Within and Between Species Variation in Male Mating Behaviors in the Mexican Sailfin Mollies Poecilia velifera and P. petenensis

Polymorphism in male morphology is often correlated with the expression of alternate behavioral tactics. This relationship between behavioral and morphological polymorphisms, however, is less well understood. We characterized male mating behaviors and morphological variation within and between Poecilia velifera and P. petenensis to understand mating signal evolution in the sailfin molly lineage. In addition, we examined whether differences between these species in the size range of mature males and the strength of allometry between dorsal fin size and body length could explain the variation observed in their expression of different mating behaviors. We determined each male's mating behavior profile by observing the behavior of a single male in the presence of a receptive female. We found that P. velifera showed evidence of an alternate male mating strategy, with small males generally performing only gonopodial thrusts (forced insemination attempts) towards receptive females, while large males performed courtship displays as well as gonopodial thrusts. Males of P. petenensis performed similar rates of courtship displays and gonopodial thrusts regardless of body length. Little variation existed among populations of P. velifera in mating behaviors, while males from different populations of P. petenensis showed population‐specific average rates of each mating behavior. Population differences in P. petenensis may be driven, in part, by its occurrence in more variable habitats than those occupied by P. velifera. Variation among individuals in the mating repertoire of P. velifera, but not P. petenensis, suggests that the greater range of variation in male size at maturity, as well as considerably stronger allometry between dorsal fin size and body length, may explain why males of P. velifera show the greatest degree of expression of alternate male mating behaviors when compared to other sailfin species. These results also suggest an important role of morphological polymorphisms in predicting the expression of alternate male mating behaviors.     

Do Male Veiled Chameleons,Chamaeleo calyptratus,Adjust their Courtship Displays in Response to Female Reproductive Status?

Variation in male courtship behavior may be due to inherent differences among males or may arise from males adjusting their courtship displays according to female responsiveness. Female veiled chameleons, Chamaeleo calyptratus , exhibit two distinctive suites of body coloration and behavior patterns that vary according to receptive and non-receptive stages of their reproductive cycle. We presented male chameleons with both receptive and non-receptive females, and recorded differences in their mating frequency, courtship intensity and courtship behavior patterns. As expected, males were more likely to court and attempt mating with receptive females. Although fewer males courted non-receptive females, their courtship displays were significantly longer than those directed towards receptive females. Males also adjusted the contents of their displays according to female reproductive condition. Certain behavior patterns were unique to courtship displays directed towards each class of females. Males exhibited the behavior pattern `head roll' only when paired with receptive females, and `chin rub' was displayed only during courtship of non-receptive females. We hypothesize that these differences in male courtship frequency, intensity and content reflect differences in female reproductive value. Although males may benefit from mating with both receptive and non-receptive females, the costs associated with courtship may depend on female responsiveness. Thus, males adjust their courtship tactics accordingly.     

Non‐Conceptive Sexual Behavior in Spiders: A Form of Play Associated with Body Condition,Personality Type,and Male Intrasexual Selection

In the socially polymorphic spider Anelosimus studiosus, males mature early in the reproductive season and recruit to the webs of juvenile females and guard them until they mature. During the period before females mature, males and females engage in repeated bouts of non‐conceptive (play) sexual behavior, where the pair courts and engages in mock copulation; both males and females gain performance‐enhancing experience via these encounters. In this study, we examined the factors that underlie individual variation in the tendency to engage in non‐conceptive mating and determine whether it impacts male–male competition for females. We found that docile females, being less resistant to mating in general, are more likely to accept male courtship and non‐conceptive copulation as juveniles. Personality type influenced the exhibition of non‐conceptive sexual behavior in males as well. High body condition males of the aggressive phenotype were more likely to engage in non‐conceptive sexual behavior than males with lower body condition. Body condition did not influence docile males’ propensity to engage in non‐conceptive sexual behavior, but female size did. Docile males engaged in more non‐conceptive sexual displays with larger females. Engaging in non‐conceptive sexual displays negatively impacted male performance in staged male–male contests for access to females. This cost was greatest for males of the aggressive phenotype, which are otherwise favored in male–male contests. Our findings indicate expression of non‐conceptive sexual displays is linked to personality and results in reproductive performance trade‐offs for male A. studiosus.     

