Sexual dimorphism and courtship behavior in Drosophila prolongata

Sexual dimorphism is often derived from sexual selection. In sexually dimorphic Drosophila species, exaggerated male structures are used for specific behaviors in male-to-male competition or courtship toward females. In Drosophila prolongata, a member of the melanogaster species group, males have enlarged forelegs whereas females do not. However, the adaptive role of the enlarged forelegs is unclear because little is known about the behavior of D. prolongata. In this study, the courtship behavior of D. prolongata was investigated in comparison with closely related species. Males of D. prolongata use their forelegs in a specific behavior, “leg vibration”, in which the male vigorously vibrates the female’s abdomen by extending his forelegs from in front of her. Leg vibration was observed immediately before “attempting copulation”, indicating that it has an adaptive role in the mating process. In contrast, leg vibration was not observed in closely related species. Because the large forelegs are necessary to accomplish leg vibration, it was suggested that the sexual dimorphism of D. prolongata forelegs is currently under the influence of sexual selection in courtship behavior.     

Variation in morphological and behavioral traits among isofemale strains of Drosophila prolongata (Diptera: Drosophilidae)

Drosophila prolongata, a member of the rhopaloa subgroup of the melanogaster species group, occurs in Southeast Asia. Drosophila prolongata is known to have unique and prominent sexual dimorphism, with extraordinarily thick and elongated forelegs only in males. Mating behavior of D. prolongata is also characteristic: males perform “leg vibration” in their courtship toward females, in which the elongated forelegs play an important role. Comparisons with closely related species suggest that these morphological and behavioral traits have evolved rapidly after the divergence of D. prolongata. In the present study, variation in morphological and behavioral traits was examined among D. prolongata strains derived from single females collected in their natural habitats. Significant variations were detected in the size of various body parts, aggressiveness of interactions between males, and mating behavior. However, no obvious relationship was observed between morphological and behavioral traits. These results suggested that genetic factors contribute to the variation in morphological and behavioral traits in D. prolongata. The strains characterized in this study are useful for studies on the genetic mechanisms underlying the evolution of characteristic traits in D. prolongata.     

A courtship behavior that makes monandrous females polyandrous

Females of many animal species mate several times with different males (polyandry), whereas females of some species mate with a single male (monandry) only once. Little is known about the mechanisms by which these different mating systems evolve. Females of Drosophila prolongata mate serially, unlike Drosophila melanogaster females that refuse to remate for several days after their first mating (remating suppression [RS]). Nevertheless, interestingly, nonvirgin D. prolongata females refuse to remate with males that are prohibited from performing their species-specific courtship behavior, leg vibration (LV), suggesting that LV overrides RS making it cryptic in D. prolongata. In this study, we examined how long this cryptic RS persists. Surprisingly, it was sustained for at least 2 weeks, showing that RS is substantially augmented in D. prolongata compared to that of D. melanogaster. The two most closely related species to D. prolongata, Drosophila rhopaloa and Drosophila carrolli, do not perform LV and showed augmented RS, supporting the idea that augmented RS could have evolved before LV was acquired. These results suggested that D. prolongata females are intrinsically monandrous, whereas the newly evolved courtship behavior makes them polyandrous. This is a rare case in which a proximate mechanism of polyandry evolution from monandry is demonstrated.     

Me against who? Male guppies adjust mating behaviour according to their rival’s presence and attractiveness

Sexual selection theory suggests that males need to constantly reappraise their mating decisions to take account of the presence and the phenotypes of their rivals. Here we examine this expectation by asking: (i) If the presence of a rival influences male mating behaviour; (ii) How important is the attractiveness of the rival (absolute attractiveness) in shaping male behaviour; and (iii) How does a male's attractiveness in comparison to his rival (relative attractiveness) influence a male's mating decisions. Using the Trinidadian guppy, a species in which female mate choice (based on males’ attractive traits) plays an important role in male mating outcomes, we recorded the frequency of courtship displays and unsolicited attempts by focal males. First, we quantified focal male mating behaviour with and without a rival. Since the probability of a successful mating is, on average, halved by the presence of a rival, we predicted that under competition the focal male would invest more in less costly mating tactic—unsolicited attempts. Second, we examined how the rival's standard length and area of orange coloration mediated focal male mating behaviour. We found that rival presence influenced how focal males responded to females in terms of both mating tactics. However, the rival attractiveness elicited changes only in male courtship display. Focal males increased courtship display rate if his rival was small or if possessed large amounts of orange, regardless of considering rival absolute or relative attractiveness. Our results show that males invest in the costlier mating tactic when there is no rival or in the presence of a smaller rival. Interestingly, they make a similar investment in the presence of an attractive orange rival. Overall, this study highlights the importance of fine‐grained male decisions in mating encounters and shows that mating tactics are differentially shaped by multiple competition risk cues.     

