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 

Boucher, D. H. (1992). Mutualism and Cooperation. In E. F. Keller & E. A. Lloyd (Eds.), Keywords in Evolutionary Biology. (pp. 208-211). London: Harvard University Press.

Bronmark, C., and Hansson, L.-A. (2005). The Biology of Lakes and Ponds. (Second ed.). Oxford: Oxford University Press.

Dawkins, R. (2004). A devil's chaplain. London: Phoenix.

McLachlan, A. J. (1976). Factors Restricting the Range of Glyptotendipes paripes EDWARDS (Diptera: Chironomidae) in a Bog Lake. Journal of Animal Ecology, 45, 105-113.

McLachlan, A. J. (1978). Interactions between Freshwater Animals and Microorganisms. Annals of applied Biology, 89, 162-165.

McLachlan, A. J., and Dickinson, C. H. (1977). Micro-organisms as a foctor in the distribution of Chironomus lugubris ZETTERSTEDT in a Bog Lake. . Archiv fur Hydrobiology, 80, 133 - 146.

McLachlan, A. J., and McLachlan, S. M. (19975). The Physical Environment and Bottom Fauna of a Bog Lake. Archiv fur Hydrobiology, 76, 198 - 217.

McLachlan, A. J., Pearce, L. J., and Smith, J. A. (1979). Feeding Interactions and Cycling of Peat in a Bog Lake. Journal of Animal Ecology, 48, 851-861.

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

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

Freshwater Biology - How I would teach it

Figure 1. The  beauty of amphibians, here an unnamed frog.

 

As a young man in Africa and later in the UK, I taught freshwater biology at both second and final year levels. My 1966 PhD and postdoc work were undertaken over a period of some eight years at such wonderful places as Lake Kariba ( 4 years) and lake Chilwa (4 years), in tropical Africa and I remained active in freshwater research and publication until the mid 1980s. I was thus presumably qualified to carry out teaching responsibilities in freshwater biology. My aim here is to produce an outline plan for a hypothetical course in freshwater biology which I would teach today, given the chance. From the perspective of nearly 40 years I have been looking back on those early years and wondering why freshwater biology seemed such an intellectually unrewarding subject and how it might be improved. A large part of this failing, I believe, is the absence of a unifying theme in undergraduate courses. This applies as much to my own earlier teaching as to the efforts of others. It  applies to freshwater biology specifically and not so much to ecology in general. Furthermore, freshwater biology, as it its taught today, has tended to be about the nature of the habitat rather than about the biota. It is this emphasis on habitat that may be responsible for the absence of a strong theme. A greater role for freshwater fauna could readily lead to a unifying theme. The theory of evolution custom made for the role. We freshwater biologists should continuously reminded ourselves of Theodore Dobzhansky's famous maxim . ... "Nothing in biology makes sense except in the light of evolution" (Dobzhansky 1973).

With this in mind I thought a way forward  might be to create a list of key literature sources. Under the umbrella of evolution I would emphasise three things. First, weight would be placed on  the waters of Africa. Africa has an exceptional diversity of freshwater habitats and faunas and was the cradle of mankind and, to quote Richard Dawkins, p265, ..." this alone makes African ecosystems an object of singular fascination" (Dawkins 2004). For that reason field courses in Africa would be desirable and a realistic possibility, at least in the financial climate prevailing before I retired in 2004. Second, in contrast to most courses I know of, I  would make vertebrates the principal study organism. This melds well with an emphasis on Africa with its wonderful world of fish and amphibians (Fig. 1). The study of amphibians leads naturally to the adaptive laboratories of ephemeral waters such as rain pools. Amphibians illustrate beautifully two things; phenotypic plasticity, that is the facultative response of which an organism is capable in the face of environmental challenges. An example of phenotypic plasticity is the development of  calluses on the hands of gardeners. Most amphibians have a larval stage dependent on standing water. It is these immature stages that show an astonishing range of adaptations to typically ephemeral and unpredictable water on which they depend. The larval stages are amenable to experimental manipulation, for example, the addition of iodine to the water, to alter developmental rate (Spaul 1928). Such manipulation opens the possibility of exploring mechanisms of plasticity and developmental adaptation. I can think of no finer laboratory to engage the interests of students.

