Bacterial Threesome Throws up Evolutionary Surprise

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Symbiotic relationships, where two organisms ‘live together’ and rely upon each other to survive, are surprisingly common in the animal kingdom. The more we look, the more we find. What is less common, or at least less well documented, is the occurrence of speciation events within these partnerships. A recent study has revealed the first documented case of the speciation of a bacterial symbiont, inside the cells of a cicada. Even more interestingly, scientists believe it may have been little more than an evolutionary screw-up!

Symbiotic relationships can be quite casual, or extremely intimate, and are literally all around you. And inside you. The mitochondria inside your cells are symbiotic bacteria that joined our cells billions of years ago. Mitochondria show a pattern that is common in such intimate symbiotic relationships – over millions of years, partners in the relationship each have a reduced genome, with a complementary set of genes. This in turn makes them even more dependent upon each other. Mitochondria have only about 37 genes, compared to 1000 in a free-living bacteria. They simply don’t need many of their genes anymore because their host cells carry them. This is known as relaxed selection – because both members of the partnership carry the genes, a mutation in a gene in one partner will probably have no effect. The other member still has a functioning version of that gene, so the organism as a whole shows no negative symptoms, and natural selection is blind to the mutation. Only when both copies of a particular gene are degraded will natural selection step in, meaning that over time random chance will degrade complementary sections of each genome.


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All of this is well-documented, and well-understood. But researchers at the University of Montana recently stumbled across something that is not so run-of-the-mill. Whilst sequencing the genome of a cicada (Tettigades undata) and it’s two known bacterial symbionts, scientists discovered the genome of a third bacterium. The cicada’s three-way had turned into a foursome!

Upon closer inspection it became clear. Cicadas feed on plant sap, a carbohydrate-rich food source that leaves them lacking in protein. Instead of consuming a more varied diet, cicadas get protein by providing a safe, warm home to a couple of bacterial symbionts – Candidatus Hodgkinia cicadicola and Candidatus Sulcia muelleri, or Hodkinia and Sulcia for short. These symbionts trade essential amino acids, usually found in protein-rich food, for a nice place to live, and during their 10 million-year co-evolution together, the bacteria have stripped their genomes down to just 170 genes.

Then, about five million years ago, something rather unusual happened. Hodgkinia speciated into two almost identical bacterial species. Although initially identical, the two new species began undergoing the same process of gene loss that occurred between the bacteria and their host. Each species compensated for the other’s mutations, preventing natural selection from doing its job and removing harmful mutations from the population. These two symbionts now each possess even fewer genes than Sulcia, a set complementary to one another to achieve all the same functions that were once achieved by Hodgkinia alone. Only some of the cicada species in the genus Tettigadeshave this extra symbiont, allowing researchers to trace it’s origin to a date about 4 – 5 million years ago.

The authors say this speciation event may not have been an good one. It may be one of the first solid examples of non-adaptive evolution. It seems this chance speciation event slipped under the radar of natural selection, and genetic drift slowly degraded the genomes of each species until there was no going back. Each member of the partnership is now reliant on three other species to achieve the same functions they once achieved with just two. Natural selection wasn’t totally snoozing on this one, though, it did step in and make sure that no functions were actually lost. It made sure that the genomes of each new bacterium remained complementary to one-another, maintaining function albeit somewhat less efficiently.

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This event may also be one of relatively few examples of sympatric speciation, that is, speciation that occurs without any geographical separation – in the same place at the same time. Although sympatric speciation has always been speculatively considered plausible, the mechanisms that drive it have remained illusive, and the issue has been controversial. It seems, however, irrefutable in this case that the two new species of Hodgkinia arose within the same cell, definitely sympatric. The precise ecological conditions that led to this sympatric speciation event may be quite rare, however more research is needed to understand the evolutionary pressures that drove it.

A similar process has happened in leafhoppers, who also feed on sap and rely upon two obligate symbiotic bacteria, Sulcia (she gets around) and Candidatus Baumannia cicadellinicola. The Glassy-winged sharpshooter (Homalodisca vitripennis) and the blue-green sharpshooter (Graphocephala atropunctata, to be precise, gain amino acids from their two symbionts. Recent research conducted at the University of Texas revealed different rates of gene loss in the two symbionts, which the authors suggest may reflect differing mutation rates, metabolism and availability of nutrients. So far nobody has found any extra symbionts in these leafhoppers though, and speciation events like that are likely to be quite rare. Certainly, as a non-adaptive event, successful speciation that persists through evolutionary time, is likely to be very rare.

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