同种雄性竞争对手的存在对星豹蛛雄蛛求偶和交配行为的影响

越来越多的研究发现,雄性产生精子(精液)也需付出代价。雄性除了依据配偶质量和竞争对手的竞争强度适应性调整生殖投入外,雄性在求偶和交配行为上也相应产生适应性反应,求偶和交配行为具有可塑性。目前雄性求偶和交配行为可塑性研究主要集中于雌性多次交配的类群中,在雌性单次交配的类群中研究甚少。以雌蛛一生只交配一次而雄蛛可多次交配的星豹蛛为研究对象,比较:(1)前一雄性拖丝上信息物质对后续雄蛛求偶和交配行为的影响,(2)雌雄不同性比对雄蛛求偶和交配行为的影响。研究结果表明,星豹蛛前一雄蛛拖丝上的信息物质对后续雄蛛求偶潜伏期、求偶持续时间和交配持续时间都没有显著影响,但前一雄蛛拖丝上的信息物质对后续雄蛛求偶强度有显著抑制作用。同时,性比对星豹蛛雄蛛求偶和交配行为都没有显著影响。可见,星豹蛛雄蛛对同种雄性拖丝上的化学信息可产生求偶行为的适应性调整,而对性比不产生适应性反应。     

Double meaning of courtship song in a moth

Males use courtship signals to inform a conspecific female of their presence and/or quality, or, alternatively, to ‘cheat’ females by imitating the cues of a prey or predator. These signals have the single function of advertising for mating. Here, we show the dual functions of the courtship song in the yellow peach moth, Conogethes punctiferalis, whose males generate a series of short pulses and a subsequent long pulse in a song bout. Repulsive short pulses mimic the echolocation calls of sympatric horseshoe bats and disrupt the approach of male rivals to a female. The attractive long pulse does not mimic bat calls and specifically induces mate acceptance in the female, who raises her wings to facilitate copulation. These results demonstrate that moths can evolve both attractive acoustic signals and repulsive ones from cues that were originally used to identify predators and non-predators, because the bat-like sounds disrupt rivals, and also support a hypothesis of signal evolution via receiver bias in moth acoustic communication that was driven by the initial evolution of hearing to perceive echolocating bat predators.     

Interacting effects of size and prior injury in jumping spider conflicts

An animal's ability to win intrasexual conflicts is often determined by the combined influence of several different traits, such as size, experience, residency and prior injury. When each of two (or more) asymmetries favours a different rival, the outcome of a conflict will reflect each asymmetry's contribution to overall status. We investigated the interacting effects of size difference and prior loss of forelegs (a common injury in nature) on the ability of males to win intrasexual conflicts in Trite planiceps, a New Zealand jumping spider (Salticidae). When both rivals were intact, the probability of the larger rival winning increased with the size difference between rivals. When rivals were of matching size, injury was a strong predictor of outcome; intact spiders beat rivals missing one or both forelegs and spiders missing one foreleg beat rivals missing both forelegs. During conflicts between spiders that differed both in size and in injury state, these two variables had combined effects on outcome. The tendency for larger rivals to win increased with size difference, but the probability of the larger rival winning diminished if the larger rival of the pair was the more injured. We used inverse prediction from logistic regression models to quantify the size advantage that is sufficient to offset the disadvantage of prior injury.Copyright 2003 Published by Elsevier Science Ltd on behalf of The Association for the Study of Animal Behaviour.      

Sex‐specific evolution of relative leg size in Drosophila prolongata results from changes in the intersegmental coordination of tissue growth

Evolution of relative organ size is the most prolific source of morphological diversity, yet the underlying molecular mechanisms that modify growth control are largely unknown. Models where organ proportions have undergone recent evolutionary changes hold the greatest promise for understanding this process. Uniquely among Drosophila species, Drosophila prolongata displays a dramatic, male‐specific increase in the size of its forelegs relative to other legs. By comparing leg development between males and females of D. prolongata and its closest relative Drosophila carrolli, we show that the exaggerated male forelegs are produced by a sex‐ and segment‐specific increase in mitosis during the final larval instar. Intersegmental compensatory control, where smaller leg primordia grow at a faster rate, is observed in both species and sexes. However, the equilibrium growth rates that determine the final relative proportion between the first and second legs have shifted in male D. prolongata compared both to conspecific females and to D. carrolli. We suggest that the observed developmental changes that produce new adult proportions reflect an interplay between conserved growth coordination mechanisms and evolving organ‐specific growth targets.     

