Effects of social information on life history and mating tactics of males in the orb‐web spider Argiope bruennichi

Informed mating decisions are often based on social cues providing information about prospective mating opportunities. Social information early in life can trigger developmental modifications and influence later mating decisions. A high adaptive value of such adjustments is particularly obvious in systems where potential mating rates are extremely limited and have to be carried out in a short time window. Males of the sexually cannibalistic spider Argiope bruennichi can achieve maximally two copulations which they can use for one (monogyny) or two females (bigyny). The choice between these male mating tactics should rely on female availability that males might assess through volatile sex pheromones emitted by virgin females. We predict that in response to those female cues, males of A. bruennichi should mature earlier and at a smaller body size and favor a bigynous mating tactic in comparison with controls. We sampled spiders from two areas close to the Southern and Northern species range to account for differences in mate quality and seasonality. In a fully factorial design, half of the subadult males from both areas obtained silk cues of females, while the other half remained without female exposure. Adult males were subjected to no‐choice mating tests and could either monopolize the female or leave her (bigyny). We found that Southern males matured later and at a larger size than Northern males. Regardless of their origin, males also shortened the subadult stage in response to female cues, which, however, had no effects on male body mass. Contrary to our prediction, the frequencies of mating tactics were unaffected by the treatment. We conclude that while social cues during late development elicit adaptive life history adjustments, they are less important for the adjustment of mating decisions. We suggest that male tactics mostly rely on local information at the time of mate search.     

Size‐Dependent Male Mate Preference and its Association with Size‐Assortative Mating in a Mangrove Snail,Littoraria ardouiniana

In many animals, body size plays a crucial role in mating success in the context of competition and preference for mates. Increasing evidence has shown that male mate preference can be size‐dependent and, therefore, an important driver of size‐assortative mating. To test this theory, mate choice experiments were performed during the three consecutive stages of mating behaviour, namely trail following, shell mounting and copulation, in the dioecious mangrove snail, Littoraria ardouiniana. These experiments identified two possible forms of size‐dependent male mate preference which could contribute to the formation of size‐assortative mating in these snails. Firstly, whereas small males were unselective, large males were selective and preferred to follow mucus trails laid by large females. Alternatively, the results can also be interpreted as all males were selective and adopted a mating strategy of selecting females similar to, or larger than, their own sizes. Both small and large males also copulated for longer with large than with small females, and this was more pronounced in large males. When two males encountered a female, they engaged in physical aggression, with the larger male excluding the smaller male from copulating with the female. This study, therefore, demonstrated that size‐dependent male mate preference may, along with male–male competition, play an important role in driving size‐assortative mating in these mangrove snails, and this may also be the case in other species that exhibit male mate choice.     

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.     

Spider Males Adjust Mate Choice but Not Sperm Allocation to Cues of a Rival

Spatial and temporal variation in ecological parameters selects for plastic responses to prevailing conditions. Males of web spiders have been shown to adjust developmental decisions to cues that relate to the degree of competition from other males. Here, we explore experimentally whether males of the spider Nephila senegalensis base behavioural decisions in the context of mate choice and sperm allocation to the presence of cues of a rival and to their own competitive dominance. Large and small males were offered a simultaneous choice between two penultimate instar females that varied in quality and in whether they were previously visited by a rival male. Large and small males avoided webs visited by a previous male, and this preference overrode differences in female quality. In a second experiment, males were assigned to copulate with a virgin female whose web was either previously visited by a rival male or not. We found substantial variation in male sperm allocation, but this variation was not related to our treatment. Our experiments demonstrate that males notice silk cues left behind by rival males on a female’s web and that they can utilize these cues in relation to decisions over whether to visit a web, but not in relation to sperm allocation.     

Old‐male paternity advantage is a function of accumulating sperm and last‐male precedence in a butterfly

Old‐male mating advantage has been convincingly demonstrated in Bicyclus anynana butterflies. This intriguing pattern may be explained by two alternative hypotheses: (i) an increased aggressiveness and persistence of older males during courtship, being caused by the older males' low residual reproductive value; and (ii) an active preference of females towards older males what reflects a good genes hypothesis. Against this background, we here investigate postcopulatory sexual selection by double‐mating Bicyclus anynana females to older and younger males, thus allowing for sperm competition and cryptic mate choice, and by genotyping the resulting offspring. Virgin females were mated with a younger virgin (2–3 days old) and afterwards an older virgin male (12–13 days old) or vice versa. Older males had a higher paternity success than younger ones, but only when being the second (=last) mating partner, while paternity success was equal among older and younger males when older males were the first mating partner. Older males produced larger spermatophores with much higher numbers of fertile sperm than younger males. Thus, we found no evidence for cryptic female mate choice. Rather, the findings reported here seem to result from a combination of last‐male precedence and the number of sperm transferred upon mating, both increasing paternity success.     

