Dissecting the mechanisms underlying old male mating advantage in a butterfly

Selection is expected to maximize an individual’s own genetic reward regardless of the potential fitness consequences for its sexual partners, which may cause sexual conflict. Although performance in holometabolous insects typically diminishes with age, old male mating advantage has been documented in a few species. Whether this pattern arises from female preference for older males based on, e.g., pheromone blends (intersexual selection), or from increased eagerness to mate in older compared to younger males is currently debated. We explore the mechanistic basis of old male mating advantage, using a series of experiments including behavioral as well as manipulative approaches, in the tropical butterfly Bicyclus anynana. Consistent with the residual reproductive value hypothesis, old male mating advantage was associated with a greater eagerness to mate, evidenced by a two times higher flying and courting activity in older than in younger males. In contrast, we found only limited support for a contribution of female preference for older males based on pheromone composition, although male sex pheromones clearly do play a role in mating success. Our results suggest that male behavior may play a primary role in old male mating advantage, and that pheromones are likely of secondary importance only. Male mating success was related to higher overall pheromone titers rather than variation in a single component. A dominant importance of male behavior in determining mating success may result in sexual conflict.     

Sequential male mate choice in a fish,the Pacific blue-eye<Emphasis Type="Italic"> Pseudomugil signifer</Emphasis>

Mate choice is not just a female preoccupation. Under some circumstances, males may also be choosy. However, studies of male mate choice have generally been confined to situations where males can make direct comparisons between potential partners. In contrast, sequential male mate choice has largely been overlooked despite its biologically importance, especially if current investment in mate attraction diminishes a males future mating opportunities. Using the Pacific blue-eye fish Pseudomugil signifer, we show that males are capable of exercising sequential mate choice. When presented sequentially with large and small females, males spent more effort courting the former. However, males did not appear to modify the time spent courting a given female based on the size of the female encountered previously. We suggest that greater attention to the sequential choice problem in males may help illuminate similarities and differences between the sexes when it comes to mating decisions.Communicated by T. Czeschlik     

Experience counts: females favor multiply mated males over chemically endowed virgins in a moth (<Emphasis Type="Italic">Utetheisa ornatrix</Emphasis>)

Determining the factors that affect male mating success is essential to understanding how sexual selection operates, including explanations of the adaptive value of female preferences and how variation in male traits is maintained in a population. Although females may appear to choose males based on a single parameter, female mate choice is often a complex series of assessments of male quality that can only be revealed through manipulation of multiple male traits. In the moth Utetheisa ornatrix (Lepidoptera: Arctiidae), females have been shown to judge males primarily on their production of a courtship pheromone, hydroxydanaidal, derived from defensive chemicals acquired as larvae. Recent work, however, suggested that other factors, including prior mating experience by males, may also influence the outcome of precopulatory interactions with females. I ran mating trials with one female and two males to determine whether there were any differences in male mating success based on their prior exposure to females, mating experience, and time between matings. Previously mated males were favored over virgins when both males lacked the pheromone, but courting experience and mating interval did not explain these differences in male mating success. Furthermore, multiply mated males lacking the pheromone were favored over virgin males that produced the pheromone, thus reversing the commonly observed trend of female precopulatory bias towards males with higher levels of the pheromone. These results demonstrate that males with mating experience can secure copulations despite deficiencies in the pheromone, and I provide possible mechanisms and discuss their implications regarding sexual selection.     

Multiple mating in a lekking bird: why do peahens mate with more than one male and with the same male more than once?

