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.

The academic life of Athol John McLachlan

 ATHOL JOHN McLACHLAN 1939 - ?

Here I attempt to pick up on what, in hindsight, were important events in my life as a zoologist. In preparing this essay I started out to do something but ended up with what turns out to be a second version of my Autobiography (A. J.  McLachlan, 2009). Here I make some different points and illustrated with photographs. Because they are better considered elsewhere, I have not included much of the experiences of wild Africa as a Nuffield PhD student at Lake Kariba (Fig. 1), the privilege of working with the visionary Professor Margaret Kalk on Lake Chilwa (Fig. 2), or the fulfilling years at Newcastle University.

Fig. 1. Elephants grazing at Sengwa on the shores of Lake Kariba in mid 1960. 

Fig. 2. Kachulu jetty on Lake Chilwa in the late 1960s.

School days and after  (1950-2004).

My school was what was called a private school located far off in the Transvaal veld. I did not excel there, either academically or, except for athletics, in sport. The academic failing was partly mine but also, it must be said, the fault of the teaching which was essentially non-existent. On the positive side, the headmaster, Evelyn Cloete, did recognise and encourage an interest as a naturalist which I and my younger brother Ian had developed together long before high school. Because of this background in natural history I was allowed free reign to study zoology for matric and to do field work in the surrounding veld, all on my own initiative. No other boy or girl was allowed to break bounds at will in this way. For much of this time my interest was taken by the termite mounds which abound on the Transvaal high veld (Fig. 3).

Fig. 3. Digging in a termite mound, perhaps looking for snakes? (from the internet).

In the natural course of events many of these mounds are abandoned by the termites and provided a habitat for a variety of animals including burrowing snakes (Typhlops and Leptoyphlops) and the black headed snake Aparallactus capensis, Fig. 4). Among mammals dwarf shrews (Suncus infintesimilus?), were common. Captured specimens were sometimes brought back to school for observation and study. The teaching staff were tolerant of this activity even when a large spitting cobra or rinkhals, Hemachatus haemachatus, Fig. 5, escaped and terrorised the school for days.

During school holidays these activities continued with observation and collecting. Reptiles were sometimes kept alive or carefully preserving in formaldehyde. Preserved material was added to the museum in the bedroom shared with my brother. At this time I was much influenced by reading the  expeditions of Gerald Durrell (Durrell, 1954) and of John Steinbeck  (Steinbeck, 1945), among others. It was the expeditions of Durrell to the Cameroons that filled me with wonder and a determination to get  to tropical Africa. My interest in tropical Africa eventually lead to my spending  some eight years there. Looking back I believe  it was the freedom  to pursue my own interests that launched me into a deeply rewarding life as a university lecturer and researcher. An Honours degree in zoology under the formidable Professor B. I. Balinsky was followed by an appointment as Nuffield Research Fellow at the University College of Rhodesia an Nyasaland. After obtaining a PhD degree there from the University of London, I gained  a lectureship at Chancellor College in Malawi and then at Newcastle University where I stayed until retirement in 2004.

Fig. 4. Some snakes that inhabit old termite mounds in South Africa. From the top,  Aparallactus capensis, and the blind burrowers Leptopyphlops and Typhlops spp.

Fig. 5. The common spitting cobra of the South African high veld.

The main line of my research over 45 years or so, stretches from Africa to the UK. For convenience I divide this period according to the life cycle of my principal subject of study -  the chironomid midge. To have devoted ones life to a single, seemingly obscure taxon, would seem narrow at best and contradicts the advice of the famous E. B. Ford (1964),p. 9...."don't be a slave to your material". By contrast,  John Tyler Bonner (Bonner, 1993), devoted his life's to a single taxon, those strange creatures, the slime moulds.