Male mating strategies under predation risk: do females call the shots?

Many authors have reported that, under elevated risk of predation,male guppies (Poecilia reticulata) alter their behavior fromcourtship to forced copulation (gonopodial thrusts not precededby sigmoid displays). This shift is presumed to benefit thebrightly colored male, whose intense courting activity mightotherwise increase his risk of detection and attack by predators.However, there is some evidence that females engaged in reproductiveactivity with males may be even more vulnerable to predatorsthan the males themselves, which suggests an alternative hypothesis:females in high-risk situations are less receptive to male courtship,and this leads males to change their behavior. We tested thishypothesis by providing either males and females separately,or both sexes concurrently, with information about elevatedpredation risk from a cichlid (Crenicichla sp.). We found thatwhen only females were provided with information about increased risk,males performed fewer courtship displays and fewer thrusts.They did not perform more forced copulations in any treatmentgroup. Nonetheless, our results suggest that the female's perceptionof predation risk can be at least as important as the male'sin changing male mating behavior.     

Diet and size influence sexual advertisement and copulatory success of males in Mediterranean fruit fly leks

1. The objective of the work reported here was to test the hypothesis that in insects that invest considerable energy in sexual displays and courtship, foraging successfully for food affects their subsequent performance and copulatory success in leks. Accordingly, the interactions between body size and diet on initiation of lekking behaviour and copulatory success in male Mediterranean fruit flies Ceratitis capitata (Diptera: Tephritidae) were investigated. 2. Protein‐fed males were heavier and contained more protein and less lipid reserves than protein‐deprived males. Protein‐fed males were more likely to emit pheromone in leks and, consequently, were more likely to copulate than protein‐deprived males. Furthermore, protein‐fed males tended to start calling earlier than their nutritionally deprived competitors. 3. Though size was not related to initiation of lek behaviour, large males were more likely to copulate than small males. Among protein‐fed males, large individuals tended to mate earlier than smaller individuals. 4. Generally, in lek mating systems where a considerable investment of time and energy is required by males, foraging successfully for nutritional resources prior to engaging in territorial or courtship behaviour is essential for reproductive success.     

Complex Courtship Behavior in the Striped Ground Cricket, Allonemobius socius (Orthoptera: Gryllidae): Does Social Environment Affect Male and Female Behavior?

Complex courtship in the striped ground cricket, Allonemobius socius, involves a series of behaviors alternating between the sexes. We examined if complex courtship allows either or both genders to evaluate their mate and how mating behavior changes in different social environments. While complex courtship may allow discrimination by both sexes, here only females exhibited a preference. Males did not alter their courtship behavior or change spermatophore size for different size females. In contrast, females initiated copulation more quickly with bigger males possessing bigger spermatophores. In a different social environment (additional male, female, or both), males were less likely to omit courtship songs and female discrimination of mates changed. The distinct differences in male and female behavior suggest that subtle changes in social environment can have important consequences in structuring courtship and mating behavior.     

Analysis of the mating behavior and some possible causes of male copulatory success in Dryas iulia alcionea (Lepidoptera, Nymphalidae, Heliconiinae)

In this study we examined the mating behavior of Dryas iulia and the acceptance and rejection mechanisms of females during courtship activity. An ethogram of mating behavior was organized on the basis of 100 h of observation in an insectarium. Several different behaviors were catalogued and separated into two behavioral repertoires (pre-coupling, post-coupling). The behavioral sequence of mating behavior was also analyzed using a total of 53 pairs of D. iulia. The courtship activities involved interactions between the sexes in three sequential phases—the aerial, air-ground, and ground phases. In 49% of observations the courtship activities led to copulation. The mean time to the occurrence of the first interaction between males and females did not differ between interactions with and without copulation. The behavior of females and males in the two groups were analyzed and differences were found between behavioral activities of both sexes. The results indicate that males’ insistence on courtship does not affect their copulatory success, and that females play a decisive role in copulation occurrence. Analysis of behavioral transitions showed there are many alternative behavioral routines in interactions with and without copulation. The number of behavioral transitions recorded was smaller in the group in which copulation occurred, indicating that males with copulatory success modified their behavior less frequently. Successful males recorded more transitions with a probability of occurrence greater than 0.4, and their behavioral activity was also less reticulated. Analysis using the stereotyping index showed that situations in which copulations occurred were more stereotyped than those in which it did not.     

