Swarm Based Mating Systems

For many years I have been grappling with the elusive mating system of the common chironomid midge. This effort has been based, at least in part, on observations of swarms in the wild. The swarm is essentially a lek with aggregations of males, often numbering many thousand individuals, keeping station over a landmark to attract patrolling females. Females enter the swarm and emerge after a short time with a mate (Downes 1969; McLachlan and Neems 1995). Mosquitoes share this mating system with chironomids and others and more than 200 years ago, Hiram Maxwell, the inventor to the machine-gun showed, in a series of careful observations on mosquitoes, that paring within the swarm hinges on the sound emitted by the wing-beat of the individuals of both sexes, cited by (Roth, Roth et al. 1966). I had lost sight of Maxwell’s work but recently rediscovered the role of sound in swarm based mating systems in a rich literature (Stumpner and van Heelversin 2001; Bailey 2003). Like that of Maxwell, this work principally concerns disease carrying mosquitoes and it has been known for many years that it is the Johnston’s organ at the base of the antenna that responds to vibrations set up in the antenna itself (Johnston, C. 1855).

I had previously concluded (McLachlan 2011) p3, para 4, as follows: …”wing beat sound, I suggest, is a fallible cue..”. This conclusion skirts close to the answer but misses the point, elegantly demonstrated by Gabriella Gibson and others (Ng'Habi, Huho et al. 2008; Cator, Arthur et al. 2009; Cator, Ng'habi et al. 2010; Gibson, Warren et al. 2010), that wing beat sound varies because individuals of both sexes are searching for harmonics, which if achieved, signals the presence of a suitable mate. Wing beat sound is related to body size (Cator, Ng'habi et al. 2010), and body size in turn generally reflects genetical quality in animals (Krebs and Davies 1981), thus facilitating mate choice within a sexual selection landscape. It is difficult to escape the conclusion that among swarm based mating systems, it is not the female that chooses a mate, as is the common situation in leks (Andersson 1994). Nor does the male make the choice (Andersson 1994; Clutton-Brock 2009). Rather, both sexes appear equally responsible for choice. It seems likely that mutual mate choice is typical of swarm based mating systems and even more generally among tiny animals such as the insects where finding a mate might be the major selective pressure leading to the evolution of this mating system. Mutual mate choice seen in a very different of insect, the fire-fly (a beetle) (Thornhill and Alcock 1983), pp156-159, lends credence to this conjecture. The speed with which a mating can be achieved in the face of danger from predators (Moller, Christiansen et al. 2011), such as empids could be a contributing factor.

Read in the context of (McLachlan and Neems 1995; McLachlan 2011), all the steps leading to mating within such leks fall into place at last. First there is the gathering of males over landmarks using both visual and auditory cues, the latter involving the elaborate antennae of the male. Next, the male swarm is located by patrolling females, again using both visual and auditory cues. The female antenna is less elaborate but is presumably sufficiently sensitive to detect the sound emitted by a large aggregation of males. Finally, both sexes deliberately vary wing beat frequency searching for harmonics which lead to mating.

These conclusions call into question my earlier suggestion that the mating system is essentially driven by sexual coercion, with aggressive males pursuing fleeing females (McLachlan, Pike et al. 2008) p.267 para.2 and (McLachlan 2011), Conclusions lines 5,6. If coercion is not part of the story, how exactly is pairing achieved? I suggest that the male is the active part of a pairing event with his superior antennae and greater agility (McLachlan 1986; McLachlan, Pike et al. 2008), but that the female does not flee. Rather she offers herself and awaits capture. Therefore, in the light of the evidence currently available, I reluctantly abandon the idea of a mating system driven by coercion. It seemed to explain so much (McLachlan, Pike et al. 2008), p267, but is not good enough. This change in emphasis has no baring on understanding the role of the key predator of male midges, the empid fly (McLachlan, Ladle et al. 2003). It is worth noting though, that by contrast with the performance of the male midge in capturing mates, this predator, possible operating entirely on sight, has a dismal performance. But, since male midges are so plentiful, the empid may not need to be any more efficient.

Some further comment is required on the term ‘choice’. This term is central to sexual selection theory but is an anthropomorphism which worries some biologists. Here I sidestep this concern by adopting the attitude of West-Eberhard (West-Eberhard 2003) pp34 – 35), where choice is defined as taking place when ... “an organism responds differentially to different stimuli”.