Summary Approximately 50% of marked peahens (Pavo cristatus) mate more than once with lek males. Some females mate with more than one male, others copulate repeatedly with the same male. The frequency of courtship also shows marked variation. Some females repeatedly engage males in courtship interactions after they have succesfully copulated with them. The likelihood of mating with more than one male increases if a female first mates with a non-preferred (unsuccessful male). There is a non-significant tendency for females to copulate with a more successful male when remating. Peahens may mate with a non-preferred male first if they do not encounter a successful male during their initial period of choice, perhaps because the most successful male on a lek was courting another female and/or was defended by another female. There are more aggressive interactions between females in front of preferred males. Preferred males receive more repetitive courtship behaviour and repeated matings. Dominant females are more likely to engage in repetitive courtship and matings. The number of times a female initiates courtship on any one day increases with the number of other females actively courting males at a lek site on that day. We suggest that there is competition amongst females for access to preferred males and that dominant females try to monopolise these males by repeatedly engaging them in courtship interactions. We discuss the implications of these observations for the idea that female may gain directly from mate choice in a species where males contribute nothing but gametes to their offspring. Correspondence to: M. Petrie at the present address     

Vocalizations by Alaskan moose: female incitation of male aggression

Evidence of female fomentation of male–male aggression as a mechanism of mate choice is rare, especially in mammals. Female choice of mates in polygynous species may be masked by intense male competition or by males attempting to restrict female choice. We studied protest moans of female Alaskan moose Alces alces gigas in interior Alaska, USA, from 1987 to 1990, to determine if moans incited male–male aggression. Alaskan moose exhibit a mating system in which one dominant male (the harem master) herds, defends, courts, and attempts to mate with females in his harem. Protest moans were given by females only in response to courtship. We hypothesized that if protest moans were related to females reducing harassment and exercising mate choice, females should give protest moans more frequently when courted by small males and less often when courted by large males, and that rates of male–male aggression would be elevated following protest moans. Harems were composed of one large male, with a mean of 4.4 females (median = 3 females); 10% of 132 harems included ≥10 females. The temporal pattern of protest moans from late August through November was associated with, but tended to lag behind, mating behavior. The rate of protest moans given by females decreased with increasing size of males courting them. Male–male aggression was significantly less during periods without protest moans than during periods in which protest moans occurred. These results indicate that female moose gave protest moans to reduce harassment by smaller males, and assure a mating opportunity with the most dominant male. Such a subtle mechanism of indirect mate choice by females may occur in other vertebrates in which choice is limited by a mating system in which male–male combat and male dominance over females reduces opportunities for female choice. The importance of female choice may be undervalued in studies of sexual selection in mammals.     

Costs of courtship and mating in a sexually cannibalistic orb-web spider: female mating strategies and their consequences for males

The costs of courtship and mating may include increased risks of predation, the transmission of pathogens, and a loss of foraging opportunities. Thus, a female's decision to tolerate a courting male will depend upon how these costs offset the benefits of mating, which will depend on her reproductive and nutritional status. While these costs may be similar for mated and unmated females, the benefits of mating will be less for mated than virgin females. However, the cost of lost foraging opportunities may be higher for females with fewer nutritional reserves necessary for forming eggs. We examined how these costs and benefits influence the courtship and mating behaviour of male and female orb-web spiders, Argiope keyserlingi. In the field, females on webs that also contained a courting male intercepted fewer prey items per hour than females on webs without a male. In the laboratory, the presence of a courting male at the hub also attracted mantid predators to the web, increasing the risk of predation for both male and female. Staged mating experiments in the laboratory revealed that the frequency of female attacks and pre-copulatory cannibalism was greater among mated than virgin females. Feeding history did not affect aggression in virgin females but, among mated females, food-deprived spiders attacked and cannibalized males more frequently than sated females and only the latter ever remated. These differences in female behaviour influenced male mating strategies. Choice experiments demonstrated that males preferred to venture onto the silk threads of virgin rather than those of mated females. Similar patterns of mate selectivity were observed in the field; females with narrow abdomens attracted more males to the webs than females with broad abdomens, and copulations were observed more frequently among females with narrow abdomens. These smaller females are likely to be virgins that have recently molted. Males that preferentially mate with virgin females will not only avoid potentially fatal attacks but also obtain, on average, a higher fertilization success.     