Turning to fish (and I expressly do not meant commercial fisheries): fish tend to dominate permanent waters to the virtual exclusion of amphibians. The fish faun of the great lakes of Africa; Malawi, Tanganyika, and Victoria,  have captured the interest of biologists for many years. Here there is an outstanding demonstration of the wonders of adaptive speciation. I refer to the  indigenous cichlid flocks inhabiting these waters (Kocker 2004).

I give little attention to rivers and streams only because I am here attempting a  hypothetical exercise with myself as sole teacher and my research experience does no fit me for advanced teaching in those habitats. 

Core literature sources appear below:

  1). Two books to provide the ecological background. Begon et al (Begon, Townsend et al. 2006)/Corze and Reader (Croze and J. 2000).

Townsend et al. are here intended to provide access to the general principles of ecology. They provide the ecological setting for freshwater biology and set ecology within the evolutionary landscape. Croze and Reader offer a good general ecology text set in Africa and hence an appropriate accompaniment for Beadle (below).  Croze and Reader provide a fine introduction to the rich mammalian ecology of Africa. *

2).  The inland waters of tropical Africa.  Leonard  Beadle (Beadle 1974).

Leonard has the knack of exciting in his reader a sense of adventure and wonder at the wilderness and the adaptive challenges encountered by freshwater dwelling animals in  the  waters of Africa. This is just the text, I believe, to attract students to a research career in the subject.  Here both an introduction to both phenotypic plasticity (traditionally called 'adaptation' by physiologists), and changes in gene frequency within a population. i.e. evolution, can be found.

3). The Biology of Lakes and Ponds. Brönmark and Hanson (Bronmark and Hansson 2005).

To broaden an African emphasis and to introduce small and ephemeral water bodies, I would  include this excellent book. Research effort in Europe and America has favoured large lakes. By contrast these authors emphasise biotic adaptations in smaller waters. These, after all must be many orders of magnitude more abundant than larger lakes and because they are small tend to be ephemeral - drying out or freezing in unpredictable patterns which raise fascinating questions about adaptation.

4) The evolutionary ecology of rain pools

To build on the biology of temporary waters there are the ubiquitous rain pool. These are the ultimate in small bodies of water. They are the  most ephemeral and numerous waters, sometimes holding only a few ml of water. They lend themselves well to experimental manipulation. In view of their abundance rain pools may be where adaptive changes in the evolution of freshwater faunas principally take place - and even where life on earth may have originated, see Charles Darwin famous,  'Warm Little Pond' (Darwin 1Feb 1871). Some fine work on the biogeography of rain pool dwelling crustacea is being undertaken  by Brian Tims, Vanshoenwinkel  and colleagues in Africa and Australia (Pinceel, Brendonck et al. 2013). My own research in Africa focused on the extraordinary insects breeding exclusively in rain pools on rock surfaces (McLachlan and Ladle 2001). A recent explosion of research on rain pool faunas include some interesting adaptations among amphibians and even fish. 

References

Strother, P.K., Battison, L., Brasier, M. D. and Wellman, C. H. (2011). Earth's earliest non-marine eukaryotes. Nature 473, 505-509.

Beadle, L. C. (1974). The Inland Waters of Tropical Africa. London, Longman.

           

Begon, M., C. R. Townsend, et al. (2006). Ecology. From Individuals to Ecosystems., Blackwell Publishing 

           

Bronmark, C. and L.-A. Hansson (2005). The Biology of Lakes and Ponds. Oxford, Oxford University Press.

           

Croze, H. and R. J. (2000). Pyramids of Life. London, Harvill Press.

