The Mating Behaviour of a Swarm Forming Insect.

This essay supersedes and expands on earlier attempts to understand swarm based mating behaviour of chironomid midges (McLachlan, 2012a, 2014a, 2018; McLachlan and Neems, 1995; swarm based mating systems 2012b). Chironomids (Chironomidae), are not the dreaded scottish midge (Ceratopogonidae). I focus on the chironomid phenotype, and mostly on behaviour, i.e. response by movement to environmental stimuli. Behaviour is taken to include phenotype limited behaviours as in the size limited behaviours of male midges described below. Unravelling the complexities has proved tricky. There appear to be multiple mating behaviours within a single species but for years I had been trying to distil my observations down to a single mating behaviour. This was a fruitless activity. Over lunch in the senior common room my friend and colleague Max Hammerton asked why it had to be only one behaviour. This led to the thought that it could perhaps involve many alternative behaviours necessary to achieve mating under different environmental conditions. How stupid of me not to have thought of this earlier. Even then I could not see how multiple behaviours would work within a single species. Mary Jane West Eberhard (West-Eberhard, 2003), has the answer. In a inspirational book she shows how alternative phenotypes governed by environmental triggered switch points are widespread among both animals and plants. I hope to show that such a condition dependent approach overcomes many of the obstacles to understanding chironomid mating behaviour. Because I have more data on it than other species, I adopt Paratrichocladius rufiventris, as the main test species for the chironomidae in general but I draw in findings from other species from time to time, e.g. (McLachlan and Allen, 1987; McLachlan and Neems, 1989).

My interest in chironomid midges stems from studies of the larval stages which often dominate freshwater habitats (McLachlan and Ladle, 2009), p.136. Specifically it is those chironomid larvae inhabiting ephemeral waters such as the margins of lakes, rain pools, and upland rivers where   adaptation to the unpredictability of the habitat has attracted my attention (McLachlan, 1974a, 1974b; A. J.  McLachlan, 2014; McLachlan and Ladle, 2001; Walentowicz and McLachlan, 1980). By contrast to work on the aquatic larvae, the adult phase of the life cycle is an aspect of chironomid biology outside the ken of mainstream freshwater ecology. A study of adults requires a fundamental shift from feeding biology to mating biology (Andersson, 1994). Indeed the biology of mating introduces an entirely different world. To start at the beginning - like all sexually reproducing species, to produce a fresh generation of aquatic larvae an adult chironomid must find an individual of a very specific kind. Not only must it be of the right species but it must be of the opposite sex. And finding the appropriate species and sex is not the end of the matter as choice among mates is a fitness priority. Adult chironomids are active in the evenings during early spring and can be seen in huge swarms over landmarks such as tree tops (Fig. 1).

  Fig.1. A swarm of male midges (Chironomus plumosus), over a tree top on a spring evening. From (McLachlan, 2010).  

 Swarms are composed almost entirely of males, usually of a single species, swarming to attract patrolling females (McLachlan and Neems, 1995). A question immediately arises – how do males find each other to form swarms in the first place? Reflect for a moment. After emerging from water, these tiny flies will be scattered by wind and their own flight over many miles. This is like attempting to find another human in the Sahara desert. The solution has been for males to aggregate over a landmark. Here sight appears to be the primary sense, but the sound of high speed wing beats like the whine of mosquito help too. The elaborate antennae of the male (Fig.2.), is the sense organ responsible for detecting wing beat sound. This simplifies the task for patrolling females because the swarms emit a conspicuous auditory signal.

Fig.2. Antennae of a typical chironomid midge showing male antennae (b) and female antennae (d). (Modified after (Freeman, 1955), with permission).

So we have reached the point where male swarms, all of the same species, are present over a landmark. Now to bring the females into the picture. I once succeeded in a striking demonstration of the role of the wing beat sound of a female entering a swarm of males. Borrowing a set of tuning forks from our Physics department, I struck each fork in turn and introduced it into a swarm. Nothing happened until one fork in particular elicited a striking response. The whole male swarm of many thousand males immediately aggregated closely around the fork. I take this particular tuning fork to represent a female. So there is no doubt about the role of female sound. It is worth recording that the same observation involving male mosquitoes aggregating around a buzzing light was made by Hiram Maxim, the inventor of the machine gun, more that 140 years ago (Roth, Roth, & Eisner, 1966). But there is more to it than the response to sound among males and between males and females. When  a female finds and enters an appropriate swarm she searches – not just for wing beat sound of males but for harmonics that match the sound of her own wing beats (McLachlan, 2012b). The use of harmonics is a sophisticated adaptation indeed. Even then there can be mistakes. For example, homosexual pairing is by no means uncommon (McLachlan, 2011; Sales et al., 2017).

