Do flies see red?

 A male chironomid midge carrying two red mites on his abdomen.











There are conceptual, philosophical and scientific difficulties in determining whether non-human animals have colour vision (see Kelber and Osario 2009, for example). In the case of insects, the received wisdom is that, in general, they are unable to detect the red part of the visible spectrum. This assumption persists and forms the theme, for example, of Richard Dawkins' compelling reasoning about the role of insects in shaping the evolution of angiosperm flowers (Dawkins 2009) pp46-54.

Studies of the mating behaviour of a common insect, the chironomid midge, Paratrichocladius rufiventris, has lead me to wonder about the assumption, specifically in the context of  chironomids and related Diptera (flies). In what follows I attempt to show why this is an interesting question and what evidence there is to resolve it. To begin I confine my reasoning to mating success in the male midge; a common type of fly. Factors determining mating success for the female are considered elsewhere (McLachlan 2008; McLachlan 2011).

Like most midge species (McLachlan and Neems 1995), P. rufiventris, mates on the wing, males forming huge swarms through which females fly to acquire a mate. Exactly how what happens in the swarm to lead to a mating remains unclear (Crompton, Thomason et al. 2003; McLachlan 2011), but there is some evidence that the chance a male has of mating is influenced by the presence of a common ectoparasitic mite, Unionicola ypsilophora (McLachlan 1999). This mite is bright red on colour and attaches to the ventral surface of its host’s abdomen. As the specific name, ‘rufiventris’ or red belly indicates, the abdomen is red in colour which raises the possibility that  improved mating success among mite-infected males is due to the mite acting as a supranormal sexual display signal, attractive to the female midge (McLachlan 1999). This in turn suggests that the mating system hinges on mate choice by the females. So, is the colour red important in the mating system  of chironoids in general? If so this effect involves well over 15,000 species worldwide (Coffman and Ferrington Jr 1984).

There is an interesting case for red detection, not only in midges but among insects in general. Indeed red pigment is widely distributed among insects.  Jerry Coyne (2009), although he does not cite his source, states  ..."pink is a color that bees favour", p,191. Here is another hint, one need think only of the wings of butterflies. These observations suggests that the sensory system of such insects is, after all, capable of detecting wavelengths in the red part of the light spectrum. For example, the giant tropical flower of Raflesia, which is pollinated by flies and is red in colour presumably to attract the pollinator. There is also the intriguing suggestion that the red of autumn leaves is a device evolved among some plant species to deter aphids. Originally suggested by Bill Hamilton I believe (Hamilton and Brown 2001), this idea has sparked much interest e.g. (Daring, Archetti et al. 2008; Archetti 2009). All this is suggestive but, for the best of my knowledge, the single case of red begin actually demonstrated to function as a sexual display ornament occurs among damselflies (Fitzstephens and Getty 2000; Sherratt and Forbes 2001). As a clincher, among the flies in general, Doekele and Stavenga (Doekele and Stavenga 1989), have found meta-state absorbing near the red part of the spectrum.


References

Archetti, M. (2009). "Evidence from the domestication of apple for the maintenance of autumn colours by coevolution." Proceedings of the Royal Society, (B).

Coffman, W. P. and L. C. Ferrington Jr (1984). Chironomidae. An Introduction to the Aquatic Insects of North America. R. W. Merritt and C. K. W. Dubuque, Iowa, Kendall/Hunt Publishing Company.

Coyne J. (2009). Why Evolution is True. Oxford University Press, Oxford, UK.

Crompton, B., J. Thomason, et al. (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.

Daring, T. F., M. Archetti, et al. (2008). "Autumn leaves seen through herbivore eyes." Proceedings of the Royal Society, (B). 276: 121-127.

Dawkins, R. (2009). The greatest show on earth. Bantam Press, London.

Doekele, G. and D. G. Stavenga (1989). Pigments in compound eyes. Facits of vision. D. G. Stavenga and R. C. Hardie. London, Springer Verlag.

Fitzstephens, D. M. and T. Getty (2000). "Colour, fat and social status in the male damselfly, Calopteryx maculata". Animal Behaviour 60: 851-855.

Hamilton, W. D. and S. P. Brown (2001). "Autumn tree colours as a handicap signal." Proceedings of the Royal Society, (B). 268: 1489-1493.