Effect of female molt stage and sex ratio on courtship behavior of the blue crab Callinectes sapidus

In many species, males and females actively participate in courtship, and the outcome of pre-mating interactions influences the mating success of both sexes. Female blue crabs, Callinectes sapidus, mate soon after their final molt to maturity; thus female molt stage dictates the timing of mating. In a field experiment, we manipulated female molt stage and sex ratio to test their effects on the courtship behavior of both sexes, if female behavior influences the behavior and pairing success of males, and if male courtship influences male pairing-success. Early-molt-stage females avoided males during courtship, whereas late-molt-stage females sought out males. As a result, males had to pursue and capture early-molt-stage females whereas males displayed to late-molt-stage females and more easily physically controlled them. Males sometimes abandoned late-molt-stage females, but this occurred more often when females were abundant. The rate at which females avoided males was positively correlated with that of males abandoning females, and males that were unsuccessful at pairing met with higher rates of female resistance than successful males, suggesting that female behavior influences male pairing-success. Unlike unsuccessful males, successful males more often made the transition between display and maintaining physical control of the female. At high male sex ratios, males initiated courtship more readily; thus both sexual competition and female behavior influence male courtship in this species. Received: 7 July 1996 / Accepted: 10 January 1998     

Repeatable female preferences, mating order and mating success in the poeciliid fish, Heterandria formosa

Sexual selection via female choice can afford preferred males comparably higher mating success than those males that lack preferred traits. In addition, many models of sexual selection assume that both male traits and female preferences are heritable. In this study we test whether females of the poeciliid fish, Heterandria formosa, have repeatable pre-copulatory preferences for larger males. We also test whether female pre-copulatory preferences are always reliable indicators of male mating success. When given a choice between a large and a small male, females prefer larger males, and the repeatability of this preference is high. Although there are no overall differences in male mating success between large and small males, large males have a higher mating success when they are the first to mate than when they are the second to mate. Likewise, preferred males also have higher mating success when they are the first to mate than when they mate second. Therefore, the repeatable female preferences observed in this study only predict male mating success when the preferred male mates first. These results illustrate that even significantly repeatable female preferences do not translate into male mating success, which is an assumption of many examinations of the importance of female choice in sexual selection.     

Phenotypic differentiation in female preference related to geographic variation in male predation risk in the Trinidad guppy (Poecilia reticulata)

Summary Populations of the Trinidad guppy range from areas with high levels of predation by other species of fish to areas with little or no piscine predation. Previous studies have shown that variation among populations in male coloration can be explained by a balance between female preference for brighter males and natural selection against bright males. High levels of male courtship activity may also increase both predation risk and mating success. Therefore, in high-predation areas, females that mate with males that court frequently as well as those that choose bright males would presumably produce male offspring with low survivorship. Consistent with this variation in natural selection, we observed that females from high-predation populations were less likely to choose bright and frequently courting males than females from low-predation populations. This result supports the hypothesis that female preference is evolving as a character genetically correlated with the preferred male character, in which case higher levels of natural selection acting against the male character should be related to lower levels of female preference.     

The assessment of female reproductive state during courtship and scramble competition in the fiddler crab, Uca paradussumieri

Male fiddler crabs, Uca paradussumieri, mate underground during a 4- to 7-day period each full and new moon. As soon as the tide recedes, males enter the burrows of females that will ovulate the following day ('pre-ovigerous' females). Males copulate with and guard these females until they ovulate. When interrupted by an intruding male, the first male to reach the female is usually able to defend her and successfully mate with her. In fiddler crabs, females mate multiply and there is last male sperm precedence. Before each semi-lunar mating period, male U. paradussumieri were more likely to court females with whom they would later mate than other nearby females with whom they did not mate. This suggests that males collect information on female reproductive state prior to the females becoming ovigerous. In this species, aggression was common between males that courted the same female. When previously courted females were approached by other males, the initial courter attempted to forcefully disrupt the courtship. This behavior may allow males the exclusive use of information on female reproductive condition. It also suggests a type of scramble competition between males over females. Furthermore, it indicates that males are able to locate receptive females prior to their becoming ovigerous. The shorter guarding period observed in this species, as compared with other fiddler crabs, is caused by females rejecting longer guarding periods. Male ability to assess female reproductive status may therefore be advantageous because it increases male mating success within a scramble type of competitive polygyny.     