Female mate choice and mating costs in the polyandrous butterflyPieris napi (Lepidoptera: Pieridae)

Males of the green-veined white butterfly (Pieris napi L.) transfer large ejaculates that represent on average 15% of their body mass when mating for a first time. Shortly after mating a male is able to transfer only a small ejaculate when mating a second time. Male ejaculate production plays a crucial role in the mating system ofP. napi because females use male-derived nutrients for egg production and somatic maintenance. Here we study how timing of female rematings and copulation duration are influenced by the mating history of their mates and, also, study if females exert mate choice to minimize their mating costs. Mating with a recently mated male increased female mating costs by increasing time in copula and mating frequency. Virgin females that mated with virgin males remated after an average of 6 days, whereas virgin females that mated with recently mated males remated after an average of 2 days. Moreover, copulations involving recently mated males lasted on average almost 7 h, whereas copulations involving virgin males lasted on average 2 h. Recently mated males were eager to remate, in spite of the fact that the size of the ejaculate they transfer is small and that they remain in copula for a long time. Hence it seems that males are more successful in the sexual conflict over mating decisions and that females do not minimize mating costs by choosing to mate preferentially with virgin males.     

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。     

Male age and sexual experience affect male mating behavior in the hawthorn spider mite,Amphitetranychus viennensis

As is reported, in species with first-male sperm precedence, male age and previous sexual experience play crucial roles in male mating behavior. In the hawthorn spider mite, Amphitetranychus viennensis Zacher, previous studies showed that only females that copulated for the first time could achieve fertilization. Based on this, the effects of male age and mating history on male mate choice and male mate competition were investigated. It was confirmed that males could distinguish virgins from fertilized females but they were unable to discriminate between virgins and unfertilized females. Interestingly, the copulation duration of males mated with fertilized females was much shorter than that of males mated with virgins or unfertilized females. Additionally, for male mating choice, males of all ages and more experienced males preferred 5-day-old virgin females, whereas only less experienced males preferred 1-day-old virgin females. In male-male competition, 3-day-old males were more competitive and obtained more copulations compared with others. Copula duration was closely related to male age. Though no significant differences were observed in mating competition between virgin and mated males, copula duration of males in first copulation was the longest and gradually shortened in subsequent copulations. In all, this investigation demonstrated that male age and sexual experience affected male mate choice and male-male competition, leading to further insight into the influences of male age and sexual experience on the reproductive fitness of both sexes.

     

Field evidence challenges the often‐presumed relationship between early male maturation and female‐biased sexual size dimorphism

Female‐biased sexual size dimorphism (SSD) is often considered an epiphenomenon of selection for the increased mating opportunities provided by early male maturation (i.e., protandry). Empirical evidence of the adaptive significance of protandry remains nonetheless fairly scarce. We use field data collected throughout the reproductive season of an SSD crab spider, Mecaphesa celer, to test two hypotheses: Protandry provides fitness benefits to males, leading to female‐biased SSD, or protandry is an indirect consequence of selection for small male size/large female size. Using field‐collected data, we modeled the probability of mating success for females and males according to their timing of maturation. We found that males matured earlier than females and the proportion of virgin females decreased abruptly early in the season, but unexpectedly increased afterward. Timing of female maturation was not related to clutch size, but large females tended to have more offspring than small females. Timing of female and male maturation was inversely related to size at adulthood, as early‐maturing individuals were larger than late‐maturing ones, suggesting that both sexes exhibit some plasticity in their developmental trajectories. Such plasticity indicates that protandry could co‐occur with any degree and direction of SSD. Our calculation of the probability of mating success along the season shows multiple male maturation time points with similar predicted mating success. This suggests that males follow multiple strategies with equal success, trading‐off access to virgin females with intensity of male–male competition. Our results challenge classic hypotheses linking protandry and female‐biased SSD, and emphasize the importance of directly testing the often‐assumed relationships between co‐occurring animal traits.     

Male age affects female mating preference but not fitness in the monandrous moth Dendrolimus punctatus Walker (Lepidoptera: Lasiocampidae)

It is widely accepted that male age can influence female mating preference and subsequent fitness consequences in many polyandrous species, yet this is seldom investigated in monandrous species. In the present study, we use the monandrous pine moth Dendrolimus punctatus to examine the effects of male age on female mating preference and future reproductive potential. In multiple male trials, when permitted free mating from an aggregation consisting of virgin males aged 0 (young), 2 (middle-aged) and 4 (old) days, virgin females preferentially mate with young and middle-aged males, although mating latency and mating duration are independent of male age. In single male trials, when virgin females are randomly assigned single virgin males of known age, a negative correlation is found between mating success and male age in this species. However, we find that male age also has no effect on mating latency and mating duration. Further fitness analysis reveals that females do not receive benefits in terms of oviposition period, total egg production, average daily egg production, percentage of egg hatching, longevity, expected reproduction and relative expected reproduction from mating with young and middle-aged males compared with mating with old males. The results of the present study are the first demonstrate that females mated preferentially with younger males but gain no apparent fitness benefits in a monandrous moth species.     

