Dual reproductive cost of aging in male Medflies: dramatic decrease in mating competitiveness and gradual reduction in mating performance

Although age-based effects on the reproductive success of males have been reported in several animal taxa the cost of aging on male mating success in lekking species has not been fully explored. We used the Mediterranean fruit fly, a lekking species, to investigate possible cost of aging on male reproductive success. We performed no choice and choice mating tests to test the hypothesis that aging does not affect the mating performance (mating success in conditions lacking competition) or the mating competitiveness (mating success against younger rivals) of males. The mating probability of older males decreased significantly when competing with younger males. Aging gradually reduced the mating performance of males but older males were still accepted as mating partners in conditions lacking competition. Therefore, older males are capable of performing the complete repertoire of sexual performance but fail to be chosen by females in the presence of young rivals. Older males achieved shorter copulations than younger ones, and female readiness to mate was negatively affected by male age. Older and younger males transferred similar amount of spermatozoids to female spermathecae. Females stored spermatozoids asymmetrically in the two spermathecae regardless the age of their mating partner. Aging positively affected the amount of spermatozoids in testes of both mated and nonmated males. No significant differences were observed on the amount of spermatozoids between mated and nonmated males.     

Plasticity in male mating behavior modulates female life history in fruit flies

In many species, intense male-male competition for the opportunity to sire offspring has led to the evolution of selfish reproductive traits that are harmful to the females they mate with. In the fruit fly, Drosophila melanogaster, males modulate their reproductive behavior based on the perceived intensity of competition in their premating environment. Specifically, males housed with other males subsequently transfer a larger ejaculate during a longer mating compared to males housed alone. Although the potential fitness benefits to males from such plasticity are clear, its effects on females are mostly unknown. Hence, we tested the long-term consequences to females from mating with males with distinct social experiences. First, we verified that competitive experience influences male mating behavior and found that males housed with rivals subsequently have shorter mating latencies and longer mating durations. Then, we exposed females every other day for 20 days to males that were either housed alone or with rivals, and subsequently measured their fitness. We found that females mated to males housed with rivals produce more offspring early in life but fewer offspring later in life and have shorter lifespans but similar intrinsic population growth rates. These results indicate that plasticity in male mating behavior can influence female life histories by altering females’ relative allocation to early versus late investment in reproduction and survival.     

同种雄性竞争对手的存在对星豹蛛雄蛛求偶和交配行为的影响

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

Sexual conflict over mating in Gnatocerus cornutus? Females prefer lovers not fighters

Female mate choice and male–male competition are the typical mechanisms of sexual selection. However, these two mechanisms do not always favour the same males. Furthermore, it has recently become clear that female choice can sometimes benefit males that reduce female fitness. So whether male–male competition and female choice favour the same or different males, and whether or not females benefit from mate choice, remain open questions. In the horned beetle, Gnatocerus cornutus, males have enlarged mandibles used to fight rivals, and larger mandibles provide a mating advantage when there is direct male–male competition for mates. However, it is not clear whether females prefer these highly competitive males. Here, we show that female choice targets male courtship rather than mandible size, and these two characters are not phenotypically or genetically correlated. Mating with attractive, highly courting males provided indirect benefits to females but only via the heritability of male attractiveness. However, mating with attractive males avoids the indirect costs to daughters that are generated by mating with competitive males. Our results suggest that male–male competition may constrain female mate choice, possibly reducing female fitness and generating sexual conflict over mating.     

酪蝇的羽化节律和交配行为

【目的】为了明确酪蝇Piophila casei的羽化节律和交配行为,为深入研究酪蝇的性信息素打下基础。【方法】在室内条件[温度(27±1)℃,光周期L︰D=14︰10]下观察了酪蝇的羽化节律和交配行为。【结果】结果表明,化蛹后第8天成虫羽化最多,羽化高峰期出现在由暗期进入光期的前后,雄虫略早于雌虫羽化。观察结果表明,当雄虫接近蛹壳时会表现出"触摸"、"经过"、"扑"、"抱握"等动作,而雌虫仅有"触摸"、"抱握"的动作。当遇到同性成虫或者已交配雌虫时,雄虫会"追逐"对方,当接触到对方时雄虫会表现出"抱握"、"触摸"动作以进行识别,被识别雄虫会"翘起腹部末端"使对方离开,已交配雌虫则猛烈"摆动身体"使对方离开。当遇到处女雌虫时,雄虫跳跃到雌虫背上迅速进行交配。雌虫羽化后1 min即可交配,雄虫羽化后30 min可交配,交配平均持续时间10 min。雄虫间会有交配竞争行为发生,后来者会跳跃到先来者背上,向下弯曲腹部试图越过先来者与雌虫交配。【结论】酪蝇的羽化高峰出现在进入光期前后。成虫对蛹壳有显著趋性,雄虫主动追逐识别异性,较雌虫表现出更强烈的交配欲望。     