Kelber, A. (2009). From spectral information to animal colour vision: experiments and concepts. Proc. R. Soc. B. doi: 10.1098/rspb.

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

McLachlan, A. J. (2008). "Another kind of symmetry: are there adaptive benefits to the arrangement of mites on an insect host?" Ethology Ecology & Evolution 20: 257-270.

McLachlan, A. J. (2011). "Phenotypic plasticity and adaptation in a holometabolous insect, the chironomid midge." ISRN zoology.  doi:10.5402/152342.

McLachlan, A. J. and R. M. Neems (1995). Swarm based mating systems. Insect Reproduction. S. R. Leather and J. Hardie. New York, CRC Press.

Sherratt, T. N. and M. R. Forbes (2001). "Sexual differences in coloration of Coenogrionid damselflies (Odonata): a case of intraspecific aposematism?" Ecological Entomology 11: 237-240.

The evolution of social behaviour in insects

My aim here is to record some ideas about social behaviour in insects that indication an early step evolution might have taken to arrive at the levels of adaptation seen among the termites and hymenopteran societies. Parental care appears to be an essential prerequisite for the evolution of eusociality.  However, Martin Nowak and co-authors in an extraordinary paper, show that evolution of parental care can be a small step, so some of the larvae I consider here, though there is no clear evidence of parental care, may be poised on the brink of the evolution of advanced insect societies ( Nowak, et al 2010).

I start with a interesting but little known proto-termite studied by Vicky Taylor (Taylor 1981). The animal concerned is the larva of the beetle Ptinella which, like a termite, consumes dead wood in which it lives. The result is the reduction of the habitat over time and the production of a winged dispersal form, the alate. The parallel to termite society is striking. Ptinella is not alone as a pre-social insect. Another is the larva of  the rain pool dwelling chironomid midge, Chironomus imicola. Just as in Ptinella, C. imicola inhabits a ephemeral habitat which diminishes in size after rain due to evaporation. Larvae respond to the resulting crowding with the production of a giant carnivorous larva. The emerging giant adult is adapted to long distance dispersal (McLachlan and Ladle 2001).














Fig 1. An aggregation of beetle larvae on a leaf (From Costa, J. T. 2007).

A fine example of aggregation in the larvae of insects is shown in Fig.1., and more can be found in Collins Nature Guides (Gibbons 1999). The topic is explored by James Costa (Costa 2006), drawing on a wide assemblage of examples from among the arthropods. Returning to the chironomid midge, the larvae of most species inhabit the mud of more permanent inland waters. These larvae typically build tubes of mud and silk which lie horizontally on the mud surface (McLachlan and Ladle 2009). The tubes are strikingly even in their distribution.













Fig. 2. The distribution of tubes of the midge Chironomus sp at high population densities in the laboratory. From (McLachlan 1983).

Indeed, larvae will not build closer than a body length to neighbours, late arrivals appear to be physically expelled. Low density treatments in laboratory rearing trials yield poor survival rates. So, there is a hint of some sort of density dependent social interaction necessary for successful development. In this connection, the enhancement of the innate immune response under crowded conditions is relevant (Ruiz-Gonzalez, Moret et al. 2009).


In some small ponds, larval tubes are built vertically from the mud surface rather than horizontally.  This may be a response to the ecology of such pools where temperatures are high and oxygen levels low. Dissolved oxygen levels are probably highest at the water surface in contact with the air. If this is so, drawing water into tubes from near the water surface would be adaptively appropriate. An hypothesis that it is oxygen that determines tube shape is a testable hypothesis but to prevent a tube from falling over, cooperation is required from neighbours. This could be seen as a step toward  sociality (Krebs and Davies 1981) p120.  Cooperation between neighbours necessary for support is shown by larvae of  Microtendipes chorlis? The end result is a massive communal construction.
















Fig. 3. A mass of mutually supporting larval tubes of Mircotendipes chlois?, take for the bottom of a small peat pool in Scotland. The structure is somewhat collapsed due to removal from the water. The picture is c. 15 cm across.


The same kind of cooperative tube construction is shown also by the larvae of the rain pool dwelling chironomid Polypedilum vanderpalnki (Hinton 1968). In both P. vanderplanki and M. chlois? larval densities are  high making possible the construction of mutually supporting vertical tubes.Thus temporary waters such as rain pools and small peat pools may have nurtured the origin of life on earth e.g. (Weisz 1959) p53 Fig 3.11, and may  have aslo to the evolution of  eusociality.


references

Costa, J. T. (2006). The other insect societies. London, Belknap Press.