As I have already hinted, selection theory predicts that individuals are highly selective in choice of the ‘best’ possible mate among those available. What is meant by best mate is an intriguing question and it is here that research on the mating behaviour of animals has been directed over the last few decades (Thornhill and Alcock, 1983). We have already seen that individuals, both male and female in a swarm, are searching for harmonics of wing beat sound. So, mate choice depends neither  on the female alone as is normally the case, nor does it depend on the male as is sometimes the case, but rather may be mutual with both sexes collaborating in choice. Chironomid swarms are lek base mating systems better known among birds such as grouse (Davies, Krebs, and West, 2012). Leks involve male animals coming together in a definite place such as a patch of ground or treetop year after year. In a lek, males provide females with nothing but sperm - no resources such as shelter or food are exchanges for sex. After mating females leave the swarm to oviposit in nearby water. Successful males by contrast, can potentially return to the swarm and achieve further matings. With chironomids, it has proved difficult to identify the ‘mating system’, essentially comprising of the alternatives - multiple male matings (polygyny) or multiple matings by females (polyandry). I have never been able to distinguish between the two for chironomids but J. A. Downes (Downes, 1969), in a clever manipulation of Chironomus plumosus, swarms found polygamy. The Downes findings appear to be contradict those of Goran Arnqvist (Arnqvist, 1998). Thus this important aspect seems not yet to be resolved but may be explained, as is much else, by environmental switches between alternative tactics within a single strategy (see below).

There is more: size is not a continuous variable among males. Instead size frequency distribution shows three discrete size classes caalled α, β and γ, with α containing the largest males and γ the smallest (A. J. McLachlan, 2014b)(Fig.3).

Fig.3. Approximate relative sizes of α and γ male chironomids. The β males are intermediate. Scale c. 6x.

 Discontinuous size classes such as these carry with them quite separate phenotype limited mating tactics. The idea of phenotype limited tactics is not original but follows the findings of Shuster and Wade in a marine isopod (Shuster and Wade, 1991). The first hint of the existence to size classes among chironomids was obtained by taking net sweeps samples from swarms and separately from the grass under the swarm. These samples showed the size of male in the swarm and in the grass to be quite different with distinctly smaller males in the grass (McLachlan and Neems, 1989). Interestingly, we found that females attracted to the swarm rest in the grass before entering the swarm and must encounter the γ males there. The possibility exists therefore, that the smallest males never enter the swarm but mate on the ground. By contrast, swarm samples reveal β males to predominate. These, it appears, depend on aerobatics and endurance to obtain a mate (Crompton, Thomason, and McLachlan, 2003), cued by harmonics. Finally, α males, also to be found in the swarm reveal something unexpected (McLachlan, MacLeod, and Neems, 2018). At least to the human observer, (α) males look very like a common predator of the swarm – males of the empid fly Empis stercorea.  Male empids enter the swarm to capture a midge as a nuptial gift for their own females. The strong resemblance between α males and empids led to the idea that mimicry may be involved. What I mean is that α males may gain in fitness by mimicking their predator and thereby decrease the chance of a fatal encounter - and at the same time increase the time spent in the swarm and the increased probability of mating. An hypothesis of mimicry could be strengthened by measuring wing beat sound in both predator and prey. Regrettably I have not done this but when it is done I predict that the wing beat sound of large chironomids and empids would be closely similar. So there are three size determined mating tactics among males. Fitness payoff to the three can be calculated with tactics played off against each other in an ESS (Maynard Smith, 1982).The three distinct tactics might be determined genetically with two alleles in a simple Mendelian model. Assuming simple dominance the two alleles in the game become AA; aa; and the heterozygote Aa. The F1 generation would occur in the Hardy - Weinberg equilibrium with gene frequencies of 1AA; 2Aa; 1aa. Of course these genes would only be expressed in males. In principle it should be easy to verify a gene determined hypotheses by counting the proportions of the three morphs is a species population. In practice this may prove very difficult, if not impossible. Furthermore, size limited male behaviours could well be environmentally induced, in which case fitness payoff to the three tactics need not be equal and proportions in the population cannot be predicted. My colleague John Lazarus has shown how three size limited phenotypes might have evolved under selective pressures from the environment (i.e. condition determined body size), as apposed to genetically determined phenotypes, in a rock – scissor – paper game built on the principles of an ESS (A. J. McLachlan, 2014a).