           

Darwin, C. (1Feb 1871). Warm Little Pond.

           

Dawkins, R. (2004). A devil's chaplain. London, Phoenix.

           

Dobzhansky, T. G. (1973). "Nothing in Biology makes sense except in the Light of Evolution." The American Biology Teacher 35: 125-129.

           

Kocker, T. D. (2004). "Adaptive Evolution and Explosive Spciation: The Cichlid Fish Model." Nature Reviews Genetics 5: 288-298.

           

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

           

Pinceel, T., L. Brendonck, et al. (2013). "Environnmental change as a driver of diversification in temporary aquatic habitats: does the genetic structure of extant fairy shrimp populations reflect historic aridification?" Freshwater Biology 58: 1556-1572.

           

Spaul, E. A. (1928). "Comparative Studies of Accelarated Amphibian Metamorphosis. ." Journal of Experimental Biology 5: 212-232.

* On reflection, and with an eye to the evolutionary theme, I cannot avoid adding the highly effective text book by Scott Freeman and Jon Herron (1988). I wish this fine book had been available when I was an undergraduate.

Freeman , S. and Herron, J. (1998). Evolutionary analysis. Prentis Hall, New Jersey.

Stephen J. Gould on the Scientific Method

Steven J. Gould is widely considered a modern evolutionary biologist of comparable public stature to Richard Dawkins. I would hold Ontogeny and Phylogeny (Gould 1977), among the half dozen most influential biology books I have read in my zoological career. The compelling poetical language is a great bonus. Yet I am puzzled by his understanding of adaptation spelled out in Wilson’s Ladder (Gould 1987) p34.

He considers the attempt to understand adaptation has failed due to what he calls a Panglossian Adaptationism. These Panglossians, he believes, are engaged in an enterprise to label every trait adaptive, purely as an act of belief. These assertions of adaptation he calls Just So Stories from the famous stories for children by Rudyard Kipling (Kipling 1902). Incidentally, it is strange that Gould appears to miss the point to these stories – they are pure Lamarckism. Something could have been made of this.

But this is a quibble. What is fundamental is his misrepresentation of the nature of scientific research. We all know that scientific research requires a testable hypothesis as a starting point. An assumption of adaptation by so called Panglossians is just such a starting point; it is an hypothesis, not a conclusion. Any hypothesis stands or falls after rigorous testing. This is how the hypothetico-deductive process in science works (Medawar 2006) p12-32. I believe Gould is wilfully misunderstanding the matter. This may be one of his bits of mischief such as the fuss over punctuated equilibria (Eldredge and Gould 1972). And reading John Tyler Bonner today (1 November 2018), I find support for my contention (Bonner 1993), pp61-62.

 I therefore reject Gould’s worries about adaptation. A much better appraisal of the difficulties involved in a proper understanding and identification of adaptation is given by George Williams encapsulated in the term teleonomy (Williams 1966).

References

Bonner, J. T. (1993). Life Cycles. Reflection of an Evolutionary Biologist. Princeon Univesity Press.

Eldredge, N. and S. J. Gould (1972). Punctuated Equilibria: an Alternative to Phyletic Gradualism. Models in Paleobiology. T. J. M. Schopf. San Francisco, Freeman Cooper: 82-115.

           

Gould, S. J. (1977). Ontogeny and Phylogeny. London, The Belknap Press of Harvard University Press.

           

Gould, S. J. (1987). An Urchin in the Storm. London, Collins Harvill.

           

Kipling, R. (1902). Just So Stories. London, MacMillan and Co.

           

Medawar, P. (2006). The Strange Case of the Spotted Mice and Other Classic Essays on Science. Oxford, Oxford University Press.

