Body size, symmetry and courtship behavior of Dysdercus maurus distant (Hemiptera: Pyrrhocoridae)

ECOLOGY, BEHAVIOR AND BIONOMICS

Body size, symmetry and courtship behavior of Dysdercus maurus distant (Hemiptera: Pyrrhocoridae)

AS Jorge; C Lomônaco

Programa de Pós-graduação em Ecologia e Conservação dos Recursos Naturais, Instituto de Biologia, Univ Federal de Uberlândia, Uberlândia, MG, Brasil

^{Correspondence}

ABSTRACT

This study analyses the role of body size and symmetry in the sexual selection and courtship behavior of Dysdercus maurus Distant. Sexual conflicts signaled by coercive mating, female resistance, and pre-copulation fights illustrate the mating system. Male-female struggles were observed in all mating attempts. Females tried to reject males by pushing or running and even by vigorously shaking their bodies, in attempts to dislodge the male from their dorsum. In spite of sexual conflicts during courtship, females actively chose their mates based on morphological and behavioral traits. Larger males with more symmetrical tibiae and longer tarsi that are better copula imposers were more successful in sexual competition. Evidence is presented that sexual conflict and female mate choice should not be mutually excluded.

Keywords: Coercive copula, cotton-stainer, fluctuating asymmetry, mate choice

Introduction

Body size is one of the most important quantitative trait that is subject to continuing evolution (Borgia 1979). It strongly affects fitness and it is also constantly being affected by environmental factors (Schmidt-Nielsen 1984). Typically, sexual selection is thought to influence male body size in the context of female choice and/or male-male competition (Dugatkin & Godin 1998). Large body size often increases pairing success in many organisms (Emlen & Oring 1977, Searcy 1982) and female choice for large males is common among insects (Choe & Crespi 1997).

Another body characteristic related to sexual selection is the fluctuating asymmetry (FA), which is defined as small random deviations of perfect trait symmetry in organisms showing bilateral symmetry (Parsons 1990). If the expression of a bilateral trait is produced by the same genome, then any asymmetry between the sides is a consequence of modifications in the normal development program that may be caused by both environmental and genetic causes (Markow 1995). Consequently, FA could be a good indicator of individual developmental stability and fitness, and females of many species have been described as choosing more symmetrical males as mates (Moller & Pomiankowski 1993, Moller & Swadle 1997), including female insects (Santos 2001).

Sexual selection based on body size is widespread, and the female choice criteria may greatly differ from one species to another (Halliday 1993). Some female insects, for example, have been described as preferring symmetrical (Santos 2001, Beck & Pruett 2002) or vigorous (Shuker et al 2002) males for mating.

In order to increase their reproductive success, males tend to compete for female attention, sometimes developing a coercive copula behavior. This kind of behavior is based on the female reluctance to accept a particular male, consequently promoting sexual conflicts between genders (Gavrilets et al 2001, Arnqvist & Rowe 2002).

Dysdercus maurus Distant, the "cotton-stainer", is a very important agricultural pest in tropical regions (Brisolla et al 1992). This species is responsible for losses of seed weight, seed oil content and for several cotton ball damages produced by bacterial and fungal opportunistic attacks in many Malvaceae species (Almeida et al 1986). According to Nóbrega (1989), this insect displays an elaborated courtship behavior, initiated by the male attempting to laterally approach the female and touching her body with his antennae. The female may reject the male by running away or may allow copulation after numerous courting positions. The male assumes the final copulation posture, positioning itself in a diametrically opposite direction in relation to the female body (tail-tail insertion). During copula, which may last three days, females may continue to feed (Siddiqi 1988, Almeida 1994). The copula does not limit both male and female to move, eat, drink and even excrete. Females will lay eggs shortly after disengagement. Pressured by intra-sexual selection, the long period of engagement is probably related to the male strategy to avoid sperm competition (Alcock 1994).

This study investigates and analyses the role of body size and symmetry in the sexual selection of D. maurus, and describes some aspects of the sexual conflict established during courtship behavior in this species. The tested hypothesis is that these insect females actively choose their reproductive partners based not only on courtship behavior, but also by considering male body traits.

Material and Methods

Sample individuals

Insect pairs in copula (n = 90) and non-paired males (n = 50) and females (n = 50) of D. maurus were collected on cotton balls of plants cultivated at the Experimental Garden of the Instituto de Agronomia da Universidade Federal de Uberlândia, Minas Gerais (18o57'S, 48o12'W). The insects were captured manually from January to April, 2007, and maintained in glass bottles. While being removed from the plants, care was taken in order to avoid disengagement of the pairs. Subsequently, after completion of observations in the laboratory, all individuals were sacrificed and preserved in 70% ethanol.

