Influences Of Fluctuating Asymmetry On Mating Behavior In Insects

 Abstract: "Fluctuating asymmetry describes differences in degrees of bilateral symmetry within and 
between organisms (Sodhi 1996, Van Valen 1962). It reflects that degree of divergence of mirror 
imagery expressed by opposite or bilateral body components or appendages. Watson and Thornhill 
(1994) refer to fluctuating asymmetries as "measures of maladaptation" which appear to be more 
stable within individuals than other indices of phenotypic quality.

Numerous entomological articles have described insect mate selection or rejection and the subsequent 
copulatory success in terms of fluctuating asymmetry (Eggert and Sakaluk 1994, Ueno 1994, Polak 
1993, Harvey and Walsh 1993). For example, Thornhill (1993) found that males of Panorpa japonica 
compete for sexual favors. First a male will capture a nuptial gift (food, e.g., a caterpillar) to present 
to a female. Next it releases pheromones to attract in a responsive female, but often it loses the 
caterpillar to a more aggressive male. That male in turn presents it to the receptive female and 
eventually he mates with her. Evidently females selected aggressive males possessing nearly 
symmetrical forewings, rejecting those with higher fluctuating asymmetries.

Other fluctuating asymmetries of male body appendages besides degree of wing variability also appear 
to influence, along with courtship behavioral patterns, the outcome of successful encounters (Allen and 
Simmons 1995). The extent of male ornamentation and body size are related to successful mating. A 
selection process by the female that creates a discriminating picture of a mate for her to accept, based 
on some degree of fluctuating asymmetry, may actually be genetically advantageous (Watson and 
Thornhill 1994). Results influence natural selection and species survival. The focus of this review is 
the investigation of fluctuating asymmetry and its role in insect sexual selection during courtship and 
the implications these fluctuating asymmetries have on mating behavior.

                            INTRODUCTION

Many genetically encoded behaviors have evolved in insects to insure successful mate attraction and 
copulation. These behaviors function both temporally and spatially to assure a successful encounter. 
Included among these courtship rituals are the offering of nuptial food gifts (caterpillars and other 
arthropods), signals announcing availability and location (visual, auditory, olfactory) that are 
produced to attract from a distance a mate's attention, and courtship dances that stimulate immediate 
up-close interest in a prospective partner by the quality of his dance, which reflects on his "fitness" as 
one suitable to pass on that specie's traits. Every species relies on its genetics as well as morphology, 
environment, and behavioral patterns to assure its perpetuation. Therefore, mate selection is very 
important even to the extreme where the male of some species removes a previous suitor's sperm from 
the female before mating with her, while the female of another species rejects a suitor that cannot 
penetrate her deeply enough.

Another important factor in mate selection is the "fluctuating asymmetry" (FA) of morphological 
bilateral symmetry. Types and extent of asymmetry are seen to influence life-history behavioral 
patterns such as mate selection, copulation success, and the probability of repeated mating encounters 
in plants and animals, vertebrates and invertebrates. This review focuses on the phenomena of 
fluctuating asymmetry and its role during courtship on insect mating behavior. The purpose here is to 
assess its role and demonstrate through examples from the literature its importance in insect mate 
selection.

DEFINING FLUCTUATING ASYMMETRY

In recent years a growing literature base has developed around fluctuating asymmetry in assorted 
contexts. The result has sparked interest across diverse disciplines from plant and animal genetics 
(Polak 1993) and botany (Jennions 1996) to human physiology (Thornhill et al. 1995). Fluctuating 
asymmetry is  defined as those differences in degrees of variation between left and right from perfect 
bilateral symmetry within and between organisms (Sodhi 1996, Van Valen 1962). It reflects that 
random degree of divergence from perfect mirror imagery desired in opposite or bilateral body 
components or appendages. Watson and Thornhill (1994) refer to fluctuating asymmetries as 
"measures of maladaptation" which appear to be more stable within individuals than other indices of 
phenotypic quality, although environmental stress (Bortolotti and Gabrielson 1995, Zakharov 1992) 
and individual trauma (Moller 1992a, Cuthill et al. 1993) also are influences.

 ROLE OF FLUCTUATING ASYMMETRY IN INSECT REPRODUCTION

Numerous articles exist from Van Valen's (1962) early works to the present describing the FA 
phenomena in a variety of organisms. Interest in FA and its relationship to mate selection began only 
recently (Ueno 1994). Interest in copulatory success and FA in insects only took hold in the 1990's 
(Moller 1991, 1992b, Moller and Hoglund 1991, Eggert and Sakaluk 1994, Ueno 1994, Polak 1993, 
Harvey and Walsh 1993, Thornhill and Sauer 1991). Thornhill's research (1979, 1980, 1981, 
1987, 1992a, 1992b, 1993) added extensively to our knowledge of the Mecoptera, with much of his 
later work directed toward FA in Panorpa species. The balance of this report reviews those behaviors 
that have been observed in insect courtships that are attributable to or are a result of FA. These 
outcomes influence natural selection and species survival. Such FA that can occur elsewhere in an 
insects life cycle and do not relate to reproduction, such as stress caused during molting, or atypical 
displays of defensive behavior are not addressed.