Spiders,microbes and sex: Bacterial exposure on copulatory organs alters mating behaviour in funnel‐web spiders

Environmental microbes have the potential to be involved in nearly all behavioural processes. For example, mating systems where males use intromittent organs to transfer sperm to females represent a means by which environmental microbes collected by males can breach entry into females' body cavities during mating. However, the degree to which the acquisition of environmental microbes onto important sex structures alters courtship behaviours remains unknown. Here, we collected bacteria from the copulatory organs of Agelenopsis pennsylvanica funnel‐weaving spiders in situ to test whether exposure to bacteria on copulatory organs can alter hosts' courtship behaviour, reproductive success and survival. We used a standardized assay to repeatedly measure each spider's aggressiveness, a behavioural component of both male courtship and female sexual receptivity. Then, we experimentally altered the bacteria present on male and female spiders' copulatory organs with an application of either (a) a mixture of bacteria collected from conspecifics to increase bacterial presence, (b) an antibiotic to reduce bacterial presence or (c) a procedural control. Each spider was paired with a size‐matched spider of the opposite sex whose copulatory organs were unaltered, and we measured the latency until the onset and the duration of courtship. Spiders were then isolated, and we measured each individual's time until death and female fecundity over the next 40 days. We found that female exposure to bacteria had multiple effects on mating dynamics. Males took over four times longer to begin courting females that had been exposed to bacteria compared to unexposed and antibiotic‐treated females. Only when courting these bacteria‐exposed females, males began courtship sooner when females were more aggressive. Lastly, females whose mate had been exposed to bacteria experienced reduced survival. These data suggest that bacteria present on animals' copulatory organs can alter courtship behaviours, female survivorship, and may potentially play a role in mating dynamics.     

Mate Choice and Spawning Success in the Fighting Fish Betta splendens: the Importance of Body Size, Display Behavior and Nest Size

Courtship displays should be exaggerated enough to attract mates and yet tempered so as not to deter them. We tested this hypothesis in the fighting fish Betta splendens by studying courtship displays and body size and their relationships with male parental quality and female fecundity, as well as the effects of display behavior and body size on mate choice decisions and spawning success. Because of their high degree of parental investment, males are expected to be discriminating in their choice of mates. Males who displayed more frequently built larger nests, a measure of parental quality, but larger males did not. When females were paired with males with high display rates, however, the pair had fewer eggs in their nest, even when accounting for female body mass. In a mate choice test using computer‐generated male stimuli that differed only in display behavior, females showed no preferences for displaying males vs. non‐displaying males, or for males with higher display rates vs. lower display rates. In similar tests in which the computer‐generated males differed only in size, females preferred larger males, but also preferred males that differed with respect to body size (negative assortative mating). Males preferred computer‐generated females that performed courtship displays over non‐displaying females, but showed no preferences for female body size. Neither a female's body size nor her display behavior was a significant predictor of her fecundity as estimated by the number of eggs released during spawning. Thus, our results suggest that female B. splendens must balance male parental quality (nest size) with the risk of potentially disruptive or dangerous behavior during spawning, and that females may minimize these risks through negative size‐assortative mating. Female display behavior, while unrelated to fecundity in our study, may attract males because it indicates reproductive readiness or serves a species‐recognition function.     

Male and Female Soldier Beetles Relax Choice for Mate Quality Across Daily Courtship Periods

