Sexual Size Dimorphism

Sexual size dimorphism in the chironomid midge: A sheep in wolf's clothing?

Athol J. McLachlan^a,*, Kirsty J. MacLeod^b, Rachel M. Neems^a.

^a School of Biology, University of Newcastle, Newcastle upon TyneNE1 7RU

^b Zoology Department, University of Cambridge, Downing Street, Cambridge XB2 3EJ.

ABSTRACT

We measure wing length as an indicator of body size for males and females in mating pairs of two ubiquitous species of chironomid midge, Microtendipes definis (Edwards) and Chironomus anthracinusZetterstedt, in the wild. These measurements show that the ratio of male to female size , sexual size dimorphism (SSD), scales hypoallometrically with overall size in the mating pair. This observation is consistent with the predictions of SSD theory and leads to testable hypotheses concerning the mating strategies of the chironomid midge. The measurement of SSD reveal a hitherto hidden relationship between the sexes in a mating pair, and opens the door to a better understanding of the midge mating system; explicitly a strong correlation is revealed between SSD and female size which leads to the suggestion that mimicry is central to male mating success in these midges. 

Key words: mimicry, predation, Rensch's rule,  sexual selection, size dimorphism.

 *correspondence: A. J. McLachlan, Larach Mhor, Torloisk, Isle of Mull, Argyll, Scotland, PA74 6NH. tel, 01688500103. E-mail address@ a.j.mclachlan@virgin.net.

INTRODUCTION

     The mating system of the chironomid midge is based on the mating swarm (McLachlan and Neems, 1995), the details of which are full of unsolved questions such as the nature of mate choice and predator avoidance (McLachlan, 2012). What is known is that the swarm functions as a lek where males form conspicuous assemblages on the wing which attract patrolling females. Females entering the swarm are captured by males to form pairs which descend to the ground where they can in turn be captured by us to make wing length measurements (McLachlan, 1999). Concurrently, empids are attracted to the swarm which they enter to attempt the capture of a midge (McLachlan, Ladle, & Crompton, 2003). The empid we studies, Empis tesselata,  is  a predacious fly which appears to make heavy use of the midge swarm as a source of  nuptial gifts for his own mate. Since males vastly outnumber females in a midge swarm the captured midge is likely to be a male. Hence, the predator/prey relationship is predominantly between male empids and male midges. For this reason we concentrate on males in this study. As so often, body size is important in this mating system. (McLachlan et al., 2003), and by extension, to predation as well. Both mating pressure (sexual selection) and predation pressure (natural selection) are likely to influence selection on body size and there may be trade-offs between sexual and natural selection.

      Among male midges three phenotypes have been recognised; ά, β and γ males, each appearing to adopt different size determined mating tactics (McLachlan, 2012). For example, both their appearance and wing-beat sound are quit distinct to each size determined phenotype (McLachlan et al., 2003), and size may thus have a strong bearing, not only on mating but on predation as well (Crompton, Thomason, & McLachlan, 2003).  In the first instance we do not set out to test specific hypotheses but rather we here explore what light can be shed on this mating system through a study of relative size of males and females in mating pairs. In this study we measure patterns of Sexual Size Dimorphism (SSD) in the midge mating system. Previous work (R. M.  Neems, Lazarus, & McLachlan, 1992; R. M. Neems, Lazarus, & McLachlan, 1998), has compared size frequency distributions in mating systems, but has not focused explicitly on the relative size of males and females. Our study reveals new testable hypotheses specifies in the Discussion, and lays foundation for future work. SSD is widespread among animals, both invertebrate and vertebrate, and has attracted much attention (Fairbairn, Blanckenhorn, & Szekely, 2007). SSD theory gives prominence to body size effects which are fundamental to the understanding of mating behaviour (M.  Andersson, 1994). Rensch’s rule (Maynard Smith, 1977), is important  to the study of SSD and states that SSD decreases with size when females are the larger sex but it increases in size when males are the larger sex. This holds both between and within species (M. Andersson & Wallander, 2004). Why SSD should be so widespread suggests adaptive advantages in the mating stakes based on the size relationship between the sexes. This is the observation which we here examine for the specific case of the chironomid midge.

     This paper is not a study of SSD or Rensch's rule per se which are both fully explored by Fairbairn and colleagues (Fairbairn et al., 2007). Our assumption is that the two common midge species available for study, Microtendipes difinis and Chironomus anthracinus, have a mating system typical of the chironomid midges. There is much conjecture in this paper. Our hope is that it provides sufficient material to encourage further work.