A female preference for experienced males in the almond moth, Cadra cautella

Male mating status can affect female reproductive output if male ejaculate investment declines over consecutive matings. Accordingly, females are predicted to mate preferentially with virgin males. In mildly polyandrous lepidopterans, female fitness is less affected by reduced male investment than in more polyandrous species, and so the predictions for female mating preferences are less clear. We examined female mating preferences in the mildly polyandrous almond moth, Cadra cautella, in which ejaculate size does not affect female reproductive output. First, we allowed females to mate with virgin or once-mated males, in which the males were presented individually or simultaneously. We recorded the latency to mating and, in the case of the simultaneously presented trials, the identity of the successful, copulating male. We found that females mated more frequently with mated males (when simultaneously presented with both males), yet females did not differ in the time taken to initiate copulation with any male. We further examined if this mated male advantage was due to differential mate detection or locomotory behaviour of the male treatments. We tested the ability of virgin and mated males to locate a receptive female within a wind tunnel using long-distance pheromone cues and recorded their activity budget. We found no difference in the ability of mated or virgin males to locate or approach a receptive female, or in their activity levels. These data suggest a female preference for mated males in this species, a preference that may minimise other potential costs of mating.     

Responses of female lizards,<Emphasis Type="Italic"> Lacerta monticola</Emphasis>, to males' chemical cues reflect their mating preference for older males

Female mate choice based on visual traits appears to be rare in lizards. Field observations suggest that females of the lizard Lacerta monticola preferred to mate with larger/older males. Although older males are usually green and larger, and younger males brown and smaller, there is some overlap in size and coloration between age classes. Thus, visual cues may not always be reliable indicators of a male's age. We hypothesized that female mate-choice preferences may be based on males' pheromones, which might transmit information about characteristics such as age. In a laboratory experiment, we analyzed the effect of age of males on attractiveness of their scents to females. When we offered scents of two males of different age, females associated preferentially with scents of older males. This suggested that females were able to assess the age of males by chemical signals alone, and that females preferred to be in areas scent-marked by older males. Thus, females may increase their opportunities to mate with males of high quality, or may avoid harassment by sneaking young males. This result agreed with field observations on females mating with old males, and rejection of advances by young males. Our results also suggested that female preference for older males may depend on their own body size. Large females showed a strong preference for older males, whereas smaller females were not so selective. This, together with males' preference for large females, might lead to size-assortative matings. We suggest that the quality and/or quantity of male pheromones could communicate to the female heritable male genetic quality (i.e. age) and thereby serve as the basis of adaptive female choice in lizards.Communicated by W.E. Cooper     

Sex ratios,mating behavior and sexual size dimorphism of the northern water snake,Nerodia sipedon

Competition among males to mate is generally associated with male-biased size dimorphism. In this study we examine mating behavior in the northern water snake (Nerodia sipedon), a species in which males are much smaller than females despite substantial competition among males to mate. Competition among males was a consequence of a male-biased operational sex ratio due to slightly higher female mortality from a birth sex ratio of 1 : 1, and, in 1 year, more synchronous and longer mating activity by males. Approximately one-third of both males and females appeared not to mate in a given year. Larger males were generally more likely to attempt mating, but size did not explain the variance in the number of aggregations in which individual males participated. Within aggregations, males that were successful at achieving intromission were larger than unsuccessful males in 1 of 2 years. Variation in condition (mass relative to length) and relative tail length were not generally useful predictors of either mating effort or success in males. Because large size was often advantageous to males, sexual size dimorphism appeared not to be a consequence of sexual selection favoring smaller males. Because sexual dimorphism was evident at birth, and both males and females matured sexually at about 4 years, sexual dimorphism was not simply a consequence of one sex growing at the maximum rate for longer. Female fecundity increased with size, and sex differences in size-fecundity relations may underly the pattern of sexual size dimorphism. However, because multiple mating by females is common, sperm competition is likely to be important in determining male reproductive success. Therefore, allocation of energy to sperm rather than growth may also prove to be an important influence on male growth rates and sexual size dimorphism.     