Mutual mate choice occurs when members of each sex will reject some potential mates in efforts to encounter better prospects later. The decision to reject may represent the interaction between mate preferences, mate availability, and temporal constraints. Theory predicts that mutual mate choice will favor relaxed choosiness as mate availability and time for courtship decline. We explored mutual mate choice in the soldier beetle, Chauliognathus pennsylvanicus (Cantharidae), where courtship consisted of males attempting to secure evasive females. We employed field observations, laboratory experiments, and stochastic simulations to investigate the decline in choosiness over the daily courtship period, during which individuals can mate at most once. We found that reproductive success of males and females increases with mate size and mating frequency. Females biased copulations toward larger mates by attempting to evade suitors, while males biased copulations by releasing the smaller females they capture. However, late in the day males and females may increase reproductive success by accepting rather than rejecting lower quality mates to maintain high mating rates. Stochastic simulations indicated that reproductive success, the product of mating frequency and mean mate size, was maximized in males and females by incrementally reducing mate standards across daily courtship periods. In the field, large males who rejected small females early in the daily courtship period rarely did so later. Large females used less effective evasive maneuvers later in the courtship period, resulting in copulations with progressively smaller males. These results support models of mutual mate choice that predict that individuals of high quality will maximize reproductive success by relaxing choosiness as the courtship period wanes.     

Reproductive Signals of Female Lizards: Pattern of Trait Expression and Male Response

Relative to the volume of studies concerning the function and evolution of male‐biased sexually dimorphic traits, instances of female‐biased sexual dimorphisms remain largely unstudied, especially in species with conventional sex roles. I investigated the signal function of a female‐specific ornamental trait using the striped plateau lizard (Sceloporus virgatus, Phrynosomatidae) as a model system. During the reproductive season, female S. virgatus develop orange color on their throats that is absent in conspecific males. I established the relationship between color expression and female reproductive state, and determined male response to female color. I show that dynamic changes occurring within the color patch can potentially identify each stage of the female reproductive cycle, largely because of a lag in patch growth relative to color intensification. Sexual receptivity is associated with intense patches rapidly growing in size; ovulation occurs near peak color expression; and the unreceptive period is associated with large patches fading in intensity. Because females express orange color during both the receptive and unreceptive periods, the pattern of color expression is consistent with the courtship‐stimulation and courtship‐rejection hypotheses of signal function. Males may preferentially associate with females that have more highly developed color patches during the courtship season, and/or ignore such females when they are unreceptive. An examination of male behavior towards unfamiliar females indicates that female color has a role in courtship stimulation but has little, if any, role in courtship rejection. During the pre‐mating season, males maintained significantly closer affiliation with, and tended to perform more social behavior towards females with more intense color. During the post‐mating season, female color had no apparent effect on male behavior. The evolution and current function of female ornaments may vary among taxonomically‐related species as a result of differences in ecology, social system, and life‐history.     

Mating Behavior, Sexual Selection, and Copulatory Courtship in a Promiscuous Beetle

The function of male movements during copulation is unclear. These movements may be a result of the necessary mechanics of insemination, or they may also have further function, for instance, stimulating or courting a female during mating, perhaps influencing female mate choice. We present data from three experiments exploring the mating behavior and copulatory movements of the highly promiscuous beetle Psilothrix viridicoeruleus. Male mating success in the struggle over mating was not related to male or female size (measured by weight) but successful males were more vigorous in terms of copulatory movements. These males took longer to mount females but copulated longer and remained mounted longer. We discuss these results in terms of the mating system of Psilothrix and also in terms of observations of the timing of insemination during copulation. We suggest that copulatory movements in this species are best understood as copulatory courtship.     

Copulatory Courtship in Drosophila birchii and D. serrata,Species Recognition and Sexual Selection

Two endemic Australian Drosophila species, D. birchii and D. serrata, have a copulatory courtship, i.e., the males court the female mainly during copulation. In the present study we found the males of both species to mount their prospective mating partners selectively, exhibiting both sex and species recognition. The males began to sing after mounting the female, and they often exhibited also postcopulatory displays typical to copulatory courtship. D. birchii and D. serrata females discriminated against males which did not sing during mounting/copulation, which suggests that the females utilize cryptic female choice. Our findings raise the question of how widespread a phenomenon cryptic female choice is in Drosophila species.     

Females produce larger eggs for large males in a paternal mouthbrooding fish.