Behavioral observations

The collected non-paired males and females were kept in plastic arenas containing wet sand as a substrate. Insects were fed daily with fresh cotton balls and the arenas were covered with nylon fabric. The study focused on two kinds of behavior: courtship activities and male competitive conducts. The courtship and copula performance were observed considering 50 couples randomly formed (one male and one female placed in a 441 cm3 arena). Individual male's competitive behavior was observed in arenas (5,400 cm³) where 10 males and 10 females were uniformly allocated, keeping 250 cm3 for each individual. Observation periods of one hour were undertaken, resulting in 30h of observations for each kind of behavior (total of 60h). Complementary field observations were also periodically carried out at the Experimental Garden.

Morphometric and biomass measurements

Pairs of antennae, and of anterior and posterior legs were taken from the collected individuals and mounted on microscope slides and a cover slip. The slides were placed in a 10x magnifying stereomicroscope and the images were scanned. The computer program Adobe Photoshop® version 6.0 (Adobe 2000) was then used to obtain measurements of the length of the following traits: first foretarsus segment (T1), foretibia (FT) hindtibia (HT); and 3º (A3) and 4º (A4) antennae segments. Measurements of bilateral traits were obtained for both sides to evaluate FA. In order to verify accuracy, each trait was measured three times in a subsample of 15 individuals. Insects that were preserved in 70% ethanol were previously dried in an absorbent paper before being weighted on analytical scales.

Statistical analyses

A correlation matrix of the original characters measured on the insect's right side was obtained using Pearson's correlation test indexes. The significant correlated characters were then used for a Principal Component Analysis (PCA) in order to reduce the multidimensionality of the data, obtaining an index of general body size (Manly 1994).

FA was calculated as the mean difference between the right (R) and the left (L) sides, i.e. FA = [(Σ | (R - L) | /n] (Palmer & Strobeck 1986). A two-factor analysis of variance (ANOVA) was used to determine whether the between-sides variation was significantly larger than the measurement error (Woods et al 1998, Perfectti & Camacho 1999). According to Palmer & Strobeck (1986), it is necessary to distinguish FA from other kinds of asymmetry. A t-test was performed to verify whether the means of the signed right minus left distribution were not significantly different from zero, in order to discard the occurrence of directional asymmetry. Antisymmetry was tested by departures of the right-left frequency distribution from normality using Kolmogorov-Smirnov test. Size dependence of FA was tested for each sample by regressing the unsigned absolute difference of the right minus left measurements on trait size.

The normality of the data distribution was subsequently verified by using the Lilliefors test. Then, the data were submitted to a "t" test in order to confirm whether there were significant differences in size, FA, weight and original morphometric measurements between paired and non-paired males (Zar 1984). The average ratio between male and female sizes was also calculated. All statistical procedures were performed using computer software package Systat® for Windows®, version 9.0 (Systat 2000).

Results

Courtship activities

The total of 234 mating attempts (male/female) and 17 successful matings were observed. In all cases, the behavior was initiated by the males, and all males tried to copulate with the first female found, even when several males and females were placed in the same arena. The male initiates the courtship behavior by touching the female's body with the antennae, and then tries to mount her. Assuming a perpendicular position, the male touches the ventral portion of the female's body with its antennae. Whilst mounted, the male everts the edeagus and rotates his body 90o in order to be in a parallel position in relation to the female's body. The male then inserts the edeagus in the female's genital cavity and dismounts the female's dorsum, performing an 180o rotation, such that the two insects now face diametrically opposite directions.

During all observed encounters females tried to reject males. Their reactions against male courtship attempts varied from pushing and running to vigorously shaking their body, trying to dismount the male from their dorsum. During the male attempts to introduce the edeagus into the female's genital cavity, she responded by touching her ventral body surface onto the floor in order to protect her genital cavities, using her legs and dorsum as shields. Immediately after the insertion of the edeagus, the female stopped reacting against the male and accepted the engagement. As a result of the female resistance to the male mating attempts, many females were left upside down, but even in this position, the male continued to attempt to introduce its edeagus into the female's genital openning.