           

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

           

Phenotype limited male mating tactics

I here attempt to extend the general overview of what looks like size determined mating tactics of male midges (McLachlan 2012). The available evidence now suggests that there may be, not one but three male phenotypes; ά, β and γ; thus the mating system of these flies may be more complex than previously imagined. Furthermore quite different mating behaviours appear to be associated with each male phenotype. The γ are the smallest and adopt a sit and wait behaviour under the mating swarm. These appear to intercept arriving females resting before entering the swarm. The mating tactic of β males depends, by contrast, on agility to capture mates on the wing in mating swarms. But, like singing crickets, these males have limited endurance (Mowles 2014). It is here that the recently discovered role of wing beat harmonics may be the proximate requirement for a successful mating event (Gibson, Warren et al. 2010; McLachlan 2012). Finally, ά males, I suggest, enjoy good endurance and there is some evidence that, to capture a mate, these mimic the flight behaviour of a major predator of mating swarms (post SSD revised 24/10/2014). The three phenotypes may demonstrate a phenotype limited ESS (Maynard Smith 1982), where size is the trait of the adult male that determines mating tactic, within a genetically determined mating strategy. The approximate relative sizes of ά and γ males are shown in Fig. 1; β males are intermediate.

  

Fig.1. Approximate relative size of ά (left) and γ males of the common chironomid midge Chironomus plumosus.

If there are distinct male phenotypes these ought to be detectable in the size frequency distribution of males from mating swarms and from individuals in the grass under a swarm. Results are shown in Fig.2.

Fig. 2. From (McLachlan and Neems 1989).

These samples were taken by net sweep through male mating swarms (a) and from the vegetation under the swarm (b), (McLachlan and Neems 1989). Recall that what is being tested is evidence for the presence of three male phenotypes. The evidence in Fig. 2 encourages a prediction of distinct male phenotypes, notably in the vegetation (a,d), but sometimes also in the swarm (b), which strongly suggest the presence of a distinct phenotype. In one case (a) three distinct size classes suggest the presence of all three phenotypes, ά, β and γ. More examples of discontinuous distributions among both midge swarm and mating pairs appear typical, e.g. Fig. 4b (McLachlan and Neems 1989): Fig. 1a (McLachlan 1986): Fig. 1a (McLachlan and Allen 1987), not shown here.  

There is more. Changes in the size frequency distribution of males in the swarm as the evening proceeds show the average size of males in the swarm to increase with time. This is what would be expected if β and γ males progressively tire and leave the swarm to rest. In the chaoborid midge Chaoborus flavicans (Fig. 3), the average size of males in two swarms increases progressively (left hand column, rs=0.29, P<0 .005="" 112="" 94="" column="" flies="" hand="" nbsp="" p="" right="" rs="0.2," span="">

Fig. 3. Size frequency distribution in the midge Chaoborus flavicans at progressive times (i) – (iii) about 15 minutes apart during swarming. Sized classes containing the mean are shaded, n = number of flies measured. Size classes are at intervals of 0.1mm starting at 4.0 mm. The two columns represent samples from duplicate swarms. After (McLachlan and Neems 1989).

Decisive evidence in support of a three phenotype hypothesis might be provided by wing shape measurements. Wing shape measurements, as used by Outomuro and co-workers for damsel flies (Outomuro, Rodriguez-Martinez et al. 2014), provide a ready-made method applicable to the midges. Wing shape measurements can readily be obtained from wings removed for the fly and measured at 10 magnifications in the usual way (McLachlan 1986). I predict that results will show statistically significant functional differences in wing shape among male phenotypes. For midges, broad wings (i.e. low aspect ration wings) are known to be are associated with sustained flight and narrow ones (high aspect ratio), with aerobatic flight (McLachlan 1986).