The larval stages of an aquatic insect

To continue in Africa, sometime in the 1980s I read a series of  papers by Howard Hinton on the larval stages of an extraordinary insect, the chironomid midge. The larvae of this midge inhabit very ephemeral rain pools on large rock expanses in tropical Africa. These pools typically last just a few hours after rain and the larval inhabitants of at least one species appear able to survive desiccation of their habitat indefinitely (Hinton, 1968; A. J. McLachlan and Ladle, 2001). I had been working on the fauna or Lake Chilwa in Malawi for some years (Kalk et al. 1979), and on one visit to Malawi. prompted by reading Hinton, I sought rain pools on rock.  With stunning luck a series of pools of the right type  (Fig. 6.), was found early one Sunday morning, close to my laboratory at Chancellor College (University of Malawi).

 

Fig. 6. Some typical rain pools on rock surfaces in Africa. 

The discovery of  these pools lead to some 30 years further work on rain pool dwellers (McLachlan and Ladle, 2001). Supported by Royal Society and Linnaen Society and with the  encouragement of Chancellor College, this was a good time. I was looking for adaptations to the ephemeral nature of rain pools, which, to slightly stretch a point, can be considered a major selective pressure of the fresh water habitat in general. Taking this as given, rain pools provide a good example of the essential adaptations required of freshwater dwelling organisms to a habitat which may last less that the minimum duration of the larval stages. To meet this difficulty two strategies have been identified. First, the evolution of desiccation resistance. Desiccation resistance has been achieved by creating a microhabitat as in Dasyhelia, the larval stages of biting midges. An alternative method of surviving desiccation in situ has been the  evolution of desiccation tolerance in the tissues of  the larvae of   Polypedilum vanderplanki. This species leads to interesting conjecture about panspermia, (Crick and Ogle, 1980), and the colonisation of space (Hinton, 1968)(see also the essay posted in April 2019). Second, there is the adaptive adjustment of the duration of larval stages by manipulation of growth rate. Growth rate depends on cues from the pool about evaporative extinction which in turn involves the adaptive ability to hasten the onset of metamorphosis.

The adult stages of aquatic insects

The adults of chironomids, like those of mayflies, are an essentially non-feeding stage of the life cycle with the sole functions of mating and dispersal. It is mating that has been my principal focus. We know that this takes place in a mating swarm, where the latest evidence suggests that there are at least two size related mating strategies (Crompton, Thomason, and McLachlan, 2003)(see also the essay posted on 24 October 2019). Both depend fundamentally on biomechanics rather than the more familiar visual displays of animals (Andersson, 1994; Darwin, 1871). Small males appear to depend on aerobatics to capture fleeing females (Crompton et al., 2003). Larger males, by contrast, appear to mimic their own predator, an empid fly, to achieve the same end (A. J. McLachlan, 2014, 2015).

A switch from the study of larval forms to that of the adult involves a bigger change of interest than might at first appear. Indeed, it required a move in subject matter from the ecology of fresh water animals to the world of evolution - specifically that of sexual selection. Furthermore, no one with an interest in sexual selection would choose chironomid midges as a case study. Accessibility to the secrets of their mating system is not easy. There is good reason for careful choice of study species. An example is the seminal work of Geoffrey Parker promoted by the readily observed and manipulated mating behaviour of dung  flies (Parker, 1978). However, my motivation was not primarily the study of mating systems. Rather my wish was to achieve a better understanding of the behavioural ecology of chironomid midges; particularly those inhabiting temporary rain pools. This seems a worth while aim. As elegantly pointed out by John Tyler Bonner (1993), p15. ...." Organisms are not just adults - they are life cycles". Indeed, a change from ecology to evolutionary thinking requires breaking away from entrenched attitudes among ecologist, expressed in such influential text books  as those of Allee and of Emerson (Allee, 1949) (Emerson, 1960), quoted by Cronin (Cronin, 1991), p278. These attitudes to adaptation set the tone for evolutionary thinking among many ecologists which persist to this day. I refer to the seductive allure of group selection of Whynne - Edwards (Wynne-Edwards, 1986), comprehensively now replaced  by Williams (Williams, 1966), individual level and Dawkins gene centred thinking (reviewed by Cronin (Cronin, 1991) pp 267-310). For ecologists this transition has been a struggle. George Williams typifies the frustration with ecologists. After a meeting at which  Emmerson presented a paper, Williams was moved to remark to his wife ..."if  Emmerson's presentation was acceptable biology, I would prefer another calling. "

References

Allee, W. C., Emerson, A. E. , Park, O., Park, T. and Schmidt, K. P. . (1949). Principles of Animal Ecology. Philadelphia: W. B. Saunders.