I come now to the second example of environmental switch points, i.e. the effect of predators and of parasites. The body size effects discussed above, were shown in the male. By contrast, it is the female that shows an adaptive response to parasites and to predators.

Predators

A general problem for animals displaying to attract mates is that others are out there listening or looking for signals. For chironomids, a common predator of mating swarms is the empid fly Empis stercorea, (McLachlan, Ladle, and Crompton, 2003). Their presence acts as an environmental switch to quite a different mating system where harmonics for wing beat sound is no longer important. Instead the mating system becomes one driven by coercion, with the male pursuing reluctant females who mistake them for a predator. So the role of coercion need not be abandoned after all (McLachlan, A. J., 2012b).

Parasites

Two parasites commonly infect P. rufiventris during mating; the mite Unionicola  ypsilophora and the nematode worm Gastromermis rosea (Fig.4).

Fig. 4. Midges infected by parasites. Male with two mites (a). Female with about 7 mites (b).  Female  (c), with a worm (g), bursting out of the abdomen, in the act of  returning  to water to close its life cycle. Scale line 0.5mm.Modified after (McLachlan, 2012a).

Male chironomids typically carry one or two mites placed mid-ventral between thorax and abdomen. Females by contrast, bear up to 23 mites on the ventral surface of the thorax (McLachlan, 1999). Samples of mating pairs reveal infected females to predominate in these pairs, indicating significantly improved mating success for mite infected females. This is a counterintuitive finding. There are at least two hypotheses to account for such a strange outcome. First, since mating depends on aerobatics, females baring mites can be expected to be compromised in flight due to biomechanical drag effects – and indeed there is good evidence that this is so (McLachlan et al., 2003). Second, mites may be revealing a hitherto hidden sexual preference, (Ryan, 2017), pp148 – 167, in this case for  the colour red. Hidden sexual preferences are an intriguing but often overlooked possibility and here imply the existence in midges of colour vision for red. Colour vision for red in a fly is theoretically unexpected (McLachlan, 2009). In the case of P. rufiventris, as the species name indicates (rufiventris), this species has a red tinge to the ventral surface which may act as a sexual display ornament, enhanced by the presence of these bright red mites (Fig 5.). There is yet another aspect of the mite mediated sexual selection. During mating mites transfer from male to female – so mites might be considered a sexual transmitted disease.

Fig.5. Female P.rufiventris with several bright red mites on the ventral surface of abdomen.

As both parasite and host gain by the association, the relationship between mite and host should properly be considered a case of mutualism rather than parasitism. I say this because the host benefits by an improved mating success (fitness). At the same time after mating, the female midge departs to water to lay her eggs, providing the mite with the opportunity to leave the female midge and return to an aquatic phase in water. There appears to be nothing gained by mites on the male except the chance of transferring to a female. The relationship between mites and midges nicely illustrates my central theme; condition dependent switches between alternative phenotype. Mating is no simple matter.

Turning to the second parasite, the worm: here is an intriguing twist to the sexual selection story. Unlike mites, worms are not harmless but render any infected female sterile. Thus an infected female and any male mating with her achieve zero fitness. But as females rarely carry both worm and mite, by mating with a mite baring female the male avoids the cost of a complete loss of fitness. So midges are at the centre of a complex, mutual benefit co-adapted mite – midge – worm interaction (McLachlan, 2006). Such close reciprocal interactions between ‘host’ and ‘parasite’ calls to mind the extended phenotype concept of Richard Dawkins (Dawkins, 1982), p21.

Summary   

This essay attempts to bring together all that is known about the lek based mating system of the chironomid midge. The attempt turns on the realisation that behaviour of a single species is highly plastic and can change adaptively depending on the environment. I have been able to identify three condition determined switch points between ‘normal’ mating behaviours and adaptive phenotypic changes in response to environmental effects. Environmental effects include the response to parasites and to predators in the female midge and to body size in the male midge. The answer has not come easily. I took the chironomid midge Paratrichocladius rufiventris, a common non-biting midge, as a case study, not because it is an especially appropriate choice. Indeed, progress in unravelling mating behaviours of animals has depended largely on the careful choice of study subject against which to test hypotheses. Studies of the dung fly (Scatophaga), Parker (Parker, 1984), and of great tits by Lack (Lack, 1966), illustrate the point. The Sydney Brenner of Caenorhabditis elegans fame expresses the point..."choosing the right organism to work on ....was as important as choosing the right problem to work on (Brenner, 2019). Chironomids have proved a rather difficult subject, but a challenge to me following years studying the larval stages. I offer a largely theoretical framework to promote understanding of the adaptive functioning of the behaviour of what I take to be a typical chironomid midge. I point up ideas that are still in need of testing and how some might be tested. The main point to emerge, I hope, is the importance of  bringing adaptive reasoning more fully into an ecological framework. 