As a first step in thinking about an hypothesis of phenotype limited mating among midges I assume that the male phenotypes are genetically determined, labelled strategies by Thornhill and Alcock (Thornhill and Alcock 1983), p286. This is a different case from a condition dependent mating behaviour discussed by West-Eberhard (West-Eberhard 2003) and Thornhill and Alcock (Thornhill and Alcock 1983), p296-293 which concerns flexible phenotypic responses within a single genotype. Based on a premise of strategies together with findings and conjecture presented here, I suggest that three male phenotypes may form an evolutionarily stable strategy in the sense that it is uninvadable by mutants of the same size but with different mating behaviours. To be an ESS all three tactics would have to carry an equal fitness payoff. Any change in behaviour would be inconsistent with the size of the individual and thus carry lower fitness benefits leading to selection against the mutant. It has been suggested by my colleague John Lazarus, that we are not here dealing with a classical  ESS game but rather with the rock-paper-sissors evolutionaly game (Sinervo & Lively 1996).  This game relaxes the need for equal fitness payoff and has great explanatory power. 

Three distinct male phenotypes appear in quite a different classes of animal, namely the isopod crustacean Paracerceis sculpta (Shuster and Wade 2003), and in three species of Calopteryx damsel flies (Outomuro, Rodriguez-Martinez et al. 2014). For the isopod Paracerceis, Shuster and Wade provide a detailed analysis of phenotype limited mating tactics. The fact that three male phenotypes are found in this completely different class of animals hints that body size based strategies may turn out to be common, or even a near universal evolved solution to size based male intrasexual competition.

To recap; the hypothesis to be tested is that the mating system of the male chironomid and chaoborid midges involves at least three, phenotype limited mating strategies, based on body size and correlated differences in wing shape. To test this hypothesis good samples are required of males in mating swarms, in the vegetation under swarms and of mating pairs from both swarms and vegetation. For anyone who knows how to find mating swarms this should not be too difficult to achieve and could result in the untangling of the components of the baffling mating system of these ubiquitous insects. More work is needed to tie in functional difference in wing shape.

References

Gibson, G., B. Warren, et al. (2010). "Humming in Tune: Sex and Species Recognition by Mosquitoes on the Wing." Journal of the Association for Research in Otolaryngology. 11: 527-540.

           

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

           

McLachlan, A. J. (1986). "Sexual dimorphism in midges: strategies for flight in the rain-pool dweller Chironomus imicola (Diptera: Chironomidae)." Journal of Animal Ecology 55: 261-267.

           

McLachlan, A. J. (1986). "Survival of the smallest: advantages and costs of small  size in flying animals." Ecological Entomology 11: 237-240.

           

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

           

McLachlan, A. J. (2012). SWARM BASED MATING SYSTEMS (revised May 2019). http://www.atholmclachlan.blogspot.com/.

           

McLachlan, A. J. and D. F. Allen (1987). "Male mating success in Diptera: advantages of small size ." Oikos 48: 11-14.

           

McLachlan, A. J. and K. J. MacLeod (In Preparation). "Sexual dimorphism in the chironomid midge - is it interesting?".

           

McLachlan, A. J. and R. M. Neems (1989). "An Alternative Mating System in Small Male Insects. ." Ecological Entomology 14: 85-91.

           

Mowles, S. L. (2014). "The physiological cost of courtship: field cricket song results in anaerobic metabolism." Animal Behaviour 89: 39-43.

           

Outomuro, D., S. Rodriguez-Martinez, et al. (2014). "Male wing shape differs between condition-dependent alternative reproductive tactics in territorial damselflies." Animal Behaviour 91: 1-7.

Sinervo, B., and Lively, C. K  (1996). The rock-paper-scissors game and the evolution of alternative male strategies. Nature, 380, 240-243, & 198-199.

           

Shuster, S. M. and M. J. Wade (2003). Mating Systems and Strategies. Princeton, Princeton University Press.

           

Thornhill, R. and J. Alcock (1983). The Evolution of Insect Mating Systems. London, Harvard University Press.

           

West-Eberhard, M. J. (2003). Developmental Plasticity and Evolution. Oxford, Oxford University  Press.

