Organisms with fuzzy borders

Everyone's on the human microbiome story these days -- the bacteria in our gut that make us fat, thin, sick, well -- but a new paper in Current Biology ("Horizontally Transmitted Symbionts and Host Colonization of Ecological Niches", Henry et al., Sept 9, 2013) tells the story of the aphid microbiome and the role that symbionts play in the life history of this insect.  Symbionts don't make aphids fat or thin, but they do have other significant effects.  

Symbiotic bacteria in the insect gut are common, as they must be if they're not pathogenic. They have been the subject of research for decades.  They are often inherited, in that offspring have the microbiome of their parents, and the bacterial mix can affect interactions between members of a given species, the use of plants on which insects feed, can boost the insect's immune system, or affect their response to temperature changes, or even manipulate their reproduction.  Insects can be host to multiple simultaneous symbionts, ecosystems which undoubtedly have their own internal dynamics:  Ferrari and Vavre suggest in a 2011 paper that symbionts and their hosts are "dynamic communities that affect and are affected by the communities in which they are embedded."

Aphids, also known as "plant lice," are sap-sucking insects that either live on or destroy plants, depending on your point of view.  If you are a farmer, they're very destructive but if you happen to be an aphid, you're just doing your job.  

Pea aphid, Acyrthosiphon pisum, mother and nymphs. Wikipedia

Aphids can host both primary and secondary symbionts; most aphids are infected with primary symbionts which can be essential to survival as they supplement the insect's nutrition and can protect the insect from pathogens, while fewer aphids host secondary symbionts, bacteria that play less crucial roles but that may still improve the insect's lot in life, including increasing its reproductive fitness.

Symbionts can reside in the cytoplasm of their hosts' cells, and are most often transferred vertically, from mother to offspring, but Henry et al. report considerable horizontal transmission as well, from adult insect to adult insect, just as the small genetic ring-structures called plasmids are transmitted from bacterium to bacterium. The mechanisms of horizontal transfer aren't well-documented, but Jennifer White notes in a perspective on the Henry paper in Current Biology, that it can be via the host plant, via a shared natural enemy, or via sexual transmission. 

Henry et al. looked at genetic diversity, ecological correlates, and mode of transmission for 1,104 pea aphids from 11 kinds of plants, in 155 different places in 14 countries.  They used the DNA sequence of the aphid's primary symbiont, the vertically inherited Buchnera, as the basis for grouping the insects by symbiont similarity.  They used nuclear markers from the aphids to group them by adaptation to specific host plants.  They also determined which of four secondary symbionts, if any, the aphid was hosting.  Knowing this alone, one would expect there to be a 'tree' of historical and/or geographical relationships based on these aspects of sharing, and this is apparently so:

The authors report that host plant was non-randomly associated with symbiont.  That is, which plant the aphid preferred was correlated with the symbionts it hosted. And, genetic structure of the symbiont was associated with host ecology -- sometimes but not always this included preferred plants, but always geographic factors such as temperature and aridity of the locale. 

Henry et al. found horizontal transfer to be common, and "associated with aphid lineages colonizing new ecological niches, including novel plant species and climatic regions."  This is a spatial kind of phylogeny rather than a temporal parent-offspring tree of relationships.  Indeed, they found that similar species of symbionts infect aphids on similar host plants in similar ecosystems around the world, and that mode of transmission is associated with type of plant and ecological setting.  This finding suggests that there is also a temporal family tree, and the authors wondered which came first then, the symbiont or the adaptation to host plant.  Whichever, it likely happened long ago.

They used a Bayesian approach to test for correlated evolution between two traits.  This means they had some prior notion of relationships that might be found, and used data to refine the likely true story.  This is a method they explained fully in the supplemental material.  "We found clear evidence that the pea aphid’s colonization of particular host plants is associated with infections by two of the four symbiont species."

And they found that aphids will switch to particular host plants when infected with a particular symbiont; indeed, they don't switch to these plants at all when they aren't infected by these symbionts.  "Our work supports the idea that symbionts assist their host in exploiting specific ecological niches and occupying different climatic zones and is consistent with the hypothesis that symbionts form a horizontal gene pool that is actively sampled by hosts when confronting novel environmental challenge." 

That means that the evolutionary history has been fostered not just by individual competition, but by shared interactions and success.  The authors suggest that the symbiont influences choice of feed plant because there is a fitness benefit to feeding on a specific plant.  And this in turn would be beneficial to the bacterium, which thrives when the aphid thrives.  Henry et al. state that "rates of colonization of new host plants are higher when a symbiont is carried rather than when aphids on particular host plant have higher rates of gaining certain bacteria."  They conclude that "secondary symbionts constitute a eukaryote horizontal gene pool, a reservoir of potential adaptations, or preadaptation."

There are no new basic concepts in this work, even though it seems to be very well done.  But every well-documented instance of complex interactions, that we have known about at more visible levels of observation, that are documented down to the molecular and cellular level, reinforces an overall view of the web-like network that evolution has woven.

Whether transmitted horizontally or vertically, or whether symbionts need to be considered purely in the light of selective adaptation, asking how symbionts can affect the behavior of their host reflects a fairly recent view of biology in which organisms have fuzzy borders. In this case, the symbiosis is good for the host and the bacteria, if not so good for the plant.  But it does reinforce the view that cooperation is important in life.