Male Mating History Influences Female Mate Choice in the Trinidadian Guppy (Poecilia reticulata)

Based on the phenotype‐linked fertility hypothesis, sexual selection should favour females that can accurately assess the recent mating history of available sexual partners and preferentially avoid mating with recently‐mated males [who may be sperm depleted (SD)] so as to minimize the risk of their eggs not being fertilized. This hypothesis has received to date only limited attention and empirical support. Therefore, in the current study, we investigated experimentally whether females of a vertebrate species, the Trinidadian guppy (Poecilia reticulata), are able to assess the recent mating history of males, and thus potentially their functional fertility, and choose to avoid mating with males that appear to have recently mated and who may be sperm limited. Individual virgin females were first given a dichotomous choice between a male that had not been recently observed to interact sexually with another female (i.e. not sperm‐depleted) and another male that had been observed to interact sexually with a female (i.e. potentially sperm‐depleted) as sexual partners. Paired males were matched for body length and coloration. Immediately following this test, the focal females were subjected to a free‐swimming mate‐choice test using the same paired stimulus males. As predicted, on average, female guppies avoided the apparently recently‐mated (and potentially sperm‐depleted) male and exhibited a significant preference for the other male not recently observed mating (and thus not likely sperm limited) during both tests. We do not yet fully understand the underlying mechanisms of this preference. Therefore, further research on the particular cues that females use to assess the recent mating history and fertility status of males is required.     

Male mate choice in the chameleon grasshopper (Kosciuscola tristis)

In many species, males can increase their fitness by mating with the highest quality females. Female quality can be indicated by cues, such as body size, age and mating status. In the alpine grasshopper Kosciuscola tristis, males can be found riding on subadult females early in the season, and as the season progresses, males engage in fights over ovipositing females. These observations suggest that males may be competing for females that are either unmated (early season) or sperm‐depleted (late season). We thus hypothesised that male K. tristis may be choosy in relation to female mating status, and specifically, we predicted that males prefer females that are unmated. We conducted behavioural experiments in which males were given the choice of two females, one mated and one unmated. Contrary to our prediction, males did not mate preferentially with unmated females. However, copulation duration with unmated females was, on average, 24 times the length of copulation with mated females. While female K. tristis can reject mates, we did not observe any evidence of overt female choice during our trials. Females may gain additional benefits from mating multiply and may therefore not readily reject males. While our experiment cannot definitively disentangle female from male control over copulation duration, we suggest that males choose to invest more time in copula with unmated females, perhaps for paternity assurance, and that male mate assessment occurs during copulation rather than beforehand.     

Detection of female mating status using chemical signals and cues

Males of many species choose their mate according to the female's reproductive status, and there is now increasing evidence that male fitness can depend on this discrimination. However, females will also aim to regulate their mating activity so as to maximize their own fitness. As such, both sexes may attempt to dictate the frequency and timing of female mating, reflecting the potentially different costs of female signaling to both sexes. Here, I review evidence that chemical cues and signals are used widely by males to discriminate between mated and unmated females, and explore the mechanisms by which female odour changes post‐mating. There is substantial empirical evidence that mated and unmated females differ in their chemical profile, and that this variation provides males with information on a female's mating status. Although there appears to be large variation among species regarding the mechanisms by which female odour is altered post‐mating, the transfer of male substances to females during or subsequent to copulation appear to play a major role. This transfer of substances by males may be part of their strategy to suppress reproduction by competing males, particularly in species where females mate more than once.     

Reproductive costs of mating with a sibling male: sperm depletion and multiple mating in Cephalonomia hyalinipennis

