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.
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