References

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

Bailey, W. J. (2003). "Insect duets: Underlying Mechanisms and their Evolution." Physiological Entomology 28: 157-174.

Cator, L. J., B. J. Arthur, et al. (2009). "Harmonic Convergence in the Love Songs of the Denque Vector Mosquito." Science 323: 1077-1079.

Cator, L. J., K. R. Ng'habi, et al. (2010). "Sizing up a mate: variation in production and response to acoustic signals in Anopheles gambiae." Behavioural Ecology 21: 1033-1039.

Clutton-Brock, T. (2009). "Sexual Selection in Females." Animal Behaviour 77: 3-11.

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

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.

Jonaston, C. (1855). "Auditory apparatus of the Culex mosquito". Quarterly Journal of Microscopic Science. 3, 97-102.

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

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

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

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

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

Moller, A. P., S. Christiansen, et al. (2011). "Sexual signals, risk of predation and escape behaviour." Behavioural Ecology doi:10.1093/beheco/arr046: 800-807.

Ng'Habi, K. R., B. J. Huho, et al. (2008). "Sexual Selection in Mosquito Swarms: May the Best Man Lose?

." Animal Behaviour 76: 105-112.

Roth, M., L. M. Roth, et al. (1966). "The allure of the female mosquito." Natural History 75: 27.

Stumpner, A. and D. van Heelversin (2001). "Evolution and Function of Auditory Systems in Insects. ." Naturwissenshaften 88: 159-170.

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.

Life in the Puddle

Darwin’s Warm Little Pond

The following might have been a better start to our 2001 paper (Athol McLachlan and Richard Ladle 2001. Life in the puddle: behavioural and life-cycle adaptation in the Diptera of tropical rain pools Biol. Rev., 76, 377-388).

ABSTRACT

For over one hundred years Charles Darwin’s “warm little pond” has been at the centre of conjecture about the origin of life. It is precisely such ponds that form the subject of the present article. These tropical ponds have some extraordinary properties. Among them is the fact that they harbour exceedingly high densities of single species of midge larvae, each carrying the clear stamp of adaptation to the durational characteristics of their pond. Exceptional too, is the property which derives from their occupying depressions on rock surfaces, of being spatially consistent over millions of years. In what follows we attempt to draw out these properties and set them against those of other very transient habitats.

INTRODUCTION

Puddles of rain water on the surfaces of rock exposures are a little known but very common habitat for freshwater-dwelling animals. They are also typical of Charles Darwin’s “warm little pond” (Conway Morris, S. 2003, p53, 64, Dawkins, R. 2009, p417, 419). In Africa, these are inhabited by the larvae of two taxa of fly unique to these pools. One of these includes species able to survive dry periods in situ; the other includes species that must reach adulthood and migrate to survive periods when the pool is dry. Hence, the opportunity exists for a comparative study of adaptation among these species. Since puddles are small, our principal method in the study of adaptation has been the experimental manipulation of puddles and their faunas in the wild. Using this method we were able to identify the spatial consistence of pools and their unpredictable duration during the rainy season as the main selective pressures shaping adaptation. Adaptations include diapause and adaptive adjustments of the life cycle. It is the second of these that provides the focus of our interest here. There are many kinds of freshwater habitat ……run on to original version (Introduction line 1).

Refrences

Darwin, C. 1871. The Descent of Man and Selection in Relation to Sex. J. Murray, London.

Conway Morris, S, 2003. Life’s Solutions: Inevitable Humans in a Lonely Universe. Cambridge University Press, Cambridge, UK.

Dawkins, R. 2009. The Greatest Show on Earth. Bantam Press, London.

My Published Work in the 'learned literature' 1965-2011

Theses, Published Symposium Proceedings and Reports

1965. Ecology of the bottom fauna of Lake Kariba, pp. 58- 59. In: LKFRI Kariba Research Symposium Proceedings.

1968. A study of the bottom fauna of Lake Kariba. PhD thesis, University of London. 348 pp.

1969. Aspects of the ecology of the bottom fauna of Lake Chilwa, pp. 27-29. In: IBP Symposium, Malawi Proceedings.

1969. A study of the bottom fauna of Lake Kariba, pp. 13-14. In: Nuffield Lake Kariba Research Sation Report, 1962-68. University College of Rhodesia Press, Salisbury.