The behavioural basis of overdominance in competitive mating success at the ebony locus of Drosophila melanogaster

Male files homozygous for the gene ebony¹¹ are partially blind, and at a disadvantage in competitive mating. The courtship of the mutant males is deficient in wing vibration stimulation, which is characterized by a low proportion of sine song and a high intra-pulse frequency. Males heterozygous for ebony have normal vision, but show an increase in courtship song, and are superior in competitive mating to wild type males. The auditory characteristics of courtship song produced by heterozygous males are indistinguishable from those of wild type, and their superiority in competitive mating success is due to overdominance involving this specific element of male courtship behaviour.     

Female Choice or Male Sex Drive? The Advantages of Male Body Size during Mating in Drosophila Melanogaster

The mating success of larger male Drosophila melanogaster in the laboratory and the wild has been traditionally been explained by female choice, even though the reasons are generally hard to reconcile. Female choice can explain this success by virtue of females taking less time to mate with preferred males, but so can the more aggressive or persistent courtships efforts of large males. Since mating is a negotiation between the two sexes, the behaviors of both are likely to interact and influence mating outcomes. Using a series of assays, we explored these negotiations by testing for the relative influence of male behaviors and its effect on influencing female courtship arousal threshold, which is the time taken for females to accept copulation. Our results show that large males indeed have higher copulation success compared to smaller males. Competition between two males or an increasing number of males had no influence on female sexual arousal threshold;—females therefore may have a relatively fixed ‘arousal threshold’ that must be reached before they are ready to mate, and larger males appear to be able to manipulate this threshold sooner. On the other hand, the females’ physiological and behavioral state drastically influences mating; once females have crossed the courtship arousal threshold they take less time to mate and mate indiscriminately with large and small males. Mating quicker with larger males may be misconstrued to be due to female choice; our results suggest that the mating advantage of larger males may be more a result of heightened male activity and relatively less of female choice. Body size per se may not be a trait under selection by female choice, but size likely amplifies male activity and signal outputs in courtship, allowing them to influence female arousal threshold faster.     

Courtship tactics in garter snakes: how do a male's morphology and behaviour influence his mating success?

The behavioural determinants of male mating success play a pivotal role in sexual selection, but remain poorly known for most kinds of organisms, including most reptiles. In Manitoba, Canada, large numbers of red-sided garter snakes, Thamnophis sirtalis parietalis, court and mate in early spring near communal overwintering dens. To understand how a male's morphology and behaviour might influence his mating success, we videotaped 21 groups of snakes each comprising four males of varying body sizes plus a female. All males engaged in courtship, and mating occurred in all groups. Males with better body condition courted more vigorously and successfully than their smaller rivals did. The males that obtained matings were those that maintained their own cloaca closest to that of the female, aligned most of their body with the female, showed high rates of caudocephalic waving, chin pressing and tail searching, and did not allow other males to insert their body beside the female's. These behavioural differences between ‘winners’ and ‘losers’ were apparent from the beginning of each trial. Thus, male mating success in this ‘scramble’ system is determined not by chaotic, stochastic struggle (as has often been inferred) but instead is strongly linked to male courtship tactics. Energy stores (as evidenced by good body condition) may be critical determinants of mating success in these vigorous courtship episodes.     

Female and male genetic contributions to post-mating immune defence in female Drosophila melanogaster

Post-mating reduction in immune defence is common in female insects, and a trade-off between mating and immunity could affect the evolution of immunity. In this work, we tested the capacity of virgin and mated female Drosophila melanogaster to defend against infection by four bacterial pathogens. We found that female D. melanogaster suffer post-mating immunosuppression in a pathogen-dependent manner. The effect of mating was seen after infection with two bacterial pathogens (Providencia rettgeri and Providencia alcalifaciens), though not after infection with two other bacteria (Enterococcus faecalis and Pseudomonas aeruginosa). We then asked whether the evolution of post-mating immunosuppression is primarily a ‘female’ or ‘male’ trait by assaying for genetic variation among females for the degree of post-mating immune suppression they experience and among males for the level of post-mating immunosuppression they elicit in their mates. We also assayed for an interaction between male and female genotypes to test the specific hypothesis that the evolution of a trade-off between mating and immune defence in females might be being driven by sexual conflict. We found that females, but not males, harbour significant genetic variation for post-mating immunosuppression, and we did not detect an interaction between female and male genotypes. We thus conclude that post-mating immune depression is predominantly a ‘female’ trait, and find no evidence that it is evolving under sexual conflict.     