Polygynous parasitoid males may be limited by the amount of sperm they can transmit to females, which in turn may become sperm limited. In this study, I tested the effect of male mating history on copula duration, female fecundity, and offspring sex ratio, and the likelihood that females will have multiple mates, in the gregarious parasitoid Cephalonomia hyalinipennis Ashmead (Hymenoptera: Bethylidae: Epyrinae), a likely candidate for sperm depletion due to its local mate competition system. Males were eager to mate with the seven females presented in rapid succession. Copula duration did not differ with male mating history, but latency before a first mating was significantly longer than before consecutive matings. Male mating history had no bearing on female fecundity (number of offspring), but significantly influenced offspring sex ratio. The last female to mate with a given male produced significantly more male offspring than the first one, and eventually became sperm depleted. In contrast, the offspring sex ratio of first‐mated females was female biased, denoting a high degree of sex allocation control. Once‐mated females, whether sperm‐depleted or not, accepted a second mating after a period of oviposition. Sperm‐depleted females resumed production of fertilized eggs after a second mating. Young, recently mated females also accepted a second mating, but extended in‐copula courtship was observed. Carrying out multiple matings in this species thus seems to reduce the cost of being constrained to produce only haploid males after accepting copulation with a sperm‐depleted male. I discuss the reproductive fitness costs that females experience when mating solely with their sibling males and the reproductive fitness gain of males that persist in mating, even when almost sperm‐depleted. Behavioural observations support the hypothesis that females monitor their sperm stock. It is concluded that C. hyalinipennis is a species with a partial local mating system.     

Mating with sperm-depleted males does not increase female mating frequency in the parasitoid Lariophagus distinguendus

Sexual conflicts due to divergent male and female interests in reproduction are common in parasitic Hymenoptera. The majority of parasitoid females are monandrous, whereas males are able to mate repeatedly. Thus, accepting only a single mate might be costly when females mate with a sperm‐depleted male, which may not transfer a sufficient amount of sperm. In the present study, we investigated the reproductive performance in the parasitoid Lariophagus distinguendus Först. (Hymenoptera: Pteromalidae) and studied whether mating with experimentally sperm‐depleted males increases the tendency of females to remate. Males were able to mate with up to 17 females offered in rapid succession within a 10‐h test period. The resulting female offspring, as an indirect measure of sperm transfer, remained constant during the first six matings and then decreased successively with increasing number of copulations by the males. Experimentally sperm‐depleted males continued to mate even if they transferred only small amounts or no sperm at all. Unlike males, the majority of females mated only once during a 192‐h test period. A second copulation was observed only in a few cases (maximum 16%). The frequency of remating was not influenced by the mating status of the first male the females had copulated with, suggesting that these events are not controlled by sperm deficiency of the females. Furthermore, we investigated male courtship behaviour towards mated females. Male courtship intensity towards mated females decreased with increasing time. However, females that had mated with an experimentally sperm‐depleted male did not elicit stronger or longer‐lasting behavioural responses in courting males than those that had mated with a virgin male. As the observed behaviours in L. distinguendus are known to be elicited by a courtship pheromone, these results suggest that females no longer invest in pheromone biosynthesis after mating (as indicated by ceasing behavioural responses of courting males), irrespective of whether they have received a sufficient amount of sperm or not. We discuss the results with respect to a possible mating strategy of sperm‐depleted males.     

Premating Avoidance of Inbreeding Absent in Female Guppies (Poecilia reticulata)

The recognition and avoidance of kin during mating can be an important means of reducing the potential for inbreeding depression in offspring. We report here that premating mechanisms to avoid inbreeding, either innate or learnt through juvenile experience, are at best weak in female guppies (Poecilia reticulata). Guppies are small, ovoviviparous, neo‐tropical freshwater fish, with a polygamous mating system where males actively court females and females are selective of their mates. In a series of mate‐choice experiments, naïve, virgin females of the Quare River population in Trinidad were given a choice between a brother and a non‐sib male from the same population. Initially, females were only provided olfactory cues upon which to base their choice and then subsequently both olfactory and visual cues. Despite the females displaying mate choice, we found no evidence of them discriminating between the male types in either experiment. There was thus no indication of inbreeding avoidance, suggesting that experiences after maturation or with mature males (e.g. rare male preference), dispersal and/or post‐mating mechanisms may be evolutionarily more important avoidance mechanisms.     