References

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

Arnqvist, G. (1998). Comparative Evidence for the Evolution of Genitalia by Sexual Selection. Nature, 393, 784-786.
Brenner, S.  (2019). A lucky accident. Wits Review, 41. 38-41.

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.

Davies, N. B., Krebs, J. R., and West, S. A. (2012). An Introduction to Behavioural Ecology. (4 ed.). Oxford: Wiley-Blackwell.

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

Downes, J. A. (1969). The swarming and mating flight of Diptera. Annual Review of Entomology 14, 171-297.

Freeman, P. (1955). A study of the Chironomidae (Diptera) of Africa South of the Sahara. . The Bulletin of the British Museum (Natural History), 4, 1-69.

Lack, D. (1966). Population Studies of Birds. Oxford: Clarendon Press.

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

McLachlan, A. J. (1974a). Development of Some Lake Ecosystems in Tropical Africa, with Special Refrence to the Invertebrates. Biological Reviews, 49, 365-397.

McLachlan, A. J. (1974b). Recovery of the Mud Substrate and its Associated Fauna Following a Dry Phase in a Tropical Lake. . Limnology and Oceanography, 10, 74 - 83.

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 & Evolution 18, 233-239.

McLachlan, A. J. (2009). Do Flies See Red?, http://www.google.co.uk/atholmclachlan.blogspot.co.uk.

McLachlan, A. J. (2010). Fluctuating Asymmetry in Flies, What Does it  Mean? Symmetry, 2, 1099-1107

McLachlan, A. J. (2011). Homosexual Pairing within a Swarm-Based Mating System: The Case of the Chironomid Midge. Psyche, ID 854820, 5 pages.

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

McLachlan, A. J. (2012b). SWARM BASED MATING SYSTEMS. 13/03/2012. http://www.atholmclachlan.blogspot.com/.

McLachlan, A. J. (2014). Blaxter Lough, http://www.google.co.uk/atholmclachlan.blogspot.co.uk.

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

McLachlan, A. J. (2014b). Phenotype Limited Mating Behaviour., http://www.google.co.uk/atholmclachlan.blogspot.co.uk.

McLachlan, A. J. (2018). http://www.google.co.uk/atholmclachlan.blogspot.co.uk.

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

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.

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

McLachlan, A. J., Ladle, R., and Crompton, B. (2003). Predator-prey interactions on the wing: aerobatics and body size among dance flies and midges. Animal Behaviour, 66, 911-915.

McLachlan, A. J., MacLeod, K. J., and Neems, R. M. (2018). SSD revised. Sexual Size Dimorphism in the chironomid midge: A Sheep in Wolf's Clothing. , http://www.google.co.uk/atholmclachlan.blogspot.co.uk.

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

McLachlan, A. J., and Neems, R. M. (1995). Swarm based mating systems. In S. R. Leather & J. Hardie (Eds.), Insect Reproduction. Neww Yourk:CRC  Press
 McLachlan, A.J. 13/03/2012. http://google.co.uk/atholmclachlan.blogspot.co.uk.                                  Parker, G. A. (1984). Evolutionarily stable strategies. In J. R. Krebs & N. B. Davies (Eds.), Behavioural Ecology: An Evolutionary Approach. Oxford: Blackwell.

Roth, M., Roth, L. M., and Eisner, T. E. (1966). The allure of the female mosquito. Natural History, 75, 27.

Ryan, M. J. (2017). A Taste for the Beautiful. Princeton, New Jersey.: Princeton University Press.

Sales, K., Trent, G., Gardner, J., Lumley, A. J., Vasudeva, R., Michalczyk, L., et al. (2017). Experimental Evolution with an Insect Model reveals that Male Homosexual Behaviour ocours due to Inaccurate Mate Choice. . Animal Behaviour, 139, 51- 59.

Shuster, S. M., and Wade, M. J. (1991). Equal mating success among male reproductive strategies in a marine isopod. Nature, 350, 608-610.

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

Walentowicz, A. T., and McLachlan, A. J. (Eds.). (1980). Chironomids and Particles: a field experiment with peat in an upland stream. Oxford: Permagon Press.

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