The role of female dominance hierarchies in the mating behaviour of mosquitofish

While studies of sexual selection focus primarily on female choice and male-male competition, males should also exert mate choice in order to maximize their reproductive success. We examined male mate choice in mosquitofish, Gambusia holbrooki, with respect to female size and female dominance. We found that the number of mating attempts made by a male was predicted by the dominance rank of females in a group, with dominant females attracting more mating attempts than subordinates. The number of mating attempts made by males was independent of the female size. The observed bias in the number of mating attempts towards dominant females may be driven either by straightforward male mate choice, since dominance and female fecundity are often closely related, or via the dominant females mediating male mating behaviour by restricting their access to subordinate females.     

Male copulation behaviour and the risk of sperm competition

When females mate with more than one male during their reproductive cycle, males may increase their share of paternity by copulating repeatedly with the same female. Accordingly, males should mate repeatedly with the same female more frequently when the risk of sperm competition is greater. We examined this idea experimentally in the orb-web spiderNephila edulis , which is characterized by both extreme sexual size dimorphism and extreme male size variation. Comparison of the mating behaviour of solitary and pairs of males on the webs of virgin and mated females revealed that males adjust the frequency and duration of copulation according to the mating history of the female and the presence of rival males. Males copulated more frequently and for longer with virgin than mated females. The copulation behaviour of males in the presence of rivals depended upon their relative size. Typically, larger males prevented smaller rivals from gaining access to the female and therefore were able to copulate more frequently. Smaller males copulated less frequently, but for longer periods, which may have increased their share of paternity. The size of male N. edulis can vary by an order of magnitude, and our results suggest that this variation may be maintained by the alternative size-dependent strategies of preventing or winning sperm competition. Copyright 2003 Published by Elsevier Ltd on behalf of The Association for the Study of Animal Behaviour.      

Pre-implantation Pregnancy Disruption in Female Meadow Voles Microtus pennsylvanicus (Rodentia: Muridae): Male Competition or Female Mate Choice?

I investigated alternative hypotheses concerning the functions of pre-implantation male-induced pregnancy disruption in meadow voles. Disruptions may be viewed as: 1. Postcopulatory male competition; 2. A mechanism for postcopulatory mate choice by females; and 3. A means of benefitting females by terminating investment in litters that may be harmed by new males. Female voles were paired with a second male 3 d after mating with their first mate. Behavioural interactions between the female and each male were compared for females that disrupted or retained the pregnancy sired by the first male. Whether they were the females' first or second mates, males siring litters showed similar high levels of approach and moderately high aggression, behaviour that differed from the females' other mates. Disrupted females huddled sooner with their second mates than females that retained their original pregnancies, and females tended to approach males that approached them. These results suggest that females influence whether a disruption occurs by the amount of contact they initiate with the second male, and thus pregnancy disruption may facilitate postcopulatory mate choice by females. This pre-implantation disruption did not enhance female reproductive success: pup survival was the same whether or not a disruption occurred, and males living with pups they had sired (after a disruption) spent as much time with them as males with unrelated pups (females did not disrupt).     