Effects of sequential mating by males on reproductive output of the stinkbug predator, Podisus nigrispinus

Reproductive output of the stinkbug predator Podisus nigrispinus (Dallas) (Heteroptera: Pentatomidae) was investigated as a function of the number of matings that the male had made with a range of females. After being placed with a female, virgin males were most likely to mate within 12 hours, while non-virgin males were most likely to mate within 12–24 hours. Although males lost weight during their first mating, the weights of mated and unmated males were not significantly different throughout their lifetime. Longevity was significantly greater for unmated males (36.0 days) than for mated males (29.8 days). Survival curves for both mated and unmated males were Type II. The capacity of males to transfer sperm to virgin females was not affected by previous matings. From 65.7 to 76.4% of eggs were viable and 206.7 to 274.6 nymphs were produced per female. Regardless of the number of matings that the male had made, females that had mated only once exhausted their stored sperm progressively and produced an increasing proportion of infertile eggs, which peaked at the end of their lives. These results show that P. nigrispinus females need more than one mating to maintain fertility, but their performance is not affected by the number of previous matings that the male has made or by male weight. Thus, the strategy of pairing with males multiple times improved production efficiency by increasing output and reducing food waste in mass production systems. This is achieved by temporarily pairing females at intervals of about 20 days during their entire lifetime.     

Female mating status affects male mating tactic expression in the wolf spider Rabidosa punctulata

Males and females have conflicting interests on the frequency and outcomes of mating interactions. Males maximize their fitness by mating with as many females as possible, whereas choosy females often reduce receptivity following copulation. Alternative male mating tactics can be adaptive in their expression to a variety of mating contexts, including interactions with a relatively unreceptive mated female. Male Rabidosa punctulata wolf spiders can adopt distinctive mating tactics when interacting with a female, a complex courtship display, and/or a more coercive direct mount tactic that often involves grappling with females for copulation. In this study, we set up female mating treatments with initial trials and then paired mated and unmated females with males to observe both female remating frequencies and the male mating tactics used during the interactions. Males adopted different mating tactics depending on the mating status of the female they were paired with. Males were more likely to adopt a direct mount tactic with already-mated females and courtship with unmated females. Already-mated females were considerably less receptive to males during experimental trials, although they did remate 34% of the time, the majority of which were with males using a direct mount tactic. Whereas males adjusting to these contextual cues were able to gain more copulations, the observation of multiple mating in female R. punctulata introduces the potential for sperm competition. We discuss this sexual conflict in terms of the fitness consequences of these mating outcomes for both males and females.     

Sex differences in dogfish behaviour: alternative activity patterns and habitat choice

Guppies are highly sexually dimorphic and females have been shown to mate preferentially with males with various visible traits. Guppies, however, have been shown to respond behaviourally to odour cues from conspecifics. Using a specially designed olfactory choice tank, we tested whether females (1) could detect other guppies on the basis of their olfactory cues alone, (2) preferred to associate with males or with females and (3) could distinguish between different males. Female guppies were found to associate preferentially with other guppies when given a choice between water containing cues from another fish and water containing no cues. When females were presented with olfactory cues from a male or a female, they preferred the female initially but most then reversed their decision and swam to the male. Females associated preferentially with certain males based upon olfactory cues alone. Males, however, preferred on the basis of olfactory cues were the least preferred for visual cues.     

Female preferences based on olfactory cues in the guppy (Poecilia reticulata)

Guppies are highly sexually dimorphic and females have been shown to mate preferentially with males with various visible traits. Guppies, however, have been shown to respond behaviourally to odour cues from conspecifics. Using a specially designed olfactory choice tank, we tested whether females (1) could detect other guppies on the basis of their olfactory cues alone, (2) preferred to associate with males or with females and (3) could distinguish between different males. Female guppies were found to associate preferentially with other guppies when given a choice between water containing cues from another fish and water containing no cues. When females were presented with olfactory cues from a male or a female, they preferred the female initially but most then reversed their decision and swam to the male. Females associated preferentially with certain males based upon olfactory cues alone. Males, however, preferred on the basis of olfactory cues were the least preferred for visual cues.     