When individuals receive different returns from their reproductive investment dependent on mate quality, they are expected to invest more when breeding with higher quality mates. A number of studies over the past decade have shown that females may alter their reproductive effort depending on the quality/attractiveness of their mate. However, to date, despite extensive work on parental investment, such a differential allocation has not been demonstrated in fish. Indeed, so far only two studies from any taxon have suggested that females alter the quality of individual offspring according to the quality/attractiveness of their mate. The banggai cardinal fish is an obligate paternal mouth brooder where females lay few large eggs. It has previously been shown that male size determines clutch weight irrespective of female size in this species. In this study, I investigated whether females perform more courtship displays towards larger males and whether females allocate their reproductive effort depending on the size of their mate by experimentally assigning females to either large or small males. I found that females displayed more towards larger males, thereby suggesting a female preference for larger males. Further, females produced heavier eggs and heavier clutches but not more eggs when paired with large males. My experiments show that females in this species adjust their offspring weight and, thus, presumably offspring quality according to the size of their mate.     

Male Reproductive Success in a Promiscuous Armoured Catfish Corydoras Aeneus (Callichthyidae)

Among a variety of fish mating systems, promiscuity with random-mating seems to be most prevalent. However, detailed studies of promiscuity have been rare due partly to the peculiar difficulty in examination of male mating and reproductive success in the random mating. Females of the armoured catfish Corydoras aeneus (no sexual dimorphism other than size of males > females) spawn 10–20 egg-clutches with multiple males at a time, but an entire egg clutch is inseminated by sperm of a single male. We studied mating system of this fish in aquarium. Males had neither mating territories nor monopolized females, never being aggressive against rival males. Evidence of female preference for certain male traits including size was not detected. Females mated a male in proportion to his relative courtship frequency among males. Courtship frequency was not related to male size, and male mating success was not different between small and large males. Clutch size and insemination rate were different neither between small and large males nor between frequently and less frequently courting males. Thus, the male reproductive success will not be related to the male size, but directly to courtship frequency, indicating the random mating in this fish. There seemed to be fecundity advantage with size in female, and the consequent sexual difference in energy allocation will be responsible to the sexual dimorphism. We also discuss the low male-GSI in this promiscuous fish in which sperm competition hardly occurred.     

The energetic costs of alternative male reproductive strategies in <Emphasis Type="Italic">Xiphophorus nigrensis</Emphasis>

The coexistence of alternative male mating strategies depends on the balance between costs and benefits. Here we examine the short-term metabolic costs associated with distinct reproductive strategies in the genetically determined alternative male phenotypes of a northern swordtail, Xiphophorus nigrensis. In this species, large males court females, non-adorned small males chase females, and intermediate males exhibit both courtship and chase behaviors. Using intermittent flow respirometry, we measure oxygen consumption rates and behaviors of each size class in isolation and in the presence of a female. Changes in oxygen consumption between solitary and female presence trials (ΔVO₂) correlated significantly with standard length across all size classes (r = 0.42). Only the large male class exhibited a significant increase in oxygen consumption in female-present trials exhibiting a range of increase from 2 to 200% relative to solitary metabolic rates, but costs of specific courtship displays could not be demonstrated. Sword length explained 54–57% of the variation in oxygen consumption in large male solitary trials and 63–65% in the female-present trials independent of any behavioral correlation with sword length. Our results exhibit similarities to condition-dependent alternative mating systems where the female-favored phenotype has higher energetic costs.     

Influence of male courtship intensity and male–male competition on paternity distribution in Hermann's tortoise,Testudo hermanni hermanni (Chelonia: Testudinidae)

Honest‐advertisement models of sexual selection suggest that condition‐dependent male secondary sexual characters could function as reliable signals of male quality, enabling females to discriminate among potential partners, both in the pre‐ and post‐copulatory phases. In this context, many studies have revealed the importance of promiscuous mating systems and female sperm storage in determining the occurrence of such a model of sexual selection. By contrast, few studies have investigated the presence and extent of post‐copulatory female choice in chelonian species. The present study aimed to investigate the effect of male size, male–male competition, and courtship intensity on paternity distribution in Testudo hermanni hermanni, combining behavioural and genetic data. We created experimental groups composed of two males of different sizes and three or four randomly selected females. Observations conducted during social interactions between males revealed that a hierarchy, unrelated to male size, was soon established: Alpha males were more aggressive towards competitors and courted females more intensively. Alpha males also achieved a higher mounting success than Beta males. Paternity analysis performed on hatchlings produced from experimental females revealed that male reproductive success was not correlated with male–female size ratio. Finally, despite the higher mounting success of Alpha males, paternity analysis revealed that male reproductive success did not differ between Alpha and Beta males. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 656–667.     