Selection for early emergence, longevity and large body size in wingless, sib-mating ant males

Sexual selection has led to male morphologies and behaviours that either increase male attractiveness or their success in male–male competition. We investigated male traits under selection in the ant Hypoponera opacior, in which wingless males mate with pupal queens inside their natal colony and guard their partners for hours. The lack of female choice and fights among adult males makes this species an ideal study system to investigate sexual selection in the absence of these selective forces. We hypothesised that males, which emerge first and live longer, should have a higher mating success because of more mating opportunities, reduced competition and the ability to kill pupal competitors. We recorded the number and length of matings and tested whether these measures of male-mating success were associated with emergence order, lifespan and body size. Indeed, early emerged males mated more often and longer than their later-emerging rivals. Furthermore, longer-lived and larger males obtained more matings. Body size might be important because larger males either produce more sperm or perform better in mounting females. We found no evidence for a trade-off between body size and emergence time. Moreover, male removal manipulations revealed that males quickly adapt their guarding behaviour to changes in the competitive environment. Under reduced competition, males guarded their partners for shorter periods. In conclusion, these sib-mating ant males are under selection to develop fast, to live long, to be large and to be able to respond to the competitive situation in the nest.     

Prior encounters with the opposite sex affect male and female mating behavior in a wolf spider (Araneae,Lycosidae)

Mate availability can vary widely in nature depending upon population density and sex ratio and can affect the ability of individuals to be selective in mate choice. We tested the effects of prior encounters with the opposite sex (i.e., exposure to the opposite sex either with or without mating) on subsequent mating behavior in two experiments that manipulated mate availability for both males and females in the wolf spider, Hogna helluo. The probability of mating in the experimental trial depended upon whether the prior encounter involved mating or not, and males and females responded in opposite directions. Exposure without mating resulted in a higher subsequent frequency of mating for females and a lower subsequent frequency of mating for males, while prior mating experience resulted in a lower frequency of female remating and a higher frequency of male remating. Prior exposure without mating did not affect female aggression. However, mated females engaged in precopulatory cannibalism more frequently than virgins. Mated males escaped postcopulatory cannibalism more frequently than virgins. Our results show that males respond to exposure without mating in the expected manner. However, prior mating (1 week earlier) had unexpected effects on males, which may be due to mated males being of higher quality. There were little or no effects of the size of the prior exposure individual or mate on subsequent mating behaviors. Further research is needed to determine why different species use different degrees of prior information in mate choice.     

Fighting success and attractiveness as predictors of male mating success in the black field cricket, Teleogryllus commodus: the effectiveness of no-choice tests

Females are generally assumed to prefer larger, more dominant males. However, a growing number of studies that control for male-male competition have shown no correlation between dominance and attractiveness. Aggressive males can interfere with female mate preference either by physically coercing females into mating or by driving submissive males away and restricting mate choice. The most common method of assessing female mate choice is by using simultaneous two-choice tests. These control for male-male interactions, but usually interfere with physical and chemical cues involved in mate selection or alter male behaviour. They are therefore unsuitable for many study species, especially insects. Another method is the no-choice test that measures a females latency to mating when placed with a single male as an indication of male attractiveness. No-choice tests control for male-male aggression while allowing full contact between pairs (they allow actual mating to be directly observed rather than to occur based on a correlated behaviour). So far, however, no study has confirmed that males that entice females to mate sooner actually enjoy increased longer-term mating success. As such, the accuracy of no-choice tests as a method of examining mate choice remains untested. Here, we used no-choice tests on the black field cricket, Teleogryllus commodus, to show that (1) females did not prefer males that won fights (dominant males), and (2) latency to mating predicts actual mating success. We have clearly demonstrated the usefulness of no-choice tests and, considering the advantages of this method, they should be more often considered for a wider variety of taxa.Communicated by D. Gwynne     