Generalization of courtship learning in Drosophila is mediated by cis-vaccenyl acetate

Reproductive behavior in Drosophila has both stereotyped and plastic components that are driven by age- and sex-specific chemical cues. Males who unsuccessfully court virgin females subsequently avoid females that are of the same age as the trainer. In contrast, males trained with mature mated females associate volatile appetitive and aversive pheromonal cues and learn to suppress courtship of all females. Here we show that the volatile aversive pheromone that leads to generalized learning with mated females is (Z)-11-octadecenyl acetate (cis-vaccenyl acetate, cVA). cVA is a major component of the male cuticular hydrocarbon profile, but it is not found on virgin females. During copulation, cVA is transferred to the female in ejaculate along with sperm and peptides that decrease her sexual receptivity. When males sense cVA (either synthetic or from mated female or male extracts) in the context of female pheromone, they develop a generalized suppression of courtship. The effects of cVA on initial courtship of virgin females can be blocked by expression of tetanus toxin in Or65a, but not Or67d neurons, demonstrating that the aversive effects of this pheromone are mediated by a specific class of olfactory neuron. These findings suggest that transfer of cVA to females during mating may be part of the male's strategy to suppress reproduction by competing males.     

Silk‐ and volatile‐based male mate choice in the genital plug‐producing spider

Female mating history can have a strong effect on male fertilization success. Although males often prefer to mate with virgin females, they often also engage with mated females. As the intensity of sperm competition can differ among mated females, males are expected to evolve means to identify their status. In spiders, males often use female silk to gather information about female quality. Males of many spider species deposit mating plugs into female genitalia to hinder further copulations. We tested whether males of the foliage‐dwelling, plug‐producing spider Philodromus cespitum, which is an important natural enemy of pests, discriminate between females of different mating status and whether they can determine the extent of genital plugging in mated females solely on the basis of cues gained from deposited female silk. We presented males with draglines of females that varied in either mating status (virgin vs. mated), the extent of plugging (small vs. big plug), or the age of the plug (fresh vs. old plug) and examined their mate preferences. Additionally, we tested whether males were attracted to volatile cues produced by female bodies. Our experiments revealed that males preferred draglines of virgin females to those of mated females, and mated females with small plugs to those with large plugs. They were also attracted to female volatile cues. This study suggests that males are able to extract fine‐scale information on mating status from female draglines.     

Mated Redback Spider Females Re-Advertise Receptivity Months after Mating

In many species, selection acts on males to recognize female reproductive status at a distance using pheromones. Unmated females may actively seek to attract males; however, mated females may become cryptic to avoid attracting additional males if multiple matings are costly. Although females of many species cease pheromone production after mating, it is often unclear whether this is a strategic part of a female reproductive strategy, or whether this is because of chemical manipulation by males. If variation in pheromone production is part of the female’s strategy, then we predicted mated females should eventually re‐advertise receptivity if the benefits of multiple mating increase with time since copulation (e.g. because of sperm depletion). Here, we tested this prediction in Australian redback spiders (Latrodectus hasselti). First, we replicated earlier results by showing that virgin males discriminate female maturity and mating status based exclusively on web‐borne chemicals. Our results show this difference must arise from a change in chemical deposition in the web as we controlled for web volume differences between mated and virgin females. Male activity on extracts from webs of virgin females exceeded activity on a solvent control and on extracts of webs of just‐mated females—confirming that female redbacks cease pheromone production immediately after mating. Second, we tested a new prediction that mated females might re‐advertise receptivity near the end of their normal breeding season to replenish diminished sperm stores prior to overwintering. Consistent with the prediction of strategic advertisement, we show that male activity on extracts from females’ webs increased significantly 3 mo after the female first mated (typical length of the breeding season). Thus, these females had begun to add pheromone to their web again. At this time, 26% of these females re‐mated with a second male. If females re‐advertise receptivity to ensure adequate sperm stores, then we predicted a positive relationship between female reproductive output during the 3‐mo interval after copulation and the subsequent intensity of male response to web extracts. However, differences in male activity time were not related to the total number of spiderlings or the number of egg sacs a female had produced during the 3‐mo interval after the first copulation. This result could arise if male chemical manipulation of female receptivity decreases with time after copulation, or if the testing interval used in our study was too long to reveal variation in sperm depletion in females. Thus, although our results are consistent with the idea that females strategically alter pheromonal advertisement, we cannot distinguish this from the hypothesis that female receptivity arises from chemical manipulation by males.     