Sperm competition and the significance of female multiple mating in the predatory miteParasitus fimetorum

Females of the predatory miteParasitus fimetorum (Gamasida; Parasitina) inhabiting animal manure indiscriminately copulate with many mates. The sperm competition between the males was estimated by electrophoresis of allozymes and the effects of multiple mating on female reproduction were investigated. When females were forced to mate only once, their fecundity decreased drastically compared to the case of multiple mating (but longevity was unaffected). When one female mated with two males, the outcome of sperm competition depended greatly upon the mating interval. When the second mating occurred immediately after the first, the female fecundity decreased as in the case of single mating and the second male fertilized only a few eggs. However, when there was an interval of 1 day between the two matings, the females achieved normal fecundity and the second male fertilized approximately half the eggs. This suggests that the spermatophore deposited by the first male may act as a short-term copulatory ‘plug’ in the female's genital opening. When one female mated with several males with 1 day intervals, three or more males shared fertilization of the eggs. This study suggests that the multiple mating of females is a necessary stimulus to continue oogenesis and some physiological factors for this stimulation may exist in spermatophores.     

Mating system in mouse lemurs: theories and facts, using analysis of paternity

Among nocturnal Malagasy prosimians, the grey mouse lemur (Microcebus murinus) is considered a solitary species which has a promiscuous mating system. Indirect indicators, such as the lack of sexual dimorphism, the overlapping of male and female home ranges with each other, the synchronism of seasonal oestrus and the high relative testes size of males, support the presence of sperm competition. In captivity, an intense sexual precopulatory competition develops among males, leading to the emergence of a dominant male who fathers the majority of the litters. Although multiple mating did occur, the dominant male achieved the majority of the matings on the first day of oestrus. A 'mate-guarding' behaviour, exhibited by the dominant male, was observed in 11 groups out of 15, on only the first day of the vaginal opening and was significantly more often directed towards younger females. Females also played an important role in sexual competition among males, since their presence enhances the aggressive interactions between males. Difference in aggressive behaviours of females, in response to male sexual solicitations, suggests female mate choice. Compared with data from wild animals, it may be hypothesised that alternative mating strategies can be used by male grey mouse lemurs to enhance their reproductive success, depending on the availability and distribution of receptive females.     

Queen-queen competition by precocious male production in multiqueen ant colonies

Arriving earlier in the breeding area than his rivals may be beneficial for a male when females mate only once or during a short time span. The timing of a male's entrance is usually determined by the male himself, e.g., through returning early from his winter quarters or through accelerated larval development . Here, we document a surprisingly simple way of "first come, first served" in a species with local mate competition. In multiqueen colonies of a Cardiocondyla ant, mother queens make sure that their own sons are the first to monopolize mating with a large harem of female sexuals by producing extremely long-lived males early in colony life. Whereas queens in newly founded single-queen colonies started to produce male and female sexuals only several weeks after the eclosion of their first worker offspring, queens in multiqueen colonies precociously reared sons long before the first female sexuals and even before the emergence of their first workers. These early males killed all later emerging males in the nest and mated with all female sexuals subsequently produced. Our data document that the patterns of growth and productivity of insect colonies are surprisingly flexible and can be turned upside down under appropriate selection pressures.     

Double insurance of paternity by a novel type of mating plug in a monandrous solitary mason bee Osmia bicornis (Hymenoptera: Megachilidae)

Males of some hymenopteran species are able to behaviourally induce unreceptivity to mating in females by a post‐copulatory display (post‐copulatory courtship). This method of preventing further inseminations requires a high degree of female cooperation by the female and is especially susceptible to manipulations. If mating chances are low and sexual competition between males high, males can be expected to evolve additional mechanisms to protect their fertilization opportunities. This hypothesis was checked in the red mason bee Osmia bicornis (Linnaeus, 1758; syn. Osmia rufa). Males of this species were found to use a mating plug as a reinsurance to protect their paternity, although they induce females' monandry by a post‐copulatory display. Male accessory gland secretions transferred during ejaculation form a plastic, spongy plug in the females' vagina that also contains the spermatozoa. This mating plug does not hinder rivals to mate with the female but prevents intermixing of the sperm. Thus, the sperm precedence of the first male is secured. The plug is ejected by the female after approximately 1 day when the spermatheca has been completely filled with sperm. The male accessory gland supply is sufficient for the formation of two to three plugs only and is not replenished. This pattern fits well with the low mating opportunities of O. bicornis males. The evolution of a mating plug in addition to the behavioural induction of unreceptivity to mate in females is discussed. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 115 , 28–37.     