1974. The development of chironomid communities in a new temperate impoundment. Ent.Tidskr., 95 (Suppl.): 162-71.

1978. Interactions between freshwater animals and micro-organisms. Ann.appl.Biol., 89: 162-65.

1980. Chironomids and particles: Micro-organisms and chironomid distribution in a peaty upland river. In: D A Murray (ed) Chironomidae: Ecology, Systematics, Cytology and Physiology. pp. 171-77. Pergamon Press, Oxford (with R J Toscano).

1980. Chironomids and particles: A field experiment with peat in an upland stream. In: D A Murray (ed) Chironomidae: Ecology, Systematics, Cytology and Physiology. pp. 179-85. Pergamon Press, Oxford (with A T Walentowicz).

1981.Biological consequences of fluctuations in lake level. In: J M Kapetsky (ed) Seminar on river basin development (IFA Technical report No 8) pp. 225-31.

Peer reviewed original research papers

1. McLachlan AJ (1969). Notes on some larval and pupal chironomids (Diptera) from Lake Kariba,Rhodesia J.Nat.Hist., 3: 261- 93.

2. McLachlan AJ (1969). Substrqate preferences and invasion behaviour exhibited by larvae of Nilodorum brevibucca Freeman (Chironomidae) under experimental conditions. Hydrobiologia, 33: 237-249.

3. McLachlan AJ (1969). The effect of aquatic macrophytes on the variety and abundance of benthic fauna in a newly created lake in the tropics (Lake Kariba). Arch. Hydrobiologia, 66: 212-31.

4. McLachlan AJ and McLachlan SM (1969). The bottom fauna and sediments in a drying place of a saline African lake (L. Chilwa, Malawi). Hydrobiologia, 34: 401-13.

5. McLachlan AJ (1970). Some effects of annual fluctuations in water level on the larval chironomid communities of Lake Kariba. J.Anim.Ecol., 39: 79-90.

6. McLachlan AJ (1970). Submerged trees as a substrate for benthic fauna in the recently created Lake Kariba (Central Africa). J.Appl.Ecol., 7: 253-66.

7. McLachlan AJ (1971). Some immature stages of the subgenus Chironomus (Meigen) (Diptera: Chironomidae) from Malawi, Central Africa. J.Ent.(B), 40: 173-78.

8. McLachlan AJ and McLachlan SM (1971). Benthic fauna and sediments in the newly created Lake Kariba (Central Africa). Ecology, 52: 800-09.

9. McLachlan AJ, Morgan PR, Howard-Willians C, McLachlan SM and Bourn D (1972). Aspects of the recovery of a saline African lake following a dry period. Arch.Hydrobiol., 70: 325-40.

10. McLachlan AJ (1974). Recovery of the mud substrate and its associated fauna following a dry phase in a tropical lake. Limnol.Oceanogr., 19: 74-83.

11. McLachlan AJ (1975). The role of aquatic macrophytes in the recovery of the benthic fauna of a tropical lake after a dry phase. Limnol. Oceanogr., 20: 54-63.

12 McLachlan AJ and McLachlan SM (1975). The physical environment and bottom fauna of a bog lake. Arch.Hydrobiol., 76: 198-217.

13. McLachlan AJ (1976). Factors restricting the range of Glyptotendipes paripes Edwards (Diptera: Chironomidae) in a bog lake. J.Anim.Ecol., 45: 105-113.

14. McLachlan AJ amd McLachlan SM (1976). Development of the mud habitat during the filling of two new lakes. Freshwat.Biol., 6: 59-67.

15. Mclachlan AJ (1976). Variation in ‘gill’ size in a larva of the African midge Chironomus transvaalensis Keiffer. Limnol.Soc.Stn.Afr., 2: 55- 56.

16. McLachlan AJ and Cantrell MA (1976). Sediment development and its influence on the distribution and tube structure of Chironomus plumosus L. (Chironomidae: Diptera) in a new impoundment. Freshwat.Biol., 6: 437-43.

17. McLachlan AJ (1977). Some effects of tube shape on the feeding of Chironomus plumosus L. (Diptera: Chironomidae). J.Anim.Ecol. 46: 139-46.

18. McLachlan AJ (1977). The changing role of terrestrial and autochthonous organic matter in newly flooded lakes. Hydrobiologia, 54: 215- 17.