Andersson, M. (1994). Sexual Selection. Princeton: Princeton University Press.

Bonner, J. T. (1993). Life Cycles. Reflections of an Evolutionary Biologist. Princeton: Princeton University Press.

Crick, F., and Ogle, L. (1980). Directed Panspermia. In D. Goldsmith (Ed.), The Quest for Extraterrestrial Life. Mill Valley, C..A.: University of Science Books.

Crompton, B., Thomason, J., and McLachlan, A. J. (2003). Mating in a viscous universe: the race is to the agile, not to the swift. Proceedings of the Royal Society, London (B). 270, 1991-1995.

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

Darwin, C. (1871). The descent of man and selection in relation to sex. (2 ed.). New York, 1959: The Modern Library, Random House.

Durrell, G. (1954). The Bafut Beagles.: Harmandsworth, Pengine

Emerson, A. E. (1960). The Evolution of Adaptation in Population Systems. In I. Tax (Ed.), The Evolution of Life: It's Origin, History and Future.
Ford, E. B. (1964). Ecological Genetics, Methuen and Co Ltd, London.

Hinton, H. E. (1968). Reversible suspension of metabolism and the origin of life. . Proceedings of the Royal Society, London (B). 171, 43-47.
Kalk, M., McLachlan, A. J. and Howard-Williams, C. (1979). Lake Chilwa. Studies of change in a tropical ecosystem. Monographiae Biologicae, 35. 

McLachlan, A. J. (2009). Autobiography Athol John McLachlan 1939 -?

McLachlan, A. J. (2014). Phenotype limited male mating tactics among some non-biting midges. (pp. http://www.co.uk/atholmclachlan.blogspot.co.uk): Google.

McLachlan, A. J. (2015). The midge in the mating system - A sheep in wolf's clothing?, http://www.google.co.uk/atholmclachlan.blogspot.co.uk.

McLachlan, A. J., and Ladle, R. (2001). Life in the puddle: behavioural and life-cycle adaptations in the Diptera of tropical rain pools. Biological Reviews 76, 377-388.

Parker, G. A. (1978). Searching for Mates. In J. R. K. N. B. Davies (Ed.), Behavioural Ecology: An Evolutionary Approach. (First ed.). Oxford: Blachwell Scientific Publications.

Steinbeck, J. (1945). Cannery Row.: Viking Press.

Williams, G. C. (1966). Adaptation and Natural Selection. Princeton: Princeton University Press.

Wynne-Edwards, V. C. (1986). Evolution Through Group Selection. . Oxford: Blackwell Scientific Publications.

Ecosystem services

I have been re-reading Sir Keith Thomas's fascinating book on the history of man's relationship with other animals (Thomas, 1983). The core belief pervading medieval Christendom appears to be that the natural world was put there, presumably by God, for a purpose, the purpose being to benefit mankind. Life, it was held, was given to animals purely to keep their flesh fresh until we wished to eat them. It is easy to feel superior to our ancestors, but hold on a minute. Are we really any better now?   