Male adaptations to minimize sexual cannibalism during reproduction in the funnel‐web spider Hololena curta

Males of many spider species risk being attacked and cannibalized while searching for, courting, and mating with conspecific females. However, there are exceptions. We show that the funnel‐web spider, Hololena curta, has 3 adaptations that minimize risk to males during courtship and mating, and enhance reproductive success. First, males detected chemical or tactile signals associated with webs of virgin females, and differentiated them from webs of mated females, enabling males to increase encounter rates with virgin females and avoid aggressive mated females. Second, males produced stereotyped vibrational signals during courting which induced female quiescence and suppressed female aggression. Third, when touched by males, sexually receptive females entered a cataleptic state, allowing males to safely approach and copulate. Because males can mate multiple times and the sex ratio in natural populations of H. curta is female biased, overall reproductive output is likely increased by males of this species avoiding sexual cannibalism.     

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.     

Female Reproductive Status and Mate Choice in the Hide Beetle, Dermestes maculatus

Models of mutual mate choice predict that when the costs of mating indiscriminately increase, so may the choosiness of the conventionally non-choosy sex. In a series of behavioral trials, we tested both male and female chemo-reception and mate choice in the hide beetle, Dermestes maculatus. Using olfactometer bioassays we found that males detected and responded more rapidly to individual mated females but had a limited ability to detect virgin females or discriminate between virgin and mated females when presented simultaneously. Both mated and virgin females were unable to detect the presence of virgin males. Copulation behaviors were comparable when males were presented with a virgin or mated female either individually or simultaneously. However, when presented simultaneously, virgin females had a higher probability of receiving a copulation than their mated counterparts. Our data show that males respond to variation in female reproductive status, but that female propensity to mate does not change. We suggest that mutual mate choice may be an important force, even in systems in which there is apparently strong selection for female mate discrimination.     

Female Mating History Influences Copulation Behavior but Not Sperm Release in the Orb-Weaving Spider <Emphasis Type="Italic">Tetragnatha versicolor</Emphasis> (Araneae,Tetragnathidae)

We examined the influence of female mating history on copulation behavior and sperm release in the haplogyne spider Tetragnatha versicolor. Despite significant behavioral differences during mating, males released equivalent amounts of sperm to virgin and non-virgin females. When mating with non-virgin females, males showed twice as many pedipalp insertions and half the copulation duration as compared to virgin females; however, males were as likely to mate with non-virgin as virgin females. Even with these overt behavioral differences, males released half of the sperm contained within their pedipalps during mating, regardless of female mating history. With respect to male mating order, first or second, we suggest the numbers of sperm released would lead to an expectation of unbiased paternity. In this species, sperm release is not directly proportional to total copulationduration.     

Males Prefer Small Females in a Dichotomous Choice Test in the Poeciliid Fish Heterandria formosa

Male choice is expected to evolve when females differ in quality, even if male investment in each mating is low. The family Poeciliidae is an example of fishes in which males show little parental investment as they only provide sperm. Up until now, a preference for large females has been found in all species studied. Here we show that unexpectedly, males of the least killifish (Heterandria formosa) prefer to interact with small instead of large females in a dichotomous male choice test, even though large females are more fecund. During a free‐swimming choice experiment, males did not discriminate between females based on their size. We suggest that this unique preference for small females, or the lack of preference for large females, results from strong first male sperm precedence in this species. Smaller females are younger and therefore more likely to be virgin, which probably makes them more profitable mates for males. When presented with a virgin and a mated female of similar size, males showed no preference for either type. This suggests that males do not use pheromone cues to assess female mating status but that they are likely to use female size as a proxy for it.     

