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

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