To get my meaning some context is necessary. A concept has recently emerged among ecologists termed 'ecosystem services' (Moss, 2010). The concept is clearly understood by ecologists and evolutionary biologists  to describe mutualistic relationships such as the service provided by bees to flowers. In an adaptive sense therefore, flowers have bread bees to pollinate them and in this way promote flower reproduction (Dawkins, 1996), p 264. This concept points to a profound level of understanding achieved by these scientists about the nature and functioning of the natural world. But, as so often happens, the popular press has got hold of the concept and sees it to mean services supplied by the natural world solely for the benefit of homo sapiens. To understand the wonders of the natural world purely as a benefit to man is degrading. Wikipedia provides the following definition. "Our health and well being depend upon the services provided by ecosystems and their components, water, soil, nutrients and  organisms. Therefore  ecosystem services are the processes by which the environment produces resources utilised by man such as clean air, water food and  materials." (The bold type is mine). So here we are right back to Keith Thomas's medieval world  - not so superior after all are we!

references

Dawkins, R. (1996). Climbing Mount Improbable. London: W. W. Norton.

Moss, B. (2010). Ecology of Fresh Waters. A view for the Twenty-First Century. (4 ed.). Chichester, UK: Wiley -Blackwell.

Thomas, K. (1983). Man and the Natural World: Changing Attitudes in England 1500 - 1800. Harmandsworth: Penguin Books.

The strange case of Mabuya quinquetaeniata.

Fig. 1. Mabuya quinquetaeniata with male above and female below.

As boys my brother and I first encountered these beautiful lizards (Fig. 1), near the Limpopo river in South Africa. Now, as a retired biologist, I look back on those early days and wonder about the evolution of the vivid uniforms of these lizards. The colours are especially noteworthy because both sexes are highly decorated, and in quite different ways. This is not unknown but it is typically the male alone that is decorated. They look so different that we believed them to be different species until one day a mating pair was observed. Even after establishing that the two lizards are of the same species, there is still the difficulty of determining which is male and which female. Many years ago I dissected a blue-tail and found eggs - hence we at last knew that the blue tails are female. This is as far as we got as boys. In those days, in the 1950s, there was no internet and none of  the many identification aids available today, so these simple observations carried a fine sense of discovery.  

What we had unknowingly stumbled onto was an area of evolutionary biology, sexual colour dimorphism, full of active debate ever since the conflict between Darwin and Wallace over 200 years ago (Cronin, 1991) pp123-155, (Roughgarden and Akcay, 2010). I here adopt sexual selection as the selective force responsible for the evolution of mating displays including an adaptive role for colour (Andersson, 1994). In principle, I use natural selection to account for colour in the female and sexual selection for that in the male. But there are caveats (see below). This is in contrast to Darwin's conclusion in The Origin (C. D. Darwin, 1859), but in full agreement with his later revision seen in The Descent (C. Darwin, 1871), quoted by (Cronin, 1991), p148.

To return to my central point to look more closely at the fact that both sexes in Mabuya, rather than just the male are uniquely decorated. Within the world of sexual selection the bright colours of the males can be understood to have evolved under choice by females but the same does no apply to the female. Unlike the male, the tail alone is  bright. The key to understanding how selection is operating here lies in the phenomenon of autotomy, widespread among lizards. This is the ability to shed the tail when attacked. When detached under attack the colourful tail squirms vigorously so it is easy to imagine a predator like a bird, attacking the conspicuous tail while the cryptic female escapes. Although I  have not attempted it, this prediction could readily be tested by experiment. So here is natural selection operating in the female.

But this is not the full story. To better understand these lizards some further points must be made. First, like the female, the male is capable of autotomy and here too the tail is the most conspicuously coloured part of the body. So he also has an anti-predator device, thus after all his colours are not determined solely by sexual selection. Second, the body of the female is not really cryptic but is dark with conspicuous pale longitudinal stripes. Such stripes are seen among many reptiles. For example, in the elegant and common schaapsteker (Fig. 2). Here longitudinal stripes make the barer difficult to catch when it is on the move as we discovered  as boys attempting to catch these snakes by hand. Presumably a predator has the same difficulty. This hypothesis too, is readily tested by experiment. Both this and the experiment to test the adaptive role of autotomy are based on such commonly observed phenomena that they have probably been done many times for many species - but perhaps not.  Have they actually been carried out or merely inferred?

