The basis for the origin of new species is thought to be well-known: new species emerge when two or more subpopulations of (what was formerly) the same species become sufficiently dissimilar in their genetic makeup that they can no longer breed with each other to produce fertile offspring. According to this narrative, changes in the genetic material of an individual organism, encoded in its DNA, represent the primary driving force behind speciation. A recent article published in Science [1] now suggests that the process of species formation may not be so straightforward, and that micro-organisms resident in the gut of a host organism may play a significant role in the evolutionary arc of their host. 

The microbial self

The concept that microbes can shape the evolution of their host is not new. Leigh van Valen, an evolutionary biologist at the University of Chicago, famously coined the “Red Queen Hypothesis” [2] that posited the unremitting arms race between an infectious bug and its host as a crucial evolutionary driving force. Just as the host is constantly evolving novel and more effective means of ridding itself of disease-causing microbes, the microbes themselves are ceaselessly improving on their armament of tools that allow them to evade the destructive immune defenses of the host.

It is not difficult to imagine how infectious pathogens can exert a powerful selective pressure on their host, since the outcome for individuals that fail to evolve new ways to best their microbial adversaries is often death. But what about the role of the trillions more microbes that colonize the gut, airways and skin of all living creatures, often without causing disease? Indeed, the vast majority of the microbes resident in an organism, collectively known as the microbiota [3], not only pose no harm but also provide countless benefits to their host. In the humble termite, gut bacteria help the insect break down the tough fibers in its wooden diet. In humans, the gut microbiota shape the development of the immune system, regulate nutrient absorption in the intestines, and have been the subject of a comprehensive research study by the National Institutes of Health (The Human Microbiome Project [4]). The fate of gut microbes is therefore intimately braided with that of their host; both sides suffer when either is missing from the partnership. No organism is then truly defined by its individual genetic material, but is instead a “superorganism” [5] emergent from the sum of its own DNA and that of its resident microorganisms. But do these resident microbes influence the evolutionary trajectory of their host and contribute to the formation of new species?

The germy cause of death in the hybrid offspring of parasitic jewel wasps

To address this question, Seth Bordenstein and Robert Bruckner at Vanderbilt University set out to investigate the role of the gut microbiota in making the offspring of two species of Nasonia unable to survive, a phenomenon known as hybrid lethality. Nasonia is a family of jewel wasps that parasitize various kinds of flies by laying their eggs into the pupae of the flies [1]. The authors looked at three closely-related species of NasoniaN. longicornis, N. giraulti, and N. vitripennis, because the hybrid offspring between the three species have very different fates; larvae born to N. longicornis and N. giraulti survive, while most male larvae born to N. vitripennis and either of the other two Nasonia species die (see Figure 1). The traditional theory of speciation would ascribe the doomed fate of the male hybrid progeny wholly to incompatibilities in the genetic material derived from the two parental wasps. However, Bordenstein and Bruckner found that most male larvae born to N. giraulti and N. vitripennis reared under sterile conditions survive. Re-introduction of bacteria into the larvae, either by exposing them to gut bacteria typically found in non-sterile hybrids or by transferring them into ambient conditions, rapidly causes death in the offspring. Interestingly, they also discovered that variations in the intestinal microbiota of different Nasonia species tracked closely with the evolutionary relationship between their hosts, suggesting co-evolution of Nasonia wasps with their microbial counterparts. Thus an incompatibility between parental genetic material and the microorganisms in their offspring also contributes to lethality in hybrids.

Figure 1. Fate of Nasonia species offspring. Photograph of a Nasonia wasp laying her eggs into the pupa of a fly courtesy of Indiana University http://newsinfo.iu.edu/asset/page/normal/8378.html.

How do the gut bacteria in the male hybrid wasps cause their demise? Bruckner and Bordenstein looked at the makeup of the bacteria in the hybrids and their parents and observed that the microbiota in hybrids destined to die is vastly different in their diversity and composition from that in their parents. Conversely, hybrids between N. longicornis and N. giraulti, which do not die, harbor a microbiota that closely resembles that of their parents. Bruckner and Bordenstein also found that doomed male hybrids turn on many immune pathways in their bodies, reminiscent of ongoing inflammation in the wasps. Hence the hybrids born to N. giraulti and N. vitripennis adopt an aberrant microbiota to which they may be maladapted to recognize and control. The ensuing inflammation, possibly coupled with an overgrowth of certain gut bacteria, could then overwhelm the developing wasp and result in its untimely death.

Beyond any single individual’s genes: the hologenome in evolution

If the microbiota of an individual organism can influence its evolutionary course, then perhaps the genetic information of an organism’s hidden microbes should also be included in the consideration of the individual’s DNA, with the totality of human and microbial genetic material known as a “hologenome” [6, 7]. Put another way, evolution would not simply be the outcome of single individuals competing against one another for survival but rather of individuals and their associated microorganisms competing together as one entity – a battle between hologenomes. The wealth and diversity of genetic material contributed by our erstwhile overlooked microbial residents would vastly increase the amount of raw material on which evolution can act. Not everyone supports the hologenomic theory of evolution [8]. But all agree that the work by Brucker and Bordenstein has introduced an entirely new and exciting aspect to the study of evolution – that we can no longer ignore the teeming microbiota in the origin story of species.

Tze G. Tan is a graduate student at Harvard Medical School.

References:

[1] Bruckner RM and Bordenstein SR (2013) “The Hologenomic Basis of Speciation: Gut Bacteria Cause Hybrid Lethality”. Science 341: 667-9.

[2] Van Halen L (1973) “A new evolutionary law”. Evolutionary Theory 1: 1-30. The name of the Red Queen Hypothesis was derived from Lewis Carroll’s Through the Looking-Glass, in which the Red Queen told Alice, “it takes all the running you can do, to keep in the same place”.

[3] An introduction to intestinal microbes and their impact on health in humans and animals by our own SITN contributors: http://sitn.hms.harvard.edu/uncategorized/2010/issue68/http://sitn.hms.harvard.edu/flash/2012/issue124b/.

[4] Human Microbiome Project. http://commonfund.nih.gov/hmp/.

[5] Wilson DS and Sober E (1989) Reviving the superorganism. J Theor Biol 136: 337-356.

[6] Ilana Zilber-Rosenberg and Eugene Rosenberg (2008) “Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution” FEMS Microbiol Rev 32: 723-735.

[7] Seth Bordenstein also maintains his own blog, http://symbionticism.blogspot.com/, where he writes about symbiosis and evolution and leads a lively discussion on the role of the hologenome in evolution.

[8] Kupferschmidt Kai (2013). “Gut microbes can split a species”. http://news.sciencemag.org/evolution/2013/07/gut-microbes-can-split-species.

One thought on “Gut Microbes and the Origin of Species

  1. Interesting that termites have a bacteria in their gut that helps them break down cellulose. I never new that before, I assumed their mandibles did most of the work.

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