           

Further discussion with John Lazarus has lead to the following note added on 23 July 2016:

Alternative male midge mating tactics and the Rock-Paper-Scissors Game

John Lazarus

Centre for Behaviour and Evolution, Newcastle University

In the original Rock-Paper-Scissors (RPS) children’s two person game each player simultaneously chooses one of three plays by showing their hand: a closed fist (Rock); an open palm (Paper) or two splayed fingers (Scissors). The rules are that Scissors cut Paper; Paper wraps Rock; and Rock blunts Scissors. Therefore each strategy beats one other and is beaten by the third, so there is no single winning strategy.

If the game is played in evolutionary time there will be a cycling in the frequency of strategy types over time since as one strategy increases in frequency this benefits the one that beats it but is worse for the one it beats. 

There is evidence for an evolved set of RPS strategies in a male lizard (Sinervo and Lively 1996). Might RPS also explain the three male midge strategies described here? We don’t know at present but here are some thoughts on the matter.

1. Although the 3 types don’t compete directly, as in RPS, the RPS evolutionary scenario would apply if the success of each type was frequency dependent in the following way. It would need to be the case that each type did better when there was an increase in the frequency of one of the other two types but worse when there was an increase in the other.

It seems that this might be the case. In the first place if there are fewer gammas intercepting females then males in the swarm would be expected, as a whole, to have higher mating success. However, it would need to be the case that one swarm type did better as gamma frequency declined but the other type did worse. This could happen in the following way. It is known that at any one time in the swarm betas have higher mating success than alphas due to their greater aerodynamic prowess (Crompton, Thomason, and McLachlan 2003;

McLachlan 2011). To simplify the argument assume that all females entering the swarm are taken by betas until all betas have left the swarm with a mate; above this threshold number of females alpha males start to get matings and increase their success as female entry rate increases further, while beta mating success remains constant (all betas having mated). Recall that female entry rate increases as gamma male frequency declines.

To summarise: for betas, below the threshold female number their success increases with female numbers, and above the threshold stays constant. For alphas it is the reverse; below the threshold their success is zero (in this simplest case) and above the threshold their success increases with female numbers. This picture fits the RPS scenario but with the complication of a threshold effect. And the threshold effect will be weakened in the real world, where some 
.alphas do get matings in the presence of betas.

2. If the 3 types are genetically distinct, as Athol Mclachlan suggests, then natural selection acting on an RPS system would result in cycling of the frequencies of the 3 types over generations. To test for such cycling one would need to be able to define a midge population in the field. 

3. The same logic might predict cycling fluctuations in male numbers in and around swarms over a single evening if males move between swarms to increase their mating success.

Athol comments on the RPS reasoning that John's ideas are testable. There are at least two testable hypotheses. First, do males move between swarms differentially depending on size? This can be tested using my swarm marking techniques. (McLachlan 1997). Second, do frequencies of the 3 phenotypes change in a swarm over time. This too is testable with the usual net sweep samples of swarms followed by wing length measurements (e.g. McLachlan and Allen 1987). 

References

Crompton, B., Thomason, J. and McLachlan, A.J. (2003). Mating in Viscous Universe: the Race is to the Agile, not to the Swift. Proc. R. Soc. London (B), 270: 1991-1995.

McLachlan, A. J. (1997). Size or symmetry: an experiment to determine which of the two accounts for mating success in male midges. Ecoscience, 4: 454-459.

McLachlan, A. J. (2011). Phenotypic Plasticity and Adaptation in a Holometabolous Insect: the case of the Chironomid midge. ISRN Zoology doi: 10.5402/2011/152342.

McLachlan, A. J. and Allen, D. F. (1987). Male mating success in Diptera: advantages of small size. Oikos 48: 11-14.

Sinervo, B., and Lively, C. M. (1996). The rock-paper-scissors game and the evolution of alternative male strategies. Nature, 380, 240-243 & 198-199 (the latter pages being a commentary by John Maynard Smith).