Energetics of the acrobatic courtship in male golden-collared manakins (Manacus vitellinus)

In lek mating systems, females choose mates through indicators of quality, which males may exhibit by their performance of courtship displays. In temperate regions, displaying seasons are brief (one to two months), whereas in the tropics courtship seasons may be prolonged. Moreover, in temperate-breeding animals lekking behaviour can be energetically demanding, but little is known about the energy costs of lekking in tropical animals. Daily, over the course of a nearly seven-month-long breeding season, male golden-collared manakins (Manacus vitellinus) of Panamanian rainforests perform acrobatic courtship displays that markedly elevate heart rates, suggesting that they require high energy investment. Typically, animals of tropical lowland forests (such as manakins) exhibit a ‘slow pace of life’ metabolic strategy. We investigated whether male manakin courtship is indeed metabolically costly or whether the birds retain a low daily energy expenditure (DEE), as seen in other tropical species. To assess these questions, we calibrated manakin heart rate against metabolic rate, examined daily lek activity and, using telemetry, obtained heart rates of individual wild, lekking male manakins. Although metabolic rates peak during courtship displays, we found that males actually invest minimal time (only approx. 5 min d⁻¹) performing displays. As a consequence, the DEE of approximately 39 kJ d⁻¹ for male manakins is comparable to other lowland tropical species. The short, intense bursts of courtship by these birds make up only approximately 1.2% of their total DEE. Presumably, this cost is negligible, enabling them to perform daily at their arenas for months on end.     

Effects of laboratory colonization on Bactrocera dorsalis (Diptera,Tephritidae) mating behaviour: ‘what a difference a year makes’

Laboratory-reared insects are widely known to have significantly reduced genetic diversity in comparison to wild populations; however, subtle behavioural changes between laboratory-adapted and wild or ‘wildish’ (i.e., within one or very few generations of field collected material) populations are less well understood. Quantifying alterations in behaviour, particularly sexual, in laboratory-adapted insects is important for mass-reared insects for use in pest management strategies, especially those that have a sterile insect technique component. We report subtle changes in sexual behaviour between ‘wildish’ Bactrocera dorsalis flies (F1 and F2) from central and southern Thailand and the same colonies 12 months later when at six generations from wild. Mating compatibility tests were undertaken under standardised semi-natural conditions, with number of homo/heterotypic couples and mating location in field cages analysed via compatibility indices. Central and southern populations of Bactrocera dorsalis displayed positive assortative mating in the 2010 trials but mated randomly in the 2011 trials. ‘Wildish’ southern Thailand males mated significantly earlier than central Thailand males in 2010; this difference was considerably reduced in 2011, yet homotypic couples from southern Thailand still formed significantly earlier than all other couple combinations. There was no significant difference in couple location in 2010; however, couple location significantly differed among pair types in 2011 with those involving southern Thailand females occurring significantly more often on the tree relative to those with central Thailand females. Relative participation also changed with time, with more southern Thailand females forming couples relative to central Thailand females in 2010; this difference was considerably decreased by 2011. These results reveal how subtle changes in sexual behaviour, as driven by laboratory rearing conditions, may significantly influence mating behaviour between laboratory-adapted and recently colonised tephritid fruit flies over a relatively short period of time.     

Comparative courtship behaviour in two species of the parasitic chalcid wasp Melittobia (Hymenoptera: Eulophidae)

Timing and form of courtship behaviour elements constitute a major isolating mechanism for two morphologically and ecologically similar parasitic wasps. Because males are blind, the complex courtship of Melittobia chalybii and a new as yet undescribed species previously confused with it, designated as M. sp. A, depends upon tactile and chemical cues. In both species, after the female orients to the male's abdomen, the male turns in the direction of contact and mounts. However, chalybii males antennate females continuously, lifting mesothoracic legs at regular intervals, while in sp. A male antennation alternates with metathoracic leg pumping. Courtship and copulation duration are greater in Chalybii than in sp. A.     