Gibbons, R. (1999). Insects of Britain & Europe. Collins Nature Guides. London, HarperCollins Publishers Ltd.

Hinton, H. E. (1968). "Reversible suspension of metabolism and the origin of life. ." Proceedings of the Royal Society, London (B). 171, 43-47.

Krebs, J. R. and N. B. Davies (1981). An Introduction to Behavioural Ecology. London, Blackwell Scientific Publications.

McLachlan, A. J. (1983). "Life-history tactics of rain-pool dwellers." Journal of Animal Ecology. 52, 545-561.

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.

McLachlan, A. J. and R. Ladle (2009). "The evolutionary ecology of detritus feeding in the larvae of freshwater Diptera." Biological Reviews. 84, 133-141.

Nowak, M. A., Tarnita, C. E. and Wilson, E. O. (2010). The evolution of eusociality. Nature. 466, 1057-1062.

Ruiz-Gonzalez, M. X., Y. Moret, et al. (2009). "Rapid induction of immune density-dependent propoholaxis in adult social insects." Biological Letters doi:10.1098/rsbl.

Taylor, V. A. (1981). The adaptive and evolutionary significance of wing polymorphism and parthenogenesis in Ptinella Motschulsly (Coleoptera: Ptillidae). Ecological Entomology. 6, 89-98.

Weisz, P. B. (1959). The Science of Biology. New York, McGraw-Hill.

autobiography

Athol John McLachlan 1939-?


I was born in Johannesburg in 1939, did my schooling in SA and after completing my undergraduate work at Wits University, moved north, with a BSc Hons in Zoology, to what was then Rhodesia. This was part of the fulfillment of a long standing interest in tropical Africa and the wilderness, sparked by a school trip to Europe. In those days, such a trip necessitated overnight stops at several places in Africa. Europe had little effect on me but I never forgot the excitement of strange and wonderful tropical Africa. In Rhodesia I took up a post as Nuffield Research Fellow at the University College of Rhodesia and Nyasaland. My PhD work was on the huge newly created Lake Kariba, on the Zambesi River. This part of Africa was one of the last truly wild places on earth, full of elephants, buffalo, leopard, crocodiles and many others. Here I studied the responses of the aquatic insect populations to the new lake habitat. This was a purely ecological project involving field work carried out at the remote Nuffield research station on the Mwenda River and it was here that I came under the influence of Arthur Cain and his Oxford research student Peter Jarman. This contact started me thinking about evolutionary ecology, in which we were quite well grounded by B. I. Balinski at Wits, but evolution did not become my major research and teaching interest until many years later.


I obtained a PhD for the Kariba work from the University of London in 1967 and after a short spell of undergraduate teaching at University College in Rhodesia, continued my northward migration to take up an appointed as lecture in Zoology at the newly created Chancellor College of the University of Malawi. This was a good move. The Zoology department at the time was chaired by Margaret Kalk, one of my teachers from Wits. In her department, teaching was informed by a strong research program which was not then, and probably is not now, the standard model in the universities of tropical Africa. My personal research was on the ecology of mud dwelling insects colonizing the newly re-filled Lake Chilwa, which had just been through one of its periodic dry phase. This work formed part of a multidisciplinary research program to study all aspects of the ecology of recovering Lake Chilwa and was an exciting time. Here my interest in transient aquatic habitats, started on the fluctuating shoreline at Lake Kariba, was reinforced and lead to a lifetime of work on tropical rain pools. These tiny habitats, in the footprints of ungulates and elephants and on rock surfaces, proved ideal for the study of temporary waters and, in contrast to giant lakes such as Kariba and Chilwa, are easily manipulated experimentally. Happily, the rain pool work necessitated return trips to Chancellor College for the rest of my working life. These visits were funded by a British Council academic link, by the Royal Society, by the Percy Sladen fund. Chancellor College generously made me welcome all those years and provide housing for my stays. All of this Africa work was suffused with a sense of  adventure.