We did not observe any contest (fights) between males for female access (intrasexual selection). Fights between males were only observed in situations in which one male tried to copulate with another male. Apparently, the sexual gender is not immediately recognized by males, since numerous courtship behaviors were observed between males when they meet each other for the first time inside the arena. In some of these cases, the courtship ended without aggressions, but sometimes the courted male pushed and tried to jump away from the other male. In addition, copula attempts with a female involving more than one male were also observed. In this case, the exclusion of one male simply occurred as the result of the impossibility of both individuals to mount the same female simultaneously, and no direct antagonistic actions between the contestant males were observed. Male copulation attempts involving paired-females were also observed, but these attempts never succeeded in separating the previous formed couples.

Size differences between paired and non-paired males

The right side measurements of all morphological traits were correlated among themselves (P < 0.05), excepting the length of the foretarsus segment, which was excluded from further analysis. The PCA analysis revealed that all coefficients of the first main component were positive, which indicates that the multivariate index of size had been adequately elaborated (Table 1). About 72.1% of the total morphometric variation corresponded to size variation (first main component), and the remaining 29.9% was attributed to shape distortion (the other main component). The multivariate index of size, the original trait measurements and the male's weight had normal distributions according to the Kolmogorov-Smirmov test (P > 0.05). The t test did not indicate any significant differences in the size index (t ₍₄₅₎ = -0.811, P = 0.422), FT (t ₍₄₅₎ = 0.209, P = 0.835), HT (t ₍₄₅₎ = -0.233, P = 0.817), A3 (t ₍₄₅₎ = -1.554, P = 0.127) nor A4 (t ₍₄₅₎ = -1.392, P < 0.171) between paired and non-paired males. On the other hand, significant differences were detected for T1 (t ₍₄₅₎ = -5.320, P < 0.001) and weight (t ₍₇₇₎ = 4.501, P < 0.001) between paired and non-paired males. Thus, D. maurus paired-males tend to have larger biomass (40.0 mg ± 1.00 and longer foretarsus segments (12.0 mm ± 0.25 than non-paired males (30.0 mg ± 1.00 and 11.1 mm ± 0.42, respectively).

Choice of symmetrical males

The measurement error of FA was negligible for all traits, as indicated by the highly significant side x individual effect on two-way ANOVA (F _(14,60) = 3051.915, P < 0.001 for T1; F _(14,60) = 345.980, P < 0.001 for FT; F _(14,60) = 449.571, P < 0.001 for HT; F = 6559.869, P < 0.001 for A3, and F _(14,60) = 189.592, P < 0.001 for the A4). All FA distributions were normal, and no evidence of antisymmetry was found. The asymmetry in all traits fluctuated around a mean zero. No correlation between size and FA was observed, except for the first foretarsus segment, which was then corrected (Table 2). The t test indicated that the successfully paired males have more symmetrical hindtibia segments (0.9 mm ± 0.12) than non-paired males (1.4 mm ± 0.22) (t ₍₅₀₎ = -2.054, P = 0.045), but no evidence of FA differences were found for the other traits analyzed (t ₍₅₀₎ = 0.726, P = 0.472 for T1; t ₍₅₀₎ = -0.906, P = 0.062 for FT; t ₍₅₀₎ = 1.185, P = 0.068 for A3, and t ₍₅₀₎ = -1.865 P = 0.242 for A4).

Discussion

Sexual behavior

Sexual conflicts signaled by coercive mating, female resistance, and pre-copulation fights between sexes are characteristic of the mating system developed by D. maurus. Forced copulation has been used as a typical example of conflict of interests between males and females, and demonstrates sexual coercion, already described for some groups of insects and arachnids (Allen & Simmons 1996, Peretti & Willemart 2007). Sexual coercion is a form of sexual antagonistic coevolution that predicts male-female struggles for controlling a reproductive event (Arnqvist & Rowe 2002, Chapman et al 2003), as seen in D. maurus courtship behavior.

The long period of copula in D. maurus, which increases the predation risk and makes foraging more difficult, may be a plausible reason for female reluctance, since coercive copula is usually associated with high reproductive costs that reduce any aspect of survivorship success (Gavrilets et al 2001, Moore et al 2001, Stutt & Siva-Jothy 2001, Arnqvist & Rowe 2002).

