Relationships involving a “household of three” hold a fascination that is part prurient and part wonderment: prurient for perhaps obvious reasons, and wonderment as it’s sometimes hard enough to make a ménage à deux work! Historically this domestic arrangement has been the lifestyle of choice of a surprisingly large and diverse set of influential thinkers and creative individuals, including Aldous Huxley, Lord Nelson, Carl Jung, Erwin Schrödinger, and Hattie Jacques.  Indeed, one of my favourite musicians, David Crosby, wrote a song about such relationships (Triad) which got him kicked out of The Byrds.

In nature, ménage à trois are occasionally encountered and may be more common than we think, and have been on my mind because this week I’ve been talking about mutualistic relationships with my first year undergraduates.  Mutualisms are interactions between species in which both benefit, as opposed to exploitative relationships such as predation or parasitism in which one of the partners is at a disadvantage (being eaten is a great disadvantage….)  Mutualistic interactions are common and important, and include many (but not all) plant-pollinator interactions, seed dispersal by birds and other animals, mycorrhizal relationships between plants and fungi, and many more.  As well as studying plant-pollinator interactions, I’ve a long-standing interest in the full breadth of these examples of “biological barter“, in all their varied forms.

In most cases mutualistic relationships involve pairs of species (for example a plant and a pollinator) although these species pairs are embedded within a larger network of interactions: that plant may have many pollinators, and those pollinators may service other plants.  In this sense it requires just two partners to make the interaction work – a “household of two”.  More rarely, research on the biodiversity of species interactions throws up examples of “households” involving three species, and a fascinating case has recently been worked out and published by Jonathan Pauli and colleagues.  This involves three-toed sloths and their relationship with the algae and moths that colonise the sloth’s fur – you can read the abstract here.  In summary, the algae benefit from nutrients provided by the moths living in the fur; the sloths eat the algae to supplement a restricted diet of leaves; the moths benefit from the sloths transporting them to defecation sites where they lay their eggs, then recolonise the sloths.  This slothy ménage à trois is a wonderful instance of interdependency within nature.

The other case of a three-part mutualism with which I’m familiar is that between anemonefish, and sea anemones and the algae which are housed in their tentacles.  The fish and the anemones provide mutual defence of one another, whilst the algae photosynthesise and provide carbohydrates to the anemone, and benefit from the nitrogenous waste produced by the fish.  It’s a system that I’ve done a little work on with marine biologist colleagues, specifically the broad scale biogeography of the interaction and its local assemblage structure, but we’ve not studied the whole three-part system. 

What other three-part examples are there in nature?  I’d be very interested to hear about any of which you’re aware.

It begs a question as to whether three is an upper limit to the number of species that can engage in such relationships?  Are there any four- or five-part mutualisms?  Or are these too unstable over evolutionary time, because if one species goes extinct it could cause the extinction of other species?  Interesting questions about fascinating interactions!