In 1970 I won a lectureship in the Zoology Department at Newcastle University, in the UK where I remained until retirement at the age of sixty-five in 2004. Here I came under another influence - that of  my colleague Alec Panchen, which lead at last, to an active interest in evolution. I clearly recall the tipping-point at a guest lecture by the late John Maynard Smith suddenly revealing to me the evolutionary way of seeing the world. Looking back in it, I see that my life’s work falls roughly into the time in Rhodesia and Malawi when I was interested in ecology and the time in the UK where my interest focused on evolution with African rain pools forming a bridge between the two. A division of this kind coincides with work on juvenile stages in Africa and on adults in the UK. The juvenile mud dwellers are composed almost entirely of insect larvae.  These do little but eat, 24 hours a day throughout the spring and summer months. The adult part of the life-cycle is quite different, being devoted almost exclusively to mating. Hence the adult comes into the realm of sexual selection theory. The insects concerned are largely chironomid midges. Like may flies, chironomids do not need to feed as adults, spending their brief lives on the wing, fuelled essentially by energy sequestered from the larva. Mating takes place in a mating swarm with males forming the swarm, typically numbering thousands of individuals, which are sought by patrolling females. Such swarm-based mating systems are little studied and provide an excellent opportunity for original research. I have chosen to stay with chironomids all my life; ever since my undergraduate research project at Wits. Concentrating on a single taxon has left me free to change research questions at will. The alternative, chosen by some of my colleagues, is to stick to one topic and addressing it in a variety of animal species. Both approaches have advantages and drawbacks.


Looking back on all this, what do I see as my scientific achievements? In my own eyes, my most serious flaw is that I have a natural antipathy to scientific meetings, which is a bad thing carrying consequences, such as missing the opportunity of being seen by colleagues. We all really need a face to which a name can be attached. On the other hand, I think I have done some things right. First, I have been active in publishing my work, nearly all in leading peer-reviewed learned journals. I managed to resist pressures to give up research in favour of the writing of endless grant application for research students and post doctoral fellows. The ethos, well entrenched in universities, of removing experience scientists from the laboratory to become bureaucrats in this way has always seemed to me a strange thing to do to science. This fact has an important bearing on the postgraduate/supervisor relationship which, at its best, is a major source of innovation in our society. More often that not however, the supervisor is typically not directly involved in the students work. His/her seminal role is to provide the initial hypothesis to be tested and the methods required to do this. At the end of the students programme a great deal of help is usually given with interpretation and presentation of the data. But since the supervisor has not been closely involved in the collection of data, it must be taken at face value. But all data is not of equal value, a fact invisible to all but the student. I recall a senior colleague boasting, during a senior common room discussion, that he was good at seeing patterns in the data of his research students. But he was put out when I asked how he assessed the reliability of the data. This raises the spectre of how often we scientist build vast edifices on the shaky foundations of poor data.

My resistance in this matter may have something to do with my late father, a chemist who as a school boy I observed becoming office bound and as a consequence, never entering his laboratory. Fortunately, my research was not costly in monetary terms, so that I could remain active on a shoestring. My work has been of curiosity driven rather than of the problem solving type. I suspect my attitude was formed partly by a reaction to the unimaginative, strongly problem orientated fisheries research programmes to which I was exposed during the Kariba/Chilwa period.

I am a great believer in teaching informed by active personal research. Because of this I was able to bring my research attitudes and insights directly to undergraduates and research students. Coupled with constant reading to keep abreast of the wider field, this meant that I never gave the same lecture twice, not even at first year level. My teaching efforts paid off in a good response from students. In all, I published 58 original research papers and several major reviews. In 1992 I was a warded a Doctor of Science (DSc) for my research efforts by the University of London. Teaching contributions are not recognised by most universities and certainly not, in my experience, by Newcastle University.

Reflection on my school and undergraduate days reminds me of how precarious the start of ones career is. At school I was poor at chemistry and physics and struggled until a textbook on zoology was discovered by my head-master. It was at that point that I took of and was encouraged by the school to peruse my own studies on the subject. I was the only boy permitted to break bounds at will to go exploring the veld, collect snakes and make personal observations on the complex communities inhabiting abandoned termite mounds. My father insisted that I study maths, which I did not excel at but matriculate in that subject made it possible to enter Wits University which was a fine experience. Whenever time permitted I pursued my interests in natural history with my brother Ian, in the veld around Johannesburg. Without my fathers intervention at that critical time my life would have been very different.