METHODS

     We obtained three samples of M. difinis from different mating swarms on different evenings, yielding a total of 203 mating pairs. Samples were collected at Washington Wildfowl Park in Northumberland (UK) in late 1980. One sample of C. anthracinus was also obtained, yielding a total of 50 mating pairs. Wings were removed from flies and measured under a stereo microscope at 10 magnifications. Wing length was taken between the anal notch and the distal edge of the wing, excluding the hair fringe (McLachlan, 1986). To test hypotheses about SSD, we use wing length as a proxy for body size, as it is a readily obtained measure, and is closely correlated with other measures of body size (McLachlan & Allen, 1987). Wing length measurements are hereafter referred to as body size.

     For each species, we tested the bias and extent of sexual size dimorphism by comparing male and female wing lengths using Students t tests and Mann Whitney U-tests, depending on estimates of variable normality. Correlation between male and female wing lengths was explored using Pearson’s product moment and Spearman’s rank tests, also depending on normality. Means are reported with standard deviations.

     To assess the allometric relationship between male and female wing length, and to determine if these species conform to Rensch’s rule (that SSD increases with the size of the male in a mating pair if males are larger than females, or vice versa), we used Model II major axis regression. This allowed us to ascertain the allometric exponent β of the power law, y = α × x^β that describes an allometric relationship: β is the slope of the log-log regression. If females are larger than males, and β<1 and="" are="" body="" decreases="" females="" hypoallometry="" if="" larger="" males="" or="" size="" ssd="" than="" with="">1, SSD increases with body size (hyperallometry). In these instances, Rensch’s rule would be supported. To carry out these regression analyses, we used the package “lmodel2” in R (Legendre 2015) to estimate β, and the package “smatr” (Warton et al. 2012) to test the null hypothesis that the slope is not different from 1. Male and female wing lengths were log-transformed before analysis. Probabilities are two-tailed, and 95% confidence intervals are reported. Note that ^β  here is not the same of  β  males discussed elsewhere.

There was a notable male wing length outlier in the M. dificilis sample (1mm smaller than the mean male wing length). We present results for the sample both with and without the outlier.

RESULTS

In both species, male wing length was significantly smaller than that of females (Table 1; M. difinis Mann Whitney test U₂₀₃= 16664.5, P < 0.001; C. anthracinus Mann Whitney test U₄₉= 710.5,, P < 0.001). In M. difinis this effect is maintained when a small male outlier is removed (Students  t test t_365.8 = -3.37, P < 0.001). According to Rensch's rule, we should therefore see a hypoallometic relationship between male and female body size, (SSD should decrease as body size increases, given that females are the larger sex).

Male and female wing length correlate positively in M. difinis(Spearman’s rho = 0.19, S₂₀₂ = 1144792, P < 0.01). The effect is maintained with the male outlier removed (Pearson’s correlation = 0.19, t₂₀₁ = 2.83, P < 0.01). By contrast, in C. anthracinus, male and female wing length do not correlate (Spearman’s rho =  0.10, S₄₉ = 18657.81, P = 0.47).

Table 1. Mean male and female wing lengths for i) M. difinis and ii) C. anthracinus. Results for i) are presented with and without a small male outlier. P values are reported for tests investigating the significance of the difference between male and female wing length.

Species	Male wing length mm ( ± s.d.)	Female wing length mm (± s.d.)	Difference (P)
M. difinis	4.39 ± 0.15	4.45 ± 0.18	< 0.001
M. difinis (without outlier)	4.39 ± 0.13	4.45 ± 0.18	< 0.001
C. anthracinus	5.20 ± 0.17	5.35 ± 0.31	< 0.001

Male and female wing length scale hypoallometrically in C. anthracinus (β = -0.001; Fig.1), and M. difinis with (β = 0.36), and without the outlier (β = 0.27) (Table 2). In all cases, the slopes of these relationships are significantly different from 1 (Table 2). Because females were significantly larger than males in both species, these hypoallometric relationships confirm that both C. anthracinus and M. difinis conform to Rensch’s rule.

Table 2. Results of major axis regressions between male and female wing lengths in C. anthracinus and M. difinis (the latter with, and without, a major outlier), reporting reduced major axis slopes (β), R²of the regressions, and 95% confidence intervals of the slope estimates. P values reported denote the significance of the difference between β and 1.

Species	R2	β	95% C.I.	P
C. anthracinus	0.00	-0.001	-0.23 - 0.23	<0 .001="" p="">
M. difinis	0.02	0.36	0.01 – 0.81	<0 .05="" p="">
M. difinis (without outlier)	0.04	0.27	0.09 – 0.48	<0 .001="" p="">

Fig.1 Male and female body size scale hypometrically in C. anthracinus (a), and M. difinis, with (b) and without (c) an outlier. (Note that in both M. difinis datasets, there is a significant correlation between male and female body size). The major axis regression slopes showing the correlations between male and female body size are shown in red; 95% confidence intervals are shown in grey.