Age-related female mating decisions are condition dependent in wolf spiders

Female mating behaviors are known to be sensitive to a variety of individual factors both external and internal to a female; however, mating decisions are likely due to a suite of interacting factors. By independently manipulating female and male diet in the wolf spider Rabidosa rabida and testing females across age groups, we demonstrate that, in addition to its independent effect, female nutritional condition interacts with female age to influence female mating behavior. Overall, high-quantity diet (HD) females were more likely to mate than low-quantity diet (LD) females. Within the LD females, older individuals were more likely to mate than younger individuals, while within HD females, mating probabilities were equal across females of different age classes. With respect to mate choice, only female age influenced the likelihood of mating based on male diet. Young females were choosier as they were more likely to mate with HD males than LD males; in contrast, older females were equally likely to copulate with males of each diet treatment. In addition, the likelihood of pre-sexual cannibalism was dependent on both female and male diet. High-quantity diet females were more likely to cannibalize than LD females, and attacks were directed towards LD males most often. We discuss our results in terms of costs versus benefits of female mate choice.     

Scramble competition polygyny in thirteen-lined ground squirrels: the relative contributions of overt conflict and competitive mate searching

Summary The scramble competition polygyny of male thirteen-lined ground squirrels involves overt conflict and sperm competition as well as competitive mate searching. The overt conflict component of intrasexual competition occurs sporadically: males sometimes are able to mate in the complete absence of competitors, while on other occasions up to five other males may be present. We examined the immediate effects of conflict on male mating behavior, and found that it increases the time spent in pursuit of an estrous female, reduces the efficiency of copulating, but carries only a small risk of exclusion from mating. In contrast to some other sciurid species, dominance appears to be a poor predictor of the mating success of male thirteen-lined ground squirrels. However, skill at locating females is very important. Because overt conflict seldom results in exclusion from mating opportunities, and because females of this species accept multiple mates, success in copulating conforms closely with success in mate searching: the sheer number of estrous females located is a consistently strong predictor of male mating success. Furthermore, individual differences in mate location ability seem to generate levels of variance in male copulatory success that are comparable to those of more combative species.     

Rhythmic male reproductive behavior controls timing of courtship and mating in Laupala cerasina

In many organisms, mating behavior occurs at a particular time of day, which may be important for avoiding mate competition or interspecific mating. Crickets of the Hawaiian genus Laupala exhibit an unusually protracted courtship in which males produce a series of nuptial gifts prior to the species-typical time of mating. Mating time is one of several rhythmic behaviors that have diverged among closely related Laupala species, which exhibit an extremely high speciation rate. Mating rhythm may reflect direct selection on male and/or female sexual receptivity or the pleiotropic consequence of selection on other rhythmic behaviors. To examine the role of sexual rhythmicity in Laupala cerasina, we characterized the time boundaries or “circadian gate” of courtship and mating, as well as female phonotactic response to male song. We also examined which sex is responsible for mating rhythmicity by phase-shifting males relative to the female photophase. Our results demonstrate that mating behavior is gated by the end of the light phase. Time limits to female mating receptivity were not observed and thus male rhythm alone appears to be responsible for the timing of mating. Furthermore, when courtship is initiated later in the day, males produce fewer nuptial gifts and increase nuptial gift production rate while delaying mating, suggesting that the number of gifts a female receives is important to male reproductive success.     

Black Grouse leks on ice: Female mate sampling by incitation of male competition?

Male-male competition is assumed to limit female choice of mates, but it may also help females to choose the most vigorous males. We studied the mate sampling behaviour of female black grouse (Tetrao tetrix) at spatially unstable leks on ice-covered lakes. In the absence of territories and site-dependence in outcomes of fights, the male dominance hierarchy is very evident on ice. When being courted by dominant males, females frequently tried to approach other males. This was frequently prevented because (1) the courting male and the approached male were involved in physical fight, or (2) the dominant male followed the female and the approached male escaped and avoided contact with him. These behaviours express dominance relationships, and the female behaviour could be considered as incitive. Rank in dominance hierarchy was a significant predictor of male mating success. In this case competition between males and female choice worked in parallel favouring male traits correlated with dominance.