First experimental evidence for female mate choice in a nocturnal primate

Female mate choice can be hypothesised in most nocturnal primates, since females show a higher investment in their offspring than males. The aim of this experimental study was to investigate if female grey mouse lemurs perform mate choice and whether age, relatedness (to the male), or male advertisement call activity systematically influence their decisions. A two-way mate choice design was developed in which females could choose between two males. Mate choice was deduced from the time spent in proximity to the males and from mating behaviour. During oestrus 12 of 17 females participated actively in the experiment and all of them showed either a significant spatial (n=11) or behavioural (n=1) preference for one male. In four cases copulations were observed. The influence of age on female mate choice was not statistically significant. In the cases with copulations, however, females mostly preferred the older male. This might indicate a preference for older age as an indicator of experience, fitness, and/or status. The influence of relatedness on female mate choice could not be definitely clarified. However, results imply a mechanism of kin recognition on the basis of familiarity. In the majority of choices, females preferred the male with higher trill call activity. Since trill call activity correlates with the relative dominance status of males, these results suggest an importance of the male dominance status for female mate choice in grey mouse lemurs. Altogether our findings indicate that females use a complex of different cues to choose their mates.     

Plasticity of the mate choice mind: courtship evokes choice‐like brain responses in females from a coercive mating system

Female mate choice is fundamental to sexual selection, and determining molecular underpinnings of female preference variation is important for understanding mating character evolution. Previously it was shown that whole‐brain expression of a synaptic plasticity marker, neuroserpin, positively correlates with mating bias in the female choice poeciliid, Xiphophorus nigrensis, when exposed to conspecific courting males, whereas this relationship is reversed in Gambusia affinis, a mate coercive poeciliid with no courting males. Here we explore whether species‐level differences in female behavioral and brain molecular responses represent ‘canalized’ or ‘plastic’ traits. We expose female G. affinis to conspecific males and females, as well as coercive and courting male Poecilia latipinna, for preference assays followed by whole‐brain gene expression analyses of neuroserpin, egr‐1 and early B. We find positive correlations between gene expression and female preference strength during exposure to courting heterospecific males, but a reversed pattern following exposure to coercive heterospecific males. This suggests that the neuromolecular processes associated with female preference behavior are plastic and responsive to different male phenotypes (courting or coercive) rather than a canalized response linked to mating system. Further, we propose that female behavioral plasticity may involve learning because female association patterns shifted with experience. Compared to younger females, we found larger, more experienced females spend less time near coercive males but associate more with males in the presence of courters. We thus suggest a conserved learning‐based neuromolecular process underlying the diversity of female mate preference across the mate choice and coercion‐driven mating systems.     

三突伊氏蛛雌蛛不同交配史对雄蛛交配行为的影响

近年来越来越多研究表明,雄性产生精子(精液)也需付出代价。在多次交配的动物中,雄性为获得最大生殖潜力,必须依据配偶的质量策略性地调整每次交配的生殖投入。雄性策略性的生殖投入主要体现在两个方面,一是精子竞争(sperm competition),二是柯立芝效应(Coolidge effect)。目前精子竞争研究主要集中于昆虫类群,而柯立芝效应研究集中于高等脊椎动物,同时验证结果也时常与假说不一致。以多次交配的三突伊氏蛛为材料,以雄蛛交配行为为指标,在蜘蛛类群中探讨和验证雄性精子竞争强度假说和柯立芝效应。设定3个交配组合:2只雄蛛依次与1只雌蛛各交配1次(A组)、2只雄蛛依次与2只雌蛛各交配1次(B组)和1只雄蛛与1只雌蛛交配2次(C组),分析比较3个交配组合的三突伊氏蛛第1次交配和第2次交配在交配潜伏期、交配持续时间和交配回合数方面的差异,比较三突伊氏蛛雌蛛不同交配史对雄蛛交配行为的影响,以此验证雄性精子竞争强度假说和柯立芝效应。研究结果表明A和B组的三突伊氏蛛第2次交配的交配潜伏期和交配持续时间显著长于第1次交配。同时,C组的三突伊氏蛛第1次交配的交配潜伏期和交配持续时间与第2次交配都没有显著差异。同时,A、B和C组的三突伊氏蛛第1次交配的交配回合数与第2次交配都没有显著差异。研究结果支持精子竞争强度假说,而不支持柯立芝效应。     

Mate choice in the predaceous mite Phytoseiulus persimilis: evidence of self‐referent phenotype matching?

Close inbreeding may have negative fitness effects. Consequently, organisms have evolved various mechanisms, which enable them to avoid close inbreeding. In no‐choice and choice experiments we assessed whether the predaceous mite Phytoseiulus persimilis Athias‐Henriot (Acari: Phytoseiidae) avoids close inbreeding by kin recognition. No‐choice experiments demonstrated that virgin females more readily accept unrelated males than they accept related ones, which suggests a female preference for unrelated mates. Because each female had been reared in isolation prior to experiments, females most likely imprinted on themselves, and later used self‐referent phenotype matching to assess potential mating partners. In contrast, neither female nor male choice experiments indicated a preference. Analyses of female and male behavior revealed that in choice experiments, female preference for unrelated males was probably confounded by male competition and/or altered by the different ecological context posed by choice experiments.     

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.