I married twice. My first wife, Sandra, was a fellow undergraduate at Wits and shared much of my working life. My second wife, Charlotte, is an artist with strong roots on the Isle of Mull where we live after my retirement. She has a studio downs stairs and I a laboratory upstairs. 

Influential text books

My development as a biologist owns much to three outstanding, terrific books. In the order in which I discovered them they are:

Stephen Jay Gould's Ontogeny and Phylogeny, Mary Jane West-Eberhard's Developmental Plasticity and Evolution and Simon Conway Morris's Life's Solution.


references

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

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

Conway Morris, S. (2003). Life's Solution. Inevitable Humans in a Lonely Universe, Cambridge University Press, Cambridge, UK.

McLachlan & Ladle. 2009. The evolutionary ecology of detritus feeding.

McLachlan, Athol. and Ladle, Richard J. (2009). The evolutionary ecology of detritus feeding in the larvae of freshwater Diptera. Biological Reviews, 84, 133-141.



Replace:
Lines 6 – 8, p138 …… “However, pure chance…..nothing to do with natural selection “

With:
Thus, tube shape plasticity in the larvae of chironomid midges such as Chironomus plumosus seem adaptively appropriate to their location in the mud of a pond or stream. There are at least two possible explanations for the evolution of this phenomenon. First, an evolutionarily stable strategy (Maynard Smith, 1974), with a fixed proportion of the population genetically programmed to survive only if they settle in the appropriate depth of sediment. Although this kind of lottery carries greater fitness benefits than a single strategy, such a wasteful programme where a proportion of offspring always perish because they settle in the wrong place, seems unlikely to be favoured by natural selection. Second, all larvae could have inherited the ability to build their tubes and develop in whatever depth of sediment they find themselves. It is the second possibility that excites my interest here. In this case it is the environment, perceived as sediment depth, that appears to be the selective force leading to the evolution of behavioural flexibility enabling larvae to build different tubes as required. If such an  alternative proves to be the correct one, it as a pretty demonstration of  the role of environment over mutation in evolution. In the words of Lee van Valen , quoted by Stephen Gould p1....."…evolution is the control of development by ecology"

Gould, S. J. 1977. Ontogeny and Phylogeny. Harvard University Press, London.

Maynard Smith, J. 1974. The theory of games and the evolution of animal conflicts. J. Theor. Biol 47, 209-221.

GOOGLE profile June 09

Pictures from top to bottom:
The larva of a pool dwelling midge species. An adult male midge with two mite parasites. AJM in laboratory.


Name: Dr Athol John McLachlan PhD DSc.


Universities:
Wits University South Africa, 1959-1963
Univerity College of Rhodesia and Nyasaland, 1963-1969
Chancellor College, University of Malawi, 1966-1969
Newcastle Univeristy UK, 1970-2004

Academic affiliation: Newcastle University (retired 2004).


Teaching:

For about fifty years I taught at first, second and final stages with an emphasis on invertebrate biology, ecology, freshwater biology and the evolution of behaviour, the last being my special interest subject taught at advanced level.


Research:

My primary research interest is the ecology and evolutionary biology of holometabolous insects, particularly those such as chironomid midges with a may-fly like life cycle. Early work in tropical Africa provides a background to the ecology of these midges and illustrates the range of habitats in which these animals are found; some of them extreme.
Among chironomid midges the larva is the feeding/energy acquisition stage. Larvae are characteristically detritus feeders which present some interesting question about co-evolution with decomposer micro-organisms. The adult male is concerned virtually exclusively with mating. Hence that part of the life-cycle falls into the realm of sexual selection. Males form mating swarms numbering thousands of individual through with patrolling females fly to acquire a mate. Success for the male appears to hinge on aerobatic ability, which favours the smaller male.

Phenotypic flexibility in mating behaviour, in the face of a large burden of parasites, has been the focus of my interest in the mating system.

Some key references are listed below.

Selected Publications:

1) McLachlan, A. J. (1974). Development of some lake ecosystems in Tropical Africa with special reference to the invertebrates. Biological Reviews, 49: 365-97.

2) 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.

3) McLachlan, A. J. and Ladle, R. (2009). The evolutionary ecology of detritus feeding in the larvae of freshwater Diptera. Biological Reviews, 84: 133-141.

4) McLachlan, A. J. and Ladle, R. J. (2011). Barriers to Adaptive Reasoning in Community Ecology. Biological Reviews. 86: 543-548.