Male Performance and Body Size Affect Female Re-Mating Occurrence in the Orb-Web Spider Leucauge mariana (Araneae, Tetragnathidae)

Females can affect male probabilities of paternity success through behavioural, morphological and/or physiological processes occurring during or after copulation. These processes under female-control include the acceptance or rejection of mating attempts by subsequent males. Leucauge mariana is an orb weaving spider that shows male mate guarding of penultimate females, male–male competition on female webs and copulatory plugs, suggesting a polyandric mating system. The aim of the present study was to ascertain whether male behaviour during courtship and copulation in L. mariana relate with female re-mating decisions. Forty-three virgin females were exposed to up to three males until they mated. In 24 cases, the copulatory plug was absent after mating and females were exposed the next day to up to three other males. Eighteen females accepted a second mating. Relatively larger females were more receptive to second matings and were more likely to copulate if the second male was smaller. Longer duration of female tapping and abdominal bobbing during courtship, and first copulations with less short insertions and more flubs, were associated with increased female acceptance to second matings. The results indicate cryptic female choice on male courtship and copulatory performance and suggest female-control over the determination of male mating success in this spider species.     

Indirect mate choice, direct mate choice and species recognition in a bower-building cichlid fish lek

Sexual selection arising through female mate choice typically favours males with larger, brighter and louder signals. A critical challenge in sexual selection research is to determine the degree to which this pattern results from direct mate choice, where females select individual males based on variation in signalling traits, or indirect mate choice, where male competition governs access to reproductively active females. We investigated female mate choice in a lekking Lake Malawi cichlid fish, Hemitilapia oxyrhynchus, in which males build and aggressively defend sand 'bowers'. Similar to previous studies, we found that male reproductive success was positively associated with bower height and centrality on the lek. However, this pattern resulted from males holding these territories encountering more females, and thus their greater success was due to indirect mate choice. Following initial male courtship, an increase in the relative mating success of some males was observed, but this relative increase was unrelated to bower size or position. Crucially, experimentally manipulating bowers to resemble those of a co-occurring species had no appreciable effect on direct choice by females or male spawning success. Together, these results suggest indirect mate choice is the dominant force determining male-mating success in this species, and that bowers are not signals used in direct mate choice by females. We propose that, in this species, bowers have a primary function in intraspecific male competition, with the most competitive males maintaining larger and more central bowers that are favoured by sexual selection due to higher female encounter rates.     

Female Remating Behavior in a Lekking Moth

In polyandrous species, male reproductive success will at least partly be determined by males' success in sperm competition. To understand the potential for post‐mating sexual selection, it is therefore important to assess the extent of female remating. In the lekking moth Achroia grisella, male mating success is strongly determined by female choice based on the attractiveness of male ultrasonic songs. Although observations have indicated that some females will remate, only little is known about the level of sperm competition. In many species, females are more likely to remate if their first mating involved an already mated male than if the first male was virgin. Potentially, this is because mated males are less well able to provide an adequate sperm supply, nutrients, or substances inhibiting female remating. This phenomenon will effectively reduce the strength of pre‐copulatory sexual selection because attractive males with high mating success will be more susceptible to sperm competition. We therefore performed an experiment designed both to provide a more precise estimate of female remating probability and simultaneously to test the hypothesis that female remating is influenced by male mating history. Overall, approximately one of five females remated with a second male. Yet, although females mated to non‐virgin males were somewhat more prone to remate, the effect of male mating history was not significant. The results revealed, however, that heavier females were more likely to remate. Furthermore, we found that females' second copulations were longer, suggesting that, in accordance with theory, males may invest more sperm in situations with an elevated risk of sperm competition.     

Sexual Strategies of a North American ‘Tarantula’ (Araneae: Theraphosidae)

Despite their general notoriety and popularity as pets, little is known of the behavioural ecology of ‘tarantulas’ or theraphosid spiders. We studied a theraphosid of the Arizona deserts, Aphonopelma sp., to determine behavioural events crucial to successful courtship and mating. Males search for spatially scattered females and, at short range, may detect females by substrate-borne cues. When two males are present with a single female, no direct competition such as aggression is observed. Both males may mate with a single female in rapid succession, with no evidence of post-copulatory mate guarding. Despite the potential for sexual cannibalism, courtship and mating behaviour patterns exhibit few aggressive elements and males nearly always survive sexual encounters with females. The mating system of this Aphonopelma species may best be described as a type of scramble-competition polygyny, in which the ability of males to locate receptive females is an important determinant of mating success in males. Multiple mating by females renders predictions concerning fertilization success uncertain, due to the possibility of sperm competition and ‘cryptic’ female mate choice.     