Female crickets assess relatedness during mate guarding and bias storage of sperm towards unrelated males

Recent evidence shows that females exert a post‐copulatory fertilization bias in favour of unrelated males to avoid the genetic incompatibilities derived from inbreeding. One of the mechanisms suggested for fertilization biases in insects is female control over transport of sperm to the sperm‐storage organs. We investigated post‐copulatory inbreeding‐avoidance mechanisms in females of the cricket Teleogryllus oceanicus. We assessed the relative contribution of related and unrelated males to the sperm stores of double‐mated females. To demonstrate unequivocally that biased sperm storage results from female control rather than cryptic male choice, we manipulated the relatedness of mated males and of males performing post‐copulatory mate guarding. Our results show that when guarded by a related male, females store less sperm from their actual mate, irrespective of the relatedness of the mating male. Our data support the notion that inhibition of sperm storage by female crickets can act as a form of cryptic female choice to avoid the severe negative effects of inbreeding.     

Male display rate reveals ejaculate characteristics in the Trinidadian guppy,Poecilia reticulata.

Previous work (Reynolds and Gross 1992) has demonstrated that mate choice enables female guppies, Poecilia reticulata, to obtain heritable benefits (''good genes'') for their offspring. It is not yet known whether males also signal their functional fertility, that is, their viability as fathers, to female guppies. Our study tested the hypothesis that a male''s behaviour reveals characteristics of his ejaculate. We uncovered a strong correlation between display rate and sperm number in male guppies derived from two wild Trinidadian populations. This result indicates that information on the functional fertility of potential mates is available to females. However, our investigation also found a significant relationship between the frequency of sneaky mating and sperm number. Female guppies in wild populations, particularly those experiencing a high predation regime, are constantly subjected to sneaky mating attempts. As the males responsible for these sneaky matings have highest reserves of sperm they may have the capacity to undermine female choice. The implications of these findings for sperm competition are discussed.     

Male Mate Choice in the Guppy (Poecilia reticulata): Do Males Prefer Larger Females as Mates?

Although females are the choosier sex in most species, male mate choice is expected to occur under certain conditions. Theoretically, males should prefer larger females as mates in species where female fecundity increases with body size. However, any fecundity‐related benefits accruing to a male that has mated with a large female may be offset by an associated fitness cost of shared paternity if large females are more likely to be multiply mated than smaller females in nature. We tested the above hypothesis and assumption using the Trinidadian guppy (Poecilia reticulata) by behaviourally testing for male mate choice in the laboratory and by ascertaining (with the use of microsatellite DNA genotyping) patterns of male paternity in wild‐caught females. We observed significant positive relationships between female body length and fecundity (brood size) and between body length and level of multiple paternity in the broods of females collected in the Quaré River, Trinidad. In laboratory tests, a preference for the larger of two simultaneously‐presented virgin females was clearly expressed only when males were exposed to the full range of natural stimuli from the females, but not when they were limited to visual stimuli alone. However, as suggested by our multiple paternity data, males that choose to mate with large females may incur a larger potential cost of sperm competition and shared paternity compared with males that mate with smaller females on average. Our results thus suggest that male guppies originating from the Quaré River possess mating preferences for relatively large females, but that such preferences are expressed only when males can accurately assess the mating status of encountered females that differ in body size.     

Effects of multiple matings on reproductive fitness of male and female Diaeretiella rapae

Mating frequency and the amount of sperm transferred during mating have important consequences on progeny sex ratio and fitness of haplodiploid insects. Production of female offspring may be limited by the availability of sperm for fertilizing eggs. This study examined multiple mating and its effect on fitness of the cabbage aphid parasitoid Diaeretiella rapae McIntosh (Hymenoptera: Aphidiidae). Female D. rapae mated once, whereas males mated with on average more than three females in a single day. The minimum time lag between two consecutive matings by a male was 3 min, and the maximum number of matings a male achieved in a day was eight. Sperm depletion occurred as a consequence of multiple mating in D. rapae. The number of daughters produced by females that mated with multiple‐mated males was negatively correlated with the number of matings achieved by these males. Similarly, the proportion of female progeny decreased in females that mated with males that had already mated three times. Although the proportion of female progeny resulting from multiple mating decreased, the decrease was quicker when the mating occurred on the same day than when the matings occurred once per day over several days. Mating success of males initially increased after the first mating, but then males became ‘exhausted’ in later matings; their mating success decreased with the number of prior matings. The fertility of females was affected by mating with multiple‐mated males. The study suggests that male mating history affects the fitness of male and female D. rapae.     