 DISCUSSION

Wing length is used as a surrogate for body size in this study of sexual size dimorphism (SSD), in chironomid midges. Such a measure is a long established devise in insects in general (Fairbairn et al., 2007), p6,  and  in chironomids and related Nematocera in particular (Maiga, Dabire, Lehmann, Tripet, & Diabate, 2012; McLachlan & Allen, 1987; Packer & S., 1989; Takamura, 1999; Xue & Ali, 1994; Yuval, Wekesa, & Washino, 1993). This holds for both sexes (Packer & S., 1989; Xue & Ali, 1994). Size differences between the sexes are almost universal in animals, and   follows from the different selective pressures to which each sex is subject (Greenwood & Adams, 1987). Among chironomid midges males are selected for agility and females for load baring (McLachlan, 1986). The interpretation of Renscsh's rule depends entirely on these differences. To quote (Fairbairn et al., 2007), p9...."SSD primarily reflects the adaptation of each sex to its distinct reproductive role".

Sexual size dimorphism (SSD) is measured here as the difference between size in each sex in a mating pair.  This is a rigorous approach because it eliminates that non-mating part of a species population which does no contribute to the next generation. This is the approach adopted by (Blanckenhorn, 2007). Making individual midges responsible for obtaining a sample of a species population avoids human based sampling errors.

     A comparison of the ratio of male over female size (SSD) in the place of size distribution data for each sex separately, as previously studied (McLachlan & Neems, 1995), reveals something new. That is, a strong correlation appears between SSD and female size. Such a finding supports Rensch's rule and supports the suggestion that there is some sort of change in mating tactic as male size in mating pairs increases (M. Andersson & Wallander, 2004). The change in male mating tactic moves from aerobatic agility for small males (γ males) (Crompton et al., 2003), to something else. We hypothesise that the large males (α males), depend not on aerobatics but rather on the imitating of their own empid predator? The suggestion rests on two observations. First, that there is a size related change in the ratio of males to females. Second, that there is a strong similarity in both appearance (to the human observer) and flight characteristics of alpha males and empids (McLachlan et al., 2003). We find this an arresting hypothesis but it awaits testing.                                       

Our study suggests the possibility of mimicry between midge and empid, specifically the mimicry of a male animal of its predator to achieve a mating, hence the suggestion that the α male should be regarded as a sheep in wolf's clothing. This suggestion begs an adaptive explanation i.e. what does the α male gain by such mimicry? Research on this mating system suggests that mating success for α males can be expected to depend on the length of time he can remain active in the swarm. Since the time spent is curtailed if he falls victim to an empid and since the empid is less likely to attack a fellow empid there are clear fitness gains for the mimic. We recently stumbled upon this insight in the beautiful experiments of (Greene, Orsak, & Whitman, 1987). They discovered a close convergence in appearance and behaviour of a fly and a spider suggesting that the prey is imitating its own predator to escape capture. They point out that: "..."the mimicry of a predator behaviour by its own prey had never before been recorded". We are pleased to acknowledge their priority and regard their aphorism as independent corroboration of the same thing within the mating world of the chironomid midge. Since the work of Greene et al., other examples have come to light, notable the experimentally verified mimicry of the hawk by the cuckoo (Davies, 2008). The mimicry of a male animal of its predator as a means of acquiring a mate would appear an unusual case of sexual selection which opens up conjecture over its evolution. We do not pursue the matter further here. Note that if this is indeed an example of mimicry, it is mimicry hinging on biomechanics, including the adaptive convergence of predator and prey on wing beat sound. Note too that any relationship between size of males and females in mating pairs becomes evident only when size is first converted to SSD. That is the value of SSD in this study of the pairing behaviour in the sexes. 

     We wish to emphasise that this paper is not about mating per se except as a consequence of predation. In other words, there may be a pre-existing sensor bias (Ryan, 2017), on wing beat sound that has been co-opted to the ultimate adaptive role in mimicry.

     The idea of convergence of flight behaviour between predator and prey is testable. A combination of emerging imaging technologies (Crompton et al., 2003; McLachlan, 2010, 2011; McLachlan et al., 2003; McLachlan, Pike, & Thomason, 2008), and of models of predator and prey along the lines of the inspirational work on the empid Ramphomyia longicauda (Funk & Tallamy, 2000) might be rewarding.  Even simple counts of the composition of mating pairs emerging from a swarm might serve the purpose.

We end with a note of caution. We should not try too hard to force ridged mating tactics on a population. Tactics may vary for a variety of ecological reasons as dramatically demonstrated by Thornhill and Alcock, p 281-277, for Panorpa scorpion flies (Thornhill & Alcock, 1983).

Acknowledgements

Michael Cant provided helpful comments on an early draft.  Research was supported by SERC studentship no. 87305549 to R.M.N.

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