EFFECTS OF FLUCTUATING ASYMMETRY IN WING LENGTHS

It is appropriate to begin by acknowledging Thornhill's contribution to insect behavior. Through his 
career he has continued to provide new knowledge about the insect order Mecoptera (scorpionflies and 
hangingflies) beginning with his Ph.D. dissertation (1974) to the present. Thornhill (1992b, 1993) 
provides an example of fluctuating asymmetry using the courtship behavior of the scorpionfly Panorpa 
japonica. Courtship in the species requires the male to present a nuptial food gift to the female before 
he can mate with her. The following courtship was observed by Thornhill to be typical of the species. 
Two adult males were seen fighting over a dead caterpillar which the winner would give a female. Upon 
subduing the rival, the winner proceeded to evert a gland in its genital apparatus releasing pheromones 
to attract in the female. Positioning itself about a foot away, the looser followed suit. Before any female 
arrived, a third male appeared, fought, and defeated the first winner, taking the caterpillar for itself. 
This time the new looser moved a short distance away and began signaling. Eventually a female arrived 
and mated with the final winner, while feeding on her nuptial caterpillar during the hour-long mating 
encounter.

Thornhill made an interesting determination after observing numerous such performances. Body size 
differences were not significant (P=0.328) between mating males (16.253 mm) and fighting ones 
(16.003 mm). Fluctuating asymmetry in this case was identified as the difference in length between 
the forewings, measured from their bases to their tips. The female would mate with that individual that 
exhibited the least degree of fluctuating asymmetry. Upon inspection, the wings of the looser from the 
first battle had the widest FA: the left and right forewings differed in length by 0.7 mm. By comparison 
the winner's forewings fluctuated 0.3 mm between left and right. In the second encounter no 
measurable difference was determined between the winner's forewings.

How can this be correlated with winning fights and mating success? One suggestion makes the argument 
that the amount of stress that P. japonica experiences correlated with the degree of FA in the forewings. 
The more stress it undergoes, the more FA it exhibits. Stress can take the form of food deprivation, 
temperature extremes, or of disease (Moller 1992).

OLFACTORY CUES PLAY A ROLE

The next question asks how the female selects that male with the least FA. Thornhill (1992b) presented 
strong evidence which demonstrated that her selection was based on acute olfactory discrimination. She 
apparently has the ability to discern between subtle differences in pheromone concentrations of 
prospective mates.

To test this a 3.5 in open-ended tube was laid on its side and a pheromone-releasing male in a mesh cage 
was placed just inside each end. Each pair of males differed from one another by its degree of FA 
between their left and right wings; occasionally a perfect male (no measurable FA) was substituted in 
one end. Next a female was introduced through a small hole in the middle of the tube and once inside, she 
could neither see nor touch the males. In 44 of 50 trials (88%) (Thornhill 1993) she was attracted 
toward the male with the least FA. The mechanism for this behavior is not understood, but Thornhill 
suggests that the answer may lie in the male's diet. A male eats some of its gift before giving it to the 
female. If nutrients in the caterpillar provide greater pheromone production, they may also provide 
greater symmetry. Symmetry equates to greater fitness. which the female wants to see for assurance 
her offspring will be healthy with good genes. Whatever this selection process by the female is, it 
creates a discriminating picture of a mate worthy of her acceptance, based on some degree of fluctuating 
asymmetry, and possibly other factors that may be genetically advantageous (Watson and Thornhill 
1994).

WING LENGTH AND LIFE SPAN

The relationship between FA of forewings and number of days that P. japonica survived were inversely 
correlated for males and females (Fig. 1). This appears consistent with findings by Ueno (1994) who 
also found a similar negative FA correlation with adult longevity of the ladybird beetle Harmonia 
axyridis (Table 1). An inverse correlation existed also in males between FA and mating frequency (Fig. 
2).  Males with little to no FA in wing length mated most often. As FA increased their mating encounters 
quickly decreased. On the other hand the average number of mates was constant for females, regardless 
of the degree of FA in their wing lengths (Fig. 2). 

SECRETS OF THE DUNG FLY

Other fluctuating asymmetries of male body appendages besides degree of wing variability also appear 
to influence, along with courtship behavioral patterns, the outcome of successful mating encounters 
(Allen and Simmons 1996). The extent of male ornamentation and body size are related to successful 
mating in some species. Male flies of the dung fly Sepsis cynipsea (Diptera: Sepsidae) apparently are 
indirectly selected by females to mate with them based on an individual male's competitive ability to 
hold on when the female attempts to dislodge him (Allen and Summons 1996). Several males may try, 
but only a few will succeed through copulatory struggles, to mate. This behavior may be a means of 
determining the male's fitness, or of reducing the energy used by the female in mating costs. 