Fig. 2. A striped Schaapsteker on the move.

Thus we can go a long way to understanding the adaptive value of colour in this  lizard. To summarise; for the female, defence against predators is a mixture of a predator confounding pattern and  a highly coloured tail which can behave as a predator lure. Appearance of the female is therefore solely under the control of natural selection.  In the male, by contrast, both sexual attraction (sexual selection), and predator avoidance (natural selection), are the adaptive forces involved. The bright colours also tell us something about the sensory systems of lizards and of predators. We can suggest that female Mabuya prefer orange/green and predators, possibly mostly  birds, bright blue.

Fig. 3. Eclectus roratus parrots with male on the left and female on the right.

Just to emphasise that these lizards are not unique in having both sexes highly coloured, I add a picture of a parrot with both sexes highly coloured (Fig. 3). What are the selective forces operating here? And what about the zebra below (Fig. 4.). Perhaps the greatest mystery of all, with indistinguishable sexes.

Fig. 4. Male and female zebra



My sole work into sexual dimorphism has concerned, not colour dimorphism at all but size differences between the sexes, referred to as sexual size dimorphism (SSD), (McLachlan, 2015; McLachlan, MacLeod, and  Neems, 2016), thus colour dimorphism is something new to me. but what a stimulating departure from the familiar it has been.

 References

Andersson, M. (1994). Sexual Selection. Princeton: Princeton University Press.

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

Darwin, C. (1871). The descent of man and selection in relation to sex. (2 ed.). New York, 1959: The Modern Library, Random House.

Darwin, C. D. (1859). The origin of species by means of natural selection, or the preservation of favoured races in the struggle of life. (Fascimile 1901 ed.). London: John Murray.

McLachlan, A. J. (2015). The midge in the mating system - A sheep in wolf's clothing?, http://www.google.co.uk/atholmclachlan.blogspot.co.uk.

McLachlan, A. J., MacLeod, K. J., and Neems, R. M. (2016). Sexual Size Dimorphism in the chironomid midge: A Sheep in Wolf's Clothing? Journal of Insect Behaviour (submitted).

Roughgarden, J., and Akcay, E. (2010). Do we need a Sexual Selection 2.0? Animal Behaviour, 79, e1- e4.

Blaxter Lough

Fig. 1. View of Blaxter Lough, the humic lake habitat studied here.

I want to return to an extraordinary situation discovered by me on the high moors of Northumberland. My intention is to re-examine this purely ecological story but this time in the light of evolution theory. This opens the door to some interesting and testable questions previously hidden. The story concerns the interrelationships among three organisms which allows them to flourish in the nutritionally impoverished environment of a humic lake. Relationship hinges on the faecal pellets produced by larvae of a chironomid midge, Chironomus lugubris, feeding on particles of peat introduced to the lake by wave action. Particles in suspension are rapidly colonised  by decomposer micro-organisms which evidently make otherwise refractory peat nourishing as food for the midge larvae. Faecal pellets are yet more heavily colonised by micro-organisms and  should therefore be attractive to the larvae as food. However, perhaps because they are too hard for their mandibles, the larvae appear not to make use of this seemingly valuable resource.

Fig. 2. Sectional diagram of a tube dwelling Chironomus larva with a swarm of Chydoris  swimming precisely over the faecal end of the tube. 

But now comes the interesting part. Midge pellets, although ignored by the insect larvae, appear to be grazed by a second arthropod, the Cladoceran Chydoris sphericus. These hold a pellet between their valves and rotate it while grazing its surface. In the lab, a cloud of Chydoris can be seen swimming precisely over the pile of faecal pellets produced by larvae, at only one end of the tube (Fig 2). Of course the crustacea also produce faecal pellets. Passing through the fug of a chironomid larva boosts  micro-organism populations so passing through the gut of a chydorid  would be predicted to harbour yet higher loads of micro-organism. Unlike their own pellets, those of Chydoris are of a size which should be easily consumed by larvae. Here there are two gaps in our data which call for formal investigation. First, what is the nutritional actual value of Chydoris pellets and are they actually consumed by Chironomus larvae? Second,  in artificial pools in the laboratory, unless chironomid larvae are added to the culture, Chydoris does not make an appearance. In the wild Chydoris adults appear in large numbers in the summer, supposedly spending the winter as diapausing eggs (ephippia), in the mud. Something, largely unknown, is required to break this diapause (Barnes, Calow, and Olive, 1988; Bronmark and Hansson, 2005). Thus there is a hint here of  some fundamental relationship between chironomids and chydorids beyond that of  food.

