The Extended Phenotype

The central theorem of the extended phenotype: An animal’s behaviour tends to maximise the survival ‘for’ the genes for that behaviour, whether or not those genes happen to be in the body of the particular animal performing it.

The quote above is from Richard Dawkins (Dawkins, 1982), p233, and there is no doubt that the idea of the extended phenotype (EP), has changed the way we think about evolution. It requires a rethink of what constitutes an individual and much else besides. My favourite example of EP is to be found in the interaction between the genes of host and parasite.  Here genes of the parasite typically reach outside the body of the parasite to manipulate host behaviour (Poulin, 2010).

By definition parasites reduce host fitness. But the parasite that harms its host may be damaging its own reproductive potential. Hence the parasite has a vested interest in the reproductive success of its host. Indeed, a parasite can enhance it’s own fitness and, at the same time that of its host, through the harmonious collaboration between the genes of host and parasite. So, in practice, parasitism merges into symbiosis and parasitism must be seem to extend from fitness benefit to parasite alone all the way to benefit for both parasite and host. He cites the extreme example of mitochondria and the chloroplasts of plants. Both originate as independent parasites, eventually evolving to an intimate permanent relationship within the cells and life cycle of the host.

My aim is to apply Dawkins' EP reasoning to a host/parasite system I have spent several years studying. I refer to the relationship between a common chironomid midge, Paratrichocladius rufiventris and two parasites, a mite Unionicola ypsilophora and a mermithid worm, probably Gastromermis rosea (McLachlan, 2006), (Figs. 1 and 2). I consider only the female host midge. For my present  purpose the male can be left aside except for his role as a mate. The part the male plays  is considered elsewhere (McLachlan, 1999). I therefore consider only three interactors; female midge, mite and worm. I do not distinguish sex in the parasites. I use the term fitness in its original sense as used by Darwin and Wallace, i.e. the capacity to reproduce (Dawkins, 1982), pp181-182.

For the host female mating is a necessary prerequisite to send her to water to oviposit. And it is in the water that both parasites find their definitive hosts; a bivalve snail for the worm and midge pupa for the mite. So, both female host and her two parasites can only close their life cycles if the host has mated (McLachlan, 1999). Furthermore, the mite appears to enhance the mating success of the host, thus promoting fitness gains, both for its self and for both parasites.

How might the midge/mite relationship have evolved? We are not dealing with an arms race where gains for interactors are apposed (Dawkins, 2006). Rather we appear to be dealing with a case where both interactors gain - aptly been termed the Jack Sprat principle by Richard Dawkins (Dawkins, 1982), pp. 239-240. It is easiest to understand the Jack Spat principle if  attention is focused on genes rather that phenotypes.  “Selection goes on at that lower level - the level of the component parts of a harmonious complex”. This is Dawkins’ model 2. In model 2 it is the genes that are the target of selection (Cronin, 1991), p1007). How do the genes of the midge gain from cooperation with those of the mite and visa versa?

Jack Sprat model 2 is essentially a frequency dependent model (Dawkins, 2006), p240). The genes at the lower frequency, in whatever player they are found, automatically carry a selective advantage due to their rarity, so increase in frequency until an Evolutionarily Stable Strategy  (ESS), is achieved (Maynard Smith, 1982). Mites are bright red which could be acting as a supranormal signal of the normal red ventral surface of the female (species name rufiventris). The male midge that mates with a female lacking a worm gains in fitness (McLachlan, 2006). Thus a gene in a male that enables him to recognise the supranormal signal of a female with a mite, would spread in the population until competition with rivals lead to an ESS. The end result is harmonious cooperation of midge and mite genes outside the bodies of each - that is, the extended phenotype in operation.

Fig. 1. Parastic mites on a female midge host. (From (McLachlan, 2012).

Now to introduce the second parasite, the mermithid worm. The worm infects only the female midge and renders her sterile. The infected female thus has zero fitness but there is something else here. Remember that worm gains when an infected female returns to water. So there is theoretical possibility of adaptive manipulation by the worm. For instance, could the worm manipulate the physiology of his host to shift resources normally put to eggs into flight muscle. Such a manipulation would  lead to improved flight range in the search for water, like the case of crabs infected with the parasite Sacculina (Dawkins, 1982), p. 214). Here we have the testable prediction that flight muscle mass is greater in worm infected females.  I wish I had carried out test.

Fig. 2.  Mermithid worm emerging from female host. g, mass of  a single worm. Scale bar 0.5mm. (From (McLachlan, 2012).

To summarise, I view manipulation between a midge and its parasites in the light of EP. The EP approach extends understanding beyond reasoning limited to manipulation (McLachlan, 1999). What new insights does EP offer in understanding the adaptive strategies of the midge and its two parasites? I suggest that EP provides something beyond the standard idea of manipulation because it includes an explanation of how manipulation happens. EP also has the power to change how we see an individual. A  midge with a mite or worm is no longer a midge but something else - rather like a rabid dog manipulated by the rabies virus. Such a dog is not longer a dog but a different organic being. So, the debate over at what level selection acts is not over (Dawkins, 1982), p.121. Because EP has focused attention on genes, I have been lead to frequency dependent selection thinking and a better understanding of how the midge system could have evolved as an ESS. 

References

Cronin, H. (1991). The Ant and the Peacock (1993 ed.). Cambridge: Cambridge University Press

Dawkins, R. (1982). The Extended Phenotype. (1999 edition ed.). Oxford: Oxford University Press

Dawkins, R. (2006). The Selfish Gene. Oxford: Oxford University Press.

Maynard Smith, J. (1982). Evolution and the Theory of Games. Cambridge, UK: Cambridge University Press.

McLachlan, A. J. (1999). Parasites promote mating success: the case of a midge and a mite. Animal Behaviour, 57, 1199-1205.

McLachlan, A. J. (2006). You are looking mitey fine: parasites as direct indicators of fitness in the mating system of a host species. Ethology Ecology and Evolution 18, 233-239.

McLachlan, A. J. (2012). Phenotypic plasticity and adaptation in a holometabolous insect, the chironomid midge. ISRN Zoology. 2012, 8 pages.

Poulin, R. (2010). Parasite manipulation of host behaviour: an update and frequently asked questions. In H. J. Brockman (Ed.), Advances in the study of behaviour. (pp. 151- 186). Burlington, MA: Academic Press.