Multiple Mating Increases Fecundity, Fertility and Relative Clutch Mass in the Female Leopard Gecko (Eublepharis macularius)

Females across many taxa may mate with several males or mate more than once with the same male within one reproductive event. Although many researchers have discussed the effects of multiple mating on reproductive success of females, few studies have attempted to disentangle whether the reproductive success of females differs with respect to whether females mate with multiple males or mate more than once with one male. In this study, we hypothesized that female leopard geckos (Eublepharis macularius) increase aspects of their reproductive success, such as fecundity, fertility and relative clutch mass, by mating more than once within one reproductive event, either by mating repeatedly with the same male or multiply mating with different males. We controlled for the potentially confounding variables of mating frequency and mate number by allowing females to mate once with one male, twice with the same male, or twice with two different males. We found that females that mated with more than one male laid more clutches, exhibited increased egg fertility and invested more in clutches relative to females that mated only once with one male, whereas females that mated twice to the same male were intermediate for these variables. Thus, reproductive success is higher among female leopard geckos that mated with more than one male compared to female leopard geckos that mated only once.     

Size-biased Mating in Both Sexes of the Black-horned Tree Cricket, <Emphasis Type="Italic">Oecanthus nigricornis</Emphasis> Walker (Orthoptera: Gryllidae: Oecanthinae)

Previous studies on tree crickets have demonstrated female choice of males based on size and courtship feeding but less is known about sexual selection under conditions of direct mating competition. I studied courtship, aggression and mating of the black-horned tree cricket Oecanthus nigricornis (Walker) to test size-related sexual selection under conditions of direct sexual competition. Results show that larger individuals of both sexes mated more frequently than their smaller counterparts, and this was due to the ability of large individuals to out compete rivals. Large males achieved the advantage by aggressively reducing courtship by small males, whereas large females responded to male courtship more quickly but with little aggression. Although there was no evidence here for mate choice, there were advantages for having larger mates; fecundity increased with female size and spermatophores (which females consume after mating) increased with male size. Size of the specialized metanotal courtship gift, however, was not related to male size.     

Sperm stratification and paternity success in red flour beetles

Abstract. When females are inseminated by multiple males, male paternity success (sperm precedence) is determined by the underlying processes of sperm storage and sperm utilization. Although informative for many questions, two-male sperm competition experiments may offer limited insight into natural mating scenarios when females are likely to mate with several males. In this study, genetic markers in Tribolium castaneum are used to trace paternity for multiple sires, and to determine whether displacement of stored sperm that occurs after a third mating equally affects both previous mates, or if fertilizations are disproportionately lost by the female's most recent mate. For 20 days after triple-matings, first males retain significantly higher paternity success (relative to first male paternity in double-matings) compared with second males. These results demonstrate that when females remate before sperm mixing occurs, sperm stratification results in differential loss of sperm from the most recent mate. This study provides insight into the mechanisms underlying sperm precedence in a promiscuous mating system, and suggests that T. castaneum females could limit paternity success of particular mates by remating with more highly preferred males.     

Sex roles and mutual mate choice matter during mate sampling

The roles of females and males in mating competition and mate choice have lately proven more variable, between and within species, than previously thought. In nature, mating competition occurs during mate search and is expected to be regulated by the numbers of potential mates and same-sex competitors. Here, we present the first study to test how a temporal change in sex roles affects mating competition and mate choice during mate sampling. Our model system (the marine fish Gobiusculus flavescens) is uniquely suitable because of its change in sex roles, from conventional to reversed, over the breeding season. As predicted from sex role theory, courtship was typically initiated by males and terminated by females early in the breeding season. The opposite pattern was observed late in the season, at which time several females often simultaneously courted the same male. Mate-searching females visited more males early than late in the breeding season. Our study shows that mutual mate choice and mating competition can have profound effects on female and male behavior. Future work needs to consider the dynamic nature of mating competition and mate choice if we aim to fully understand sexual selection in the wild.