Plastic male mating behavior evolves in response to the competitive environment*

Male reproductive phenotypes can evolve in response to the social and sexual environment. The expression of many such phenotypes may also be plastic within an individual's lifetime. For example, male Drosophila melanogaster show significantly extended mating duration following a period of exposure to conspecific male rivals. The costs and benefits of reproductive investment, and plasticity itself, can be shaped by the prevailing sociosexual environment and by resource availability. We investigated these ideas using experimental evolution lines of D. melanogaster evolving under three fixed sex ratios (high, medium, and low male‐male competition) on either rich or poor adult diets. We found that males evolving in high‐competition environments evolved longer mating durations overall. In addition, these males expressed a novel type of plastic behavioral response following exposure to rival males: they both significantly reduced and showed altered courtship delivery, and exhibited significantly longer mating latencies. Plasticity in male mating duration in response to rivals was maintained in all of the lines, suggesting that the costs of plasticity were minimal. None of the evolutionary responses tested were consistently affected by dietary resource regimes. Collectively, the results show that fixed behavioral changes and new augmentations to the repertoire of reproductive behaviors can evolve rapidly.     

Stickleback Males Increase Red Coloration and Courtship Behaviours in the Presence of a Competitive Rival

In species where females preferentially select the most colourful males, males may strategically invest in courtship and nuptial colour according to the presence of rivals. In this experimental study, we tested this in the three‐spined stickleback (Gasterosteus aculeatus) in which mature males exhibit carotenoid‐based red coloration to attract mates and defend their territories against male competitors. We challenged experimental males with either a red‐ornamented dummy male or a non‐ornamented dummy for five min per day in six‐d experimental trial, which was repeated twice during the breeding season. We found that the males presented with a coloured rival exhibited more frequent courtship behaviours (i.e. fanning and gluing) to females than those presented with a non‐coloured intruder during the second experimental trial. At the end of each trial, the experimental males also showed a significantly larger area of red coloration in the presence of a coloured intruder. Our findings suggest that male sticklebacks regulate mating effort according to the presence of competitive rivals by increasing their investment in costly signals when successful mating and territory defence is at risk.     

Courtship with two spoons—Anatomy and presumed function of the bizarre antennae of Cardiocondyla zoserka ant males

Mating in ants often occurs on the wing during nuptial flights or on the ground when scattered female sexuals attract males by pheromones. In both scenarios, there is little opportunity for males to engage in prolonged aggressive competition or elaborate courtship displays. Male morphology is therefore adapted to locating female sexuals and mating, and it lacks specific weapons or other traits associated with courtship. In contrast, sexuals of the ant genus Cardiocondyla typically mate in their natal nests. As a consequence, in many species winged males have been replaced by wingless fighter or territorial males, which kill or expel rival males with their strong mandibles and show complex mating behavior. However, no wingless males are known from Cardiocondyla zoserka from West Africa, and instead, winged males have evolved a bizarre secondary sexual trait: uniquely shaped antennae with spoon‐like tips that show heavily sculptured ventral surfaces with numerous invaginations. We here report on the courtship behavior of C. zoserka males and describe antennal glands with class 3 gland cells, which presumably secrete a close range sex pheromone. Antennal glands have not yet been found in males of other ant species, including a close relative of C. zoserka, suggesting that in ants with intranidal mating sexual selection can rapidly lead to highly divergent adaptations and the evolution of novel structures.     

Male Wing Fanning Performance During Successful and Unsuccessful Mating in the Parasitic Wasp Lariophagus distinguendus Förster (Hymenoptera: Pteromalidae)

Lariophagus distinguendus Förster (Hymenoptera: Pteromalidae) is a generalist solitary ectoparasitoid that parasitizes the immature stages of at least 11 foodstuff beetles from five families, including species developing in the seeds of Poaceae, Fabaceae and in dried natural products. In L. distinguendus, male wing fanning is a key phase in the courtship sequence and is elicited by a female-borne sex pheromone. However, studies aimed at understanding the role of wing vibration in L. distinguendus during courtship are lacking. In this research, the wing fanning performances of the L. distinguendus male towards other females and males were analyzed through high-speed video recordings and examined in relation to mating success. Only small differences were found between the fanning characteristics displayed toward females and young males, highlighting that young males are really perceived as females by older males. Male mating success was affected by the quality of the wing fanning in the courtship phase. Indeed, both immediately after the female perception and during mating attempts, fanning before a successful courtship differed compared to wing fanning performed prior to an unsuccessful courtship in terms of their mean frequency, but not their amplitude. Overall, our work increases knowledge of the courtship behavior of L. distinguendus and highlights the crucial importance of wing fanning among the range of sensory modalities used in the sexual communication of this parasitic wasp.