19. McLachlan AJ (1977). Density and distribution in laboratory populations of midge larvae (Chironomidae: Diptera). Hydrobiologia, 55: 195- 99.

20. Cantrell MA and McLachlan AJ (1977). Competition and chironomid distribution patterns in a newly flooded lake. Oikos, 29: 429-33.

21. McLachlan AJ and Dickinson CH (1977) Micro-organisms as a factor in the distribution of Chironomus lugubris in a bog lake. Archiv fur Hyrobiology, 80: 133-146.

22. Brennan A, McLachlan AJ & Wotton RS (1978). Particulate material and midge larvae (Chironomidae:Diptera) in an upland river. Hydrobiologia, 59: 67-73.

23. McLachlan AJ, Brennan A andWotton RS (1978). Particle size and chironomid (Diptera) food in an upland river. Oikos, 31: 247-52.

24. Baker A and McLachlan AJ (1979). Food preferences of Tanypodinae larvae (Diptera: Chironomidae). Hydrobiologia, 62: 283-88.

25. Brennan A and McLachlan AJ (1979). Tubes and tube building in a lotic chironomid (Dipteran) community. Hydrobiologia, 67: 173-78.

26. McLachlan AJ, Pearce LJ and Smith JA (1979). Feeding interactions and cycling of peat in a bog lake. J.Anim.Ecol., 48: 851-61.

27. Brennan A and McLachlan AJ (1980). Species of Eukieffreriella Theinemann (Diptera: Chironomidae) from a northern river, with some notes on larval dwellings. Ent.Mon.Mag.16: 109-11.

28. McLachlan AJ and Cantrell MA (1980). Survival strategies in tropical rain-pools. Oecologia Berl., 47: 344-51.

29. McLachlan AJ (1981). Food sources and foraging tactics in tropical rain-pools. Z.J.Linn.Soc. 75: 267-277.

30. McLachlan AJ (1981). Interactions between insect larvae and tadpoles in tropical rain-pools. Ecol.Ent., 6: 175-82.

31. Cantrell MA and McLachlan AJ (1982). Habitat duration and dipteran larvae in tropical rain-pools. Oikos, 38: 343-48.

32. McLachlan AJ (1983). Life history tactics of rain-pool dwellers. J.Anim.Ecol. 52: 545-61.

33. McLachlan AJ (1983). Habitat distribution and body size in rain-pool dwellers. Zool.J.Linn.Soc., 79: 399-407.

34. McLachlan AJ (1985). The relationship between habitat predictability and wing length in midges (Chironomidae). Oikos, 44: 391-97.

35. McLachlan AJ (1985). What determines the species present in a rain-pool? Oikos, 45: 1-7.

36. Osborne PL andMcLachlan AJ (1985). The effect of tadpoles on algal growth in temporary, rain- filled rock pools. Freshwat.Biol., 15: 77-87.

37. McLachlan AJ (1986). Sexual dimorphism in midges; strategies for flight in the rain-pool dweller Chironomus imicola (Diptera: Chironomidae). J.Anim.Ecol., 55: 261-67.

38. Burtt ET, Perry RJO and McLachlan AJ (1986). Feeding and sexual dimorphism in adult midges (Diptera:Chironomidae). Holarctic Ecology, 9: 27-32.

39. McLachlan AJ (1986). Survival of the smallest: advantages and costs of small size in flying animals. Ecol.Ent.,11: 237-40.

40. McLachlan AJ and Allen DA (1987). Male mating success in Diptera: advantages of small size. Oikos, 48: 11-14

41. McLachlan AJ (1988). Refugia and habitat partitioning among midges (Diptera: Chironomidae) in rain-pools. Ecol.Ent., 13: 185-93.

42. McLachlan AJ and Neems RM (1989). An alternative mating system in small male insects. Ecol.Ent., 14: 85-91.

43. McLachlan AJ and Yonow T (1989). Reproductive strategies in rain-pool dwellers and the model freshwater insect. Hydrobiologia, 171: 223-230.

44. Patterson JW and McLachlan AJ (1989). Larval habitat duration and size at metamorphosis in frogs. Hydrobiologia, 171: 121- 126.

45. Neems RM, McLachlan AJ and Chambers R (1990). Body size and lifetime mating success of male midges (Diptera:Chironomidae). Animal Behaviour., 40: 648-652.