This whole interaction between these two arthropods is discussed by Mike Begon and colleagues (Begon, Townsend, and Harper, 2006), pp 340-341, and by Brian Moss (Moss, 2010), p 315. Research details can be found in (McLachlan, 1976, 1978; McLachlan and Dickinson, 1977; McLachlan and McLachlan, 19975; McLachlan, Pearce, and Smith, 1979).

Fig. 3.  Diagram summarising relationships between players, an insect larva, a crustacean and micro-organisms, in a putative mutualism centred on faecal pellets. a, chironomid faecal pellets. b, chydorid faecal pellets. The consumption of 'b' by the chironomid awaits testing.

I turn now to look at this story from an evolutionary perspective. As far as I know this has not been attempted before. The central question is whether the observed relationship between three organism; insect, crustacean and micro-organism, is an economy in the sense of Richard Dawkins (Dawkins, 2004), p 266, or an adaptation in the sense of George Williams (Williams, 1966). Only if it is an adaptation can it be referred to as a mutualism (Boucher, 1992). This is not an easy question to answer because economy and adaptation merge into each other and an economy may be moving, under selective pressure, toward an adaptation. The application of Pittendrigh's principal of teleonomy (discussed by George Williams (Williams, 1966), is useful here. What is required is the identification of a function. For example, in one case of well established mutualism, that of bees and flowers, the question 'what is the function of a flower?', is readily answered - it is to attract bees. Hence the bee/flower relationship is a true mutualism. Turning to the feeding relationships shown in Fig.3., feeding relationships based on faeces are by-product relationships (Dawkins, 2004). Faecal pellets are not organisms and hence cannot respond to natural selection. But they are colonised by bacteria and fungi which can respond. So we may be dealing with a mutualism after all. For a discussion of the relationship between mutualism and reciprocal altruism see (Boucher, 1992).

Turning from feeding to diapause; recall the finding that the presence of Chironomus larvae appear necessary for the appearance of Chydoris. What is implied is that the chironomid larvae somehow break the diapause of  Chydoris. In other words, there  appears to be some kind of intimate  relationship here not based on by-products. A formal, but straight forward experiment is required to explore this idea. A survey of humic lakes and perhaps of other representative kinds of lakes as well, could strengthen an assumption of mutualism if all three players are invariably found together. Thus diapause could be an adaptation if it answers to the principle of teleonomy because a function is readily identified - the function of Chironomus is to break diapause of Chydoris.

To summarise - what I have attempted is to re-examine an old piece of work in the light of evolution theory. This shows up a new set of questions. Key questions are; first that we are dealing with a true mutualism based on faeces and second that Chironomus larvae must be present for Chydoris also to be present. The first question can be tested by determining how consistently the three players are found together. An obligate association supports an hypothesis of mutualism. The second, the diapause breaking,  is readily tested by a simple experiment in the laboratory with replicate aquaria containing winter lake mud with chironomid larvae and a control set of replicate aquaria but without insect larvae. Thus both question are testable. Perhaps some one will pick it up. It could be rewarding.

references

Barnes, R. S. K., Calow, P., and Olive, P. J. W. (1988). The Invertebrates, A new synthesis. Oxford: Oxford University Press.

Begon, M., Townsend, C. R., and Harper, L. (2006). Ecology. From Individuals to Ecosystems. (4 ed.): Blackwell Publishing 

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