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).