This species pursues an unusual mating procedure takes place: oviposition is undertaken before mating 
(Parker 1972). When females are at the dung, males mount them clamping themselves on with 
forefemora and foretibia modified to clasp the female's thorax. Other males try to dislodge them, but are 
generally unsuccessful. During this period of ovipositioning, the male simply hangs on, or 'passively 
guards' her, not attempting genital contact. Afterwards, the female leaves the dung and enters the 
surrounding grass where she then attempts to dislodge him with shaking and struggling. Although larger 
males are more likely to eventually mate with her, their size distribution changed little before and 
after struggling. Therefore, struggling appeared not to be an elimination filter for males of less than 
optimum size (Allen and Simmons 1996).

Absolute fluctuating asymmetry in males' foretibiae influenced their mating success; foretibiae were 
most symmetrical in males paired in copula and least symmetrical in those paired prior to copulation. 
Symmetrical foretibiae apparently gave males a mechanical advantage in maintaining their grip which 
decreased with increasing FA. This indirect mate-selection-by-struggling process may provide females 
with the best and most symmetrical male offering to father her progeny.

Harvey and Walsh (1993) found that FA and lifetime mating successes are correlated in males of the 
damselfly Coenagrion puella. By recording the number of successful matings of males that had been 
marked and measured, they report that the wings of those that obtained more mates were, on average, 
more symmetrical than those with fewer matings. However, they could not determine if this success 
(Fig. 3) was attributed to symmetrical males enjoying a higher daily mating rate, and thus a higher 
lifetime mating success, or whether they lived longer thus giving more opportunities to encounter 
females.

Males appear not to perform any extended courtship, though scramble competition exists. These 
premating activities appear to interfere very little with their fitness, with negligible effect on their 
life span, so they get on with mating over and over. This appears consistent with studies on Drosophila 
melanogaster where males that spent most of their time courting died young, compared to males that 
either mated unhindered or not at all lived consistently longer (Motluk 1996).

FLUCTUATING ASYMMETRY IS NOT ALWAYS INDICATIVE OF SUPERIORITY

Eggert and Sakaluk (1994) investigated relationships between FA and investment in courtship food 
gifts in the decorated cricket, Gryllodes sigillatus (Orthoptera: Gyrillidae). Males were observed to 
create a two-part spermatophore consisting of the ampulla that contains the sperm. This is surrounded 
by a larger gelatinous mall, the spermatophylax. This latter is consumed by the female after mating. 
But first she removes the spermatophylax, leaving the ampulla attached to her genital opening. 
Spermatophylax size indicates to the female the male's insemination success. The larger the 
spermatophylax, the longer time for her to consume it, hence more time for sperm transfer from the 
ampulla. The more sperm transferred, the greater fitness that is passed on, based on numerical 
abundance (Sakaluk 1986). Synthesis of the spermatophylax is costly to the male and only stronger 
more fit individuals would be expected to possess resources for their manufacture. Given such costs, 
Eggert and Sakaluk (1994) would have predicted a negative correlation between FA and spermatophylax 
mass. However, here was an example where after observing 202 sires and sons, spermatophylax mass 
was correlated with male body mass, but FA of the wings was not correlated with male body mass.

IN CLOSING

Many studies have concerned themselves with the phenomena of fluctuating asymmetry. In this review I 
had hoped to find more examples of observed insect mating behavior influenced by fluctuating 
asymmetry. The behavioral studies I found were done primarily during the first half of the 1990's. 
Indeed, there is the question if FA is the factor involved, or whether several genetically encoded traits 
are responsible for the observed actions by females. Ueno (1994) showed that not all comparisons 
involving FA should be expected to be negative. Measuring ladybird beetles for directional asymmetry 
using ANOVA populations were found normally distributed. Tests for differences in FA between mated 
and unmated mates showed no relationship with male mating success. Ueno (1994) offered three 
explanations. First, male fitness may not be a factor in this species. In Drosophila melanogaster it was 
the species-specific mating system that regulated the relationship between mating success and 
fluctuating asymmetry (Markow and Ricker 1992). Second, fluctuating asymmetry does not reveal all 
male qualities. The males may possess unobservable heritable traits which cannot be assessed by FA, 
but the females make their assessment of the males based on their assessment of them. Third, one 
character may be insufficient for estimating FA; additional characaters may be necessary. Knowledge of 
other characters may lead to different conclusions. On the other hand, as shown above, symmetrical 
wings should provide a direct benefit for more than just mate selecation (Harvey and Walsh 1993); in 
males they should equate to better flight and maneuverability and thus more likely to catch females.

It appears in certain situations that what fluctuating asymmetry demonstrates in not clear. It has been 
equated to fitness, but that may just be the form in which the fitness of the individual is visually 
perceived, not the manner in which a female selects a prospective mate. As Thornhill (1993) 
demonstrated, Panorpa japonica females can select a male possessing the least FA without seeing or 
touching the individual, presumably by odor. How such acute pheromonal recognition and 
discrimination are accomplished may be: (1) through recognition of a single pheromonal compound, 
(2) through recognition of a combination of such compounds, (3) through recognition of their 
combined concentration, or (4) through recognition of ratios of individual concentrations. There is a 
need for more interest in insect behavioral work to answer these and other questions about fluctuating 
asymmetry.

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