Patterns of Inheritance of Mating Signals in Sailfin and Shortfin Mollies (Poeciliidae: Poecilia: Mollienesia)

Divergence in mating signals is a primary factor leading to reproductive isolation, and thus, speciation. However, the genetic changes underlying such divergence are poorly understood, especially in vertebrates. We used two species of poeciliid fishes, Poecilia velifera and P. mexicana , to explore the link between genes and mating behaviors that has resulted in pre-mating reproductive isolation between these species. Using backcross hybrids created from the F1 male offspring of reciprocal interspecific crosses between a sailfin molly ( P. velifera ) and a shortfin molly ( P. mexicana ), we examined the effects of Y-linkage and autosomal contributions on the expression of two male mating behaviors: courtship displays and gonopodial thrusts. The F1 hybrid males displayed a strong influence of sire on courtship display rates, with F1 males sired by the sailfin species showing courtship display rates that were up to three times higher than the rates of displays performed by F1 males sired by the shortfin species. These results suggest a Y-linked genetic effect on the expression of courtship display behavior. Comparisons between backcross hybrid males with sailfin Y-chromosomes or shortfin Y-chromosomes suggested that the interaction of autosomal genes also influences the inheritance of courtship display rates. Sailfin autosomal genes significantly increased the probability of performing courtship displays for hybrid males, and increased display rate for males from the sailfin Y-chromosome line. Autosomal genes had less of an impact on gonopodial thrusting behavior, however, thrust rates did significantly decrease with an increasing proportion of sailfin autosomes in males from the shortfin Y-chromosome line. These results suggest that the inheritance of species differences in mating signals between shortfin and sailfin mollies involves both genes found on the Y-chromosome and autosomal gene influences on their expression.     

Mating behavior of Aegla platensis (Crustacea, Anomura, Aeglidae) under laboratory conditions

The mating behavior of several decapod crustaceans has been extensively studied; however, this aspect of anomuran biology is still poorly known in some groups. Aeglids are the only anomurans inhabiting freshwaters, and the mating behavior of the species in this family is unknown. We provide the first account of the mating behavior of an aeglid, Aegla platensis, under laboratory conditions. The precopulatory phase was characterized by male agonistic display, male approach, and courtship. Males exhibited the agonistic display toward immature and mature females, but only physiologically mature females allowed males to approach. Male approach led to display of courtship behaviors (body vibration, thrust, body lifting, and abdomen flapping). During the copulatory phase, males and females touched each other with the antennae (antennae touch), and males positioned themselves beneath the females (supine position). Although sperm transfer was not directly observed, a “white mass” was detected among oocytes in the female abdominal chamber shortly after some copulations. Finally, in the postcopulatory phase, males guard females during the process of egg attachment. Despite their morphological similarities with other anomurans, the mating behavior of aeglids seems to be unique, and the freshwater environment appears to have an important role in driving these differences.     

Unravelling the evolution of complex reproductive traits with phenotypic engineering

The social dynamics surrounding courtship, mating and parental care are complex enough when just a single male and female are involved, but for species that employ multiple strategies for achieving fertilization success, the network of interactions among rivals, allies and suitors can be utterly complicated. Such is the case in the ocellated wrasse, Symphodus ocellatus, in which males adopt one of three mating strategies. The large, colourful “nesting males” court females, defend territories and care for fertilized eggs until they hatch. The smaller “satellite males” help the nesting males court females and guard against the third morph, the “sneaker males”, which sneak in when a nesting male is spawning with a female and surreptitiously release sperm. Sneaker males perform no courtship displays nor defend territories, so their reproductive investment is devoted entirely to sperm production. And these alternative male strategies work: 100% of nests contain some eggs fertilized by sneaker and satellite males, despite the fact that parental care is solely the responsibility of nesting males In this issue of Molecular Ecology, work to untangle the proximate mechanisms regulating the reproductive physiology of nesting males and their behaviour towards other males, which impacts the entire social network. Moreover, they describe how variation in neuroendocrine regulation can give rise to variation in reproductive traits, upon which sexual selection can act.