46. Jackson JM and McLachlan AJ (1991). Rain-pools on peat moorland as island habitats for midge larvae. Hydrobiologia, 209: 59-67.

47. Neems RM, Lazarus J and McLachlan AJ (1992). Swarming behaviour in male chironomid midges; a cost-benefit analysis. Behavioural Ecology, 3: 285-290.

48. McLachlan AJ and Neems RM (1993). Are females selected against in ephemeral habitats? The case of a holometabolous insect (Chironomus pulcher). Oecologia, 94: 83-86.

49. McLachlan AJ and Cant M (1995). Small males are more symmetrical: mating success in the midge Chironomus plumosus (Diptera:Chironomidae). Animal Behaviour, 50: 841-846.

50. McLachlan AJ and Neems RM (1996). Is flight architecture determined by physical constraints or by natural selection: the case of the midge Chironomus plumosus. Journal of Zoology (London), 240: 301-308.

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

52. Neems RM, Lazarus J and McLachlan AJ (1998). Lifetime reproductive success in a swarming midge: Trade-offs and stabilizing selection for male body size. Behavioural Ecology, 9: 249-256.

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

54. McLachlan AJ, Ladle R and Bleay C (1999). Is infestation the result of adaptive choice behaviour by the parasite? A study of mites and midges. Animal Behaviour, 58: 615-620.

55. McLachlan AJ, 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.

56. Crompton B, Thomason J and McLachlan A (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.

57. McLachlan AJ (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.

58. McLachlan AJ, Pike, TW and Thomason JC (2008). Another kind of symmetry: are there adaptive benefits to the arrangement of mites on an insect host? Ethology Ecology and Evolution, 20: 257-270.

Reviews, Debates and Book Chapters

1. McLachlan AJ (1969). Some effects of water level fluctuation on the benthic fauna of two central African lakes. Limnol.Soc.S.Afr.Newsl., 13: 58-63.

2. McLachlan AJ (1970). The bottom fauna: distribution patterns and invasion behaviour. pp. 34-35. In: Kalk, M (ed) Decline and recovery of a saline Lake. Lake Chilwa Coordinated Research Report, 1966- 70. Government Printer, Zomba (with S M McLachlan).

3. McLachlan AJ (1974). Development of some lake ecosystems in Tropical Africa with special reference to the invertebrates. Biol.Rev., 49: 365-97.

4. McLachlan AJ (1979). Decline and recovery of the benthic invertebrate communities. pp. 143-60. In: Kalk et al (eds.) Lake Chilwa. Studies of change in a tropical ecosystem. Monographiae biologicae, 35. Junk. The Hague.

5. McLachlan AJ (1979). The aquatic environment: I. Chemical and physical characteristics of Lake Chilwa.pp.59-78. In: Kalk et al. (eds.) Lake Chilwa. Studies of change in a tropical ecosystem.

6. McLachlan AJ (1986). Chironomid wing length: a measure of habitat duration and predictability? A reply to Vepsalainen. Oikos, 46: 271-73.

7. McLachlan AJ. (1988). Male mating success in Diptera: A reply to Thompson. Oikos, 51: 109.

8. McLachlan AJ (1988). Animal populations at extreme densities: size dimorphism by frequency dependent selection, in ephemeral habitats. Functional Ecology, 3: 633-43.

9. McLachlan AJ and Neems RM. (1995). Swarm-Based Mating Systems. In: Insect Reproduction (eds SR Leather & J Hardie). CRC press, London.

10. McLachalan AJ 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.

11. McLachlan AJ and Ladle R. (2008). The evolutionary ecology of detritus feeding in the larvae of freshwater Diptera. Biological Reviews, 84: 133-141.

12. McLachlan, AJ and Ladle, R (2010). Barriers to Adaptive Reasoning in Community Ecology. Biological Reviews, 86, 543-548. (doi: 10.1111/j.1469-185X.2190.00159.x).

13. McLachlan, AJ and Ladle, R (2010). Fluctuating Asymmetry in Flies, What Does It Mean? Symmetry, 2, doi:10.3390/sym2021099, 1099-1107.13.

14. McLachlan, AJ (2011). Homosexual Pairing within a Swarm-Based mating System: The Case of the Chironomid Midge. Article ID 854820, 5 pages (doi: 10.1155/2011/854820).