbiota could affect mate preference in Drosophila fruitflies4. Brucker and Bordenstein's work likewise examined the role of gut microbiota in reproductive isolation, but focused on the death of hybrid larvae rather than mate preference, and studied a situation in which the pool of environmental microbes was constant.
Their study organisms were parasitic wasps of the genus Nasonia, which lay their eggs in the pupae of flesh and filth flies (Fig. 1). The fly host represents both a source of nutrition and an environmental pool of microbes, and the authors had previously established5 that different Nasonia species acquire distinct communities of resident gut microorganisms (their 'gut microbiomes') from this common microbial pool. This differentiation of microbiomes was linked to the hosts' phylogeny: the microbiomes of individuals from the closely related species Nasonia giraulti and Nasonia longicornis were more similar than that of a more distantly related species, Nasonia vitripennis. Brucker and Bordenstein hypothesized that this differentiation creates a setting in which dysfunctional interactions could arise between hybrids and their gut microbiota.
To test this idea, the authors examined the male offspring formed by crosses between N. vitripennis and N. giraulti, most of which die during larval development. They noted that dying larvae were melanized, a characteristic of microbial pathology. Furthermore, the gut microbiota of the hybrid larvae were dominated by Proteus mirabilis bacteria, in contrast to those of the parental species, which are dominated by Providencia species. By manipulating the exposure of the larvae to bacteria, the researchers established that the presence of gut microorganisms was necessary for hybrid pathology and death: the hybrid larvae had near-normal fitness when they were reared on a bacteria-free diet, but their viability declined when Proteus and Providencia bacteria were introduced to the culture medium together, and when Providencia were introduced alone. Hybrid lethality was also reinstated when Escherichia coli bacteria, which are not typically found in the guts of these wasps, were introduced to the bacteria-free medium. Intriguingly, the authors also found that several gene-variant combinations in the host genome that have previously been associated with hybrid inviability were present in normal inheritance ratios in larvae reared on a bacteria-free diet.
These findings demonstrate that hybrid inviability can be associated with a perturbed host–microbiome interaction. Indeed, there are reasons to believe that the involvement of symbiotic microorganisms in reproductive isolation may be common. First, resident microbiota affect both organismal development and function6, and this is likely to be the case in all species with a gut. Second, divergences in animal–microbiome interactions between lineages are widely observed2,7, and lineage divergence is the core requirement for hybrid dysfunction. Dietary shifts, for instance, alter the microbes to which a species is exposed and those that flourish in its gut7,8. The different characteristics of these organisms and the differing services they provide to the host may create selective pressures for modification of host systems. Furthermore, evolutionary changes in host systems can modify the constitution of the microbiome5,7. In sum, there is good reason to believe that the host–microbiome interface will diverge over time, from both sides, such that hybridization creates interface combinations that may malfunction.
Brucker and Bordenstein previously extended2 the concept of genetic interactions leading to hybrid dysfunction (called Bateson–Dobzhansky–Muller incompatibilities) to include potential incompatibilities between the genomes of the host and its microbiota. But the bacteria-reintroduction experiments in the current study suggest that, although the inviability of Nasonia hybrids results from disharmony of gut bacteria, this is not particularly dependent on the identity (nor, therefore, the specific genetics) of the microbes. Rather, it seems that hybrid Nasonia mishandle what is possibly the most fundamental and universal biotic interaction: the development and regulation of their microbiome. This breakdown echoes other cases in which biotic interactions are important in creating hybrid inviability. In Heliconius butterflies, for example, related species diverge to have distinct warning colouration patterns that reduce predation by birds, but hybrids between the species have a pattern that is not recognized, resulting in increased predation and a form of 'extrinsic' hybrid inviability9.
The work of Brucker and Bordenstein provokes several questions. For example, how many cases of hybrid inviability derive from a misfunctioning interface between the host and its microbiota? Can dietary shifts drive evolutionary divergence at the host–microbiome interface, and thereby contribute to the evolution of reproductive isolation? Perhaps most exciting is the idea that there may be interactions with specific microbiome components in hybrids. If this were the case, the microbiome would expand the network of possible interactions within an organism, and potentially accelerate the rate at which incompatibility evolves. Our gut feeling is clear: the evolutionary biology of the intimate and complex interactions between animals and microbes will be a hot topic in the years to come.
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