Nevertheless, if this kind of intersexual selection tends to favor more manipulative males that are better copula-imposers, it is also an indirect indicative of male's fitness and vigor (Cordero & Eberhard 2003). Consequently, Eberhard (2002) considers that female resistance behavior during courtship does not necessarily imply forced copulation, but persuasion, because such behavior may function instead as a test in order to favor some males over others, or to induce the male to give up. As such, female defenses against coercive copula may be alternatively interpreted as an indirect way of male selection (Cordero & Eberhard 2003). Consequently, although receiving no direct benefits for having a confrontational behavior during courtship, females would be indirectly benefitted by producing good manipulative offspring (Kirkpatrick 1982, Price et al 1993, Iwasa & Pomiankowski 1999, Day 2000, Gavrilets et al 2001).

Sexual selection based on female choice results in any behavioral or physiological mechanism that makes a particular male more successful as a sexual mate (Kirkpatrick & Ryan 1991, Andersson 1994). Although sexual conflict and female choice are different hypotheses explaining the function and the evolution of sexual traits involved in mating, they are not necessarily mutually exclusive (Thornhill 1981, Peretti & Willemart 2007). In fact, Allen & Simmons (1996) and Peretti & Willemart (2007) presented evidence that sexual coercion and selective female choice may occur simultaneously.

Selected males

Heavy D. maurus males possessing longer foretarsus segments tend to reproduce more successfully, probably because of their enhanced ability to enforce copulation. The advantages of these characteristics for coercive copula may be related to the ability of such males to subdue females during the courtship behavior in spite of their reluctance. Additionally, larger males are probably better to spatially exclude their competitor when a female is being harassed by another male.

The absence of any observed difference in size between paired and non-paired males, in spite of the significant evidence of biomass differences between them, was probably due to the use of body appendices as the original variables for the estimation of the size index, instead of the use of measurements made on the body itself.

The success of larger males during sexual selection and the selection for larger females, which are usually more fecund, are the two main evolutionary forces favoring the increase of body size in several species (Honek 1993, Andersson 1994). Numerous studies have already registered the influence of body size in the results of aggressive combats between insect males (O'Neill 1983, Goldsmith 1987, O'Neill et al 1989, Rasmussen 1994). Sexual size dimorphism, as seen in D. maurus, with females being larger than males, is common in the majority of insects and it is referred to as female-biased size dimorphism (Andersson 1994). This pattern is most frequently attributed to fecundity selection, since egg or offspring size strongly increases with body size (Honek 1993).

Nevertheless, sexual selection can also favor smaller males through greater agility during courtship displays (Andersson & Norberg 1981, McLachlan 1987), faster development (Singer 1982, Bulmer 1983), higher searching capabilities for females (Fagerström & Wiklund 1982) or even due the female preference for smaller males (Petrie 1983, Steele & Partridge 1988).

Our previous observations (Jorge & Lomônaco 2009) indicated that female choice for a particular male is also based on her own size, which is a result of a trade-off between the negative influence of large partner size in female fecundity and the advantages of large male size for offspring fitness (Oliveira et al 2003). Although larger males may have the advantage of being better manipulators, they do not benefit the female's movements and foraging activities during the copulation period, which can be extended for up to three days, when the couple assumes the diametrically opposite direction posture. If females fail to conduct necessary feeding and defensive movements during the copula, the survivorship of their offspring may be at risk.

Females of D. maurus also choose males with more symmetrical hindtibiae. Symmetry may be related to female choice because it reflects an animal's ability to cope with the sum of the challenges during its growing period and, thus, it is a potential benefit or fitness indicator (Moller & Pomiankowski 1993). Additionally, symmetry may confer an advantage for males in maintaining themselves on the female's dorsum. Some studies support the idea that low FA is linked to enhanced fitness when a structure having a mechanical significance is under selection. For example, Sepsis cynipsea (L.) females tends to copulate with males possessing more symmetrical foretibiae because of their better competitive ability to grip the female's wing bases and thereby remain on the female dorsum during the guarding period (Allen & Simmons 1996).

In conclusion, D. maurus females choose larger males with more symmetrical tibiae and longer tarsus that are better copula imposers. Evidence is presented that sexual conflict and female mate choice should not be mutually excluded.

Acknowledgments

This project was partially supported by CAPES, which provided a scholarship to A S Jorge. We thank Dr Peter Gibs for English revision and FAPEMIG for publishing support.

Received 02 April 2010 and accepted 27 August 2010

Edited by Angelo Pallini - UFV

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Publication Dates

• Publication in this collection
  21 June 2011
• Date of issue
  June 2011

History

• Received
  02 Apr 2010
• Accepted
  27 Aug 2010