Mating Frequency, Fecundity and Fertilization Success in the Hide Beetle, Dermestes Maculatus

While the immediate benefits accrued to females through multiple mating are well documented, the effect of sperm depletion for multiply mating males is rarely considered. We show that, in small mixed-sex laboratory aggregations, both male and female hide beetles, Dermestes maculatus (De Geer) mated multiply. There was considerable variation in the mating frequency of both sexes; however the skew in mating success was comparable for males and females. Several individuals that mated multiply also re-mated with a previous partner, but in a competitive environment no male copulated more than seven times. Mating success was unrelated to an individual's size, but males that had the most inter-sexual matings also engaged in the most intra-sexual mating attempts. In a second experiment, we show that, even in the absence of rivals, only a small number of males mated with all available virgin females. Moreover, even though males were mated twice to each female, males that copulated more than eight times failed to fertilize any eggs. We suggest that under natural conditions male hide beetles may refrain from mating either prior to, or at the point of, sperm depletion thereby reducing the selection pressure for females to discriminate against sperm depleted males. However, fecundity and fertilization success varied considerably across females and even those mating with sperm-replete males were unable to fertilize 100% of their egg batch. Thus, direct fertilization benefits accrued by females through mating more than once with the same male may play a key role in the maintenance of polyandry in this species.     

Sexual History Affects Mating Behavior and Mate Choice in the Crayfish Orconectes limosus

Because mating entails both costs and potential benefits to both sexes, males and females should be under selection to make optimal choices from among available potential mates. For example, in some cases, individuals may benefit by using information on potential mates' previous sexual histories to make mate choices. In such cases, the form and direction of these benefits may vary both between the sexes and based on the sexual history of the choosing individuals themselves. We investigated the effects of recent previous sexual history on the mate choice and mating behavior of both males and females of the crayfish Orconectes limosus. In one experiment, we found that opposite‐sex dyads comprising crayfish that had both mated 7–8 d previously with other conspecifics were significantly less likely to mate than dyads in which at least one crayfish was unmated. In a second experiment, we found that, when presented with a choice of tethered (but free to move) opposite‐sex conspecifics, only virgin females discriminated between males based on sexual history, showing a preference for virgin males over recently mated males. Mated females, mated males, and virgin males showed no preferences based on the sexual histories of potential mates. We discuss the implications of these inferences in the context of what was previously known about mating behavior and potential sperm limitation in crustaceans and other taxa.     

Male-derived cuticular hydrocarbons signal sperm competition intensity and affect ejaculate expenditure in crickets

Female sexual promiscuity can have significant effects on male mating decisions because it increases the intensity of competition between ejaculates for fertilization. Because sperm production is costly, males that can detect multiple matings by females and allocate sperm strategically will have an obvious fitness advantage. The presence of rival males is widely recognized as a cue used by males to assess sperm competition. However, for species in which males neither congregate around nor guard females, other more cryptic cues might be involved. Here, we demonstrate unprecedented levels of sperm competition assessment by males, which is mediated via the use of chemical cues. Using the cricket Teleogryllus oceanicus, we manipulated male perception of sperm competition by experimentally coating live unmated females with cuticular compounds extracted from males. We found that males adjusted their ejaculate allocation in response to these compounds: the viability of sperm contained within a male's ejaculate decreased as the number of male extracts applied to his virgin female partner was increased. We further show that males do not respond to the relative concentration of male compounds present on females, but rather to the number of distinct signature odours of individual males. Our results conform to sperm competition theory, and show for the first time, to our knowledge, that males can detect different intensities of sperm competition by using distinct chemical cues of individual males present on females.