Death feigning as an adaptive anti‐predator behaviour: Further evidence for its evolution from artificial selection and natural populations

Death feigning is considered to be an adaptive antipredator behaviour. Previous studies on Tribolium castaneum have shown that prey which death feign have a fitness advantage over those that do not when using a jumping spider as the predator. Whether these effects are repeatable across species or whether they can be seen in nature is, however, unknown. Therefore, the present study involved two experiments: (a) divergent artificial selection for the duration of death feigning using a related species T. freemani as prey and a predatory bug as predator, demonstrating that previous results are repeatable across both prey and predator species, and (b) comparison of the death‐feigning duration of T. castaneum populations collected from field sites with and without predatory bugs. In the first experiment, T. freemani adults from established selection regimes with longer durations of death feigning had higher survival rates and longer latency to being preyed on when they were placed with predatory bugs than the adults from regimes selected for shorter durations of death feigning. As a result, the adaptive significance of death‐feigning behaviour was demonstrated in another prey–predator system. In the second experiment, wild T. castaneum beetles from populations with predators feigned death longer than wild beetles from predator‐free populations. Combining the results from these two experiments with those from previous studies provided strong evidence that predators drive the evolution of longer death feigning.     

Effects of starvation on death‐feigning in adult Eucryptorrhynchus brandti (Coleoptera: Curculionidae)

In insects, death‐feigning is an effective defence strategy. Eucryptorrhynchus brandti, a major borer pest in China, has a weak flight ability and exhibits obvious death‐feigning behaviour when disturbed. Despite a large number of studies of its biological and ecological properties as well as control methods, the death‐feigning behaviour has not been specifically described. In laboratory conditions, we recorded the survival rate under starvation and feeding conditions and evaluated the effect of starvation on the duration and occurrence of death‐feigning. In a continuous experiment, we examined variation in the death‐feigning duration every day over 7 day. Then, we evaluated the effects of starvation for 3, 6 and 9 day in a non‐continuous experiment and further observed variation in the death‐feigning intensity. We found that starvation significantly affected the survival rate. Survival time was significantly longer in the starvation group than in the feeding group, and females had longer survival times than males (female: 14 day, male: 8 day). In the continuous experiment, starved E. brandti had the longest duration of death‐feigning at 2 day, followed by a significant decrease. In the non‐continuous experiment, the duration and proportion of death‐feigning decreased significantly as the duration of starvation increased and were significantly lower than feeding. These observations suggest that starvation is a non‐negligible factor in the death‐feigning behaviour of E. brandti adults, facilitating the interpretation of future ecological and behavioural data of thanatosis.     

Avoiding Male Harassment: Wing‐Closing Reactions to Flying Individuals by Female Small Copper Butterflies

Males of many butterfly species persistently court and attempt to mate with females even if the females reject courtship. This male harassment almost certainly has negative effects on female fitness. Therefore, females have likely evolved strategies to avoid such encounters. To investigate the harassment avoidance strategy of females of the small copper butterfly, Lycaena phlaeas daimio, I observed the reactions of females to other individuals flying nearby in the field. In response to the conspecific butterflies, females closed their wings if they had previously been open and did not exhibit any action if the wings had been closed. Females that closed their open wings in response to a conspecific received fewer mating attempts than did females that held their wings open. These results indicate that the wing‐closing behaviour of L. phlaeas females functions to deter male mating attempts. The wing‐closing reaction occurred primarily in mated females. Because females of L. phlaeas copulate only once during their lives, this behaviour is not considered an indirect mate choice but rather an attempt to avoid persistent mating attempts (i.e. sexual harassment) by males.     

Egg dumping and life history strategy of Callosobruchus maculatus

Abstract.  Previous studies have demonstrated that female Callosobruchus maculatus adjust oviposition rates to cope with changes in host availability. A female lays fewer eggs when host availability is low, and hence decreases larval competition. However, females will also dump eggs on unsuitable substrates under conditions of host deprivation. Because the female does not feed as an adult, egg dumping possibly wastes energy and may thus be a maladaptive behaviour. In this study, the effect of mating and age on the egg-dumping behaviour and the life history strategy of the female are explored. Under host-deprived conditions, mating is seen to trigger egg-dumping behaviour. Also, females mated at 6 days dump significantly fewer eggs and live longer than females mated at 0 or 3 days. Thus, a trade-off between fecundity and longevity is seen among females subjected to different manipulations. In addition, 6-day-old virgin females contain more mature eggs than females mated at 6 days can produce when deprived of hosts. This finding indicates that the female reallocates internal energy resources by oosorption in a resource-limited environment. To test the maladaptive hypothesis, mated females were deprived of a host for 6 days and then given sufficient hosts each day. The results show that the more eggs dumped by a female in the first 6 days, the more eggs are laid later on beans. Egg dumping is thus not maladaptive.     

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.     

Age at mating and male quality influence female patterns of reproductive investment and survival

The trade‐off between the allocation of resources toward somatic maintenance or reproduction is one of the fundamentals of life history theory and predicts that females invest in offspring at the expense of their longevity or vice versa. Mate quality may also affect life history trade‐offs through mechanisms of sexual conflict; however, few studies have examined the interaction between mate quality and age at first mating in reproductive decisions. Using house crickets (Acheta domesticus), this study examines how survival and reproductive trade‐offs change based on females’ age at first reproduction and exposure to males of varying size. Females were exposed to either a large (presumably high‐quality) or small male at an early (young), middle (intermediate), or advanced (old) age, and longevity and reproductive investment were subsequently tracked. Females mated at a young age had the largest number of eggs but the shortest total lifespans while females mated at older ages produced fewer eggs but had longer total lifespans. The trade‐off between age at first mating and eggs laid appears to be mediated through higher egg‐laying rates and shorter postmating lifespans in females mated later in life. Exposure to small males resulted in shorter lifespans and higher egg‐laying rates for all females indicating that male manipulation of females, presumably through spermatophore contents, varies with male size in this species. Together, these data strongly support a trade‐off between age at first reproduction and lifespan and support the role of sexual conflict in shaping patterns of reproduction.     

The effect of mass‐rearing on death‐feigning behaviour in the sweet potato weevil (Coleoptera: Brentidae)

The aim of our study was to examine the effect of mass‐rearing, in which there is no exposure to predators, on antipredator traits of insects for improving sterile insect technique programs. The duration of death‐feigning (antipredator behaviour) in sweet potato weevil Cylas formicarius (Summers) (Coleoptera: Brentidae) after mass‐rearing for 71 generations were compared with those in wild strain. There was no significant difference in the duration of death‐feigning between wild and mass‐reared strains. This indicated that the death‐feigning behaviour of mass‐reared strain was maintained for 71 generations even in the absence of predators. We discuss the reasons why death‐feigning behaviour is maintained after mass‐rearing.     

Time spent in distinct life history stages has sex‐specific effects on reproductive fitness in wild Atlantic salmon

In species with complex life cycles, life history theory predicts that fitness is affected by conditions encountered in previous life history stages. Here, we use a 4‐year pedigree to investigate if time spent in two distinct life history stages has sex‐specific reproductive fitness consequences in anadromous Atlantic salmon (Salmo salar). We determined the amount of years spent in fresh water as juveniles (freshwater age, FW, measured in years), and years spent in the marine environment as adults (sea age, SW, measured in sea winters) on 264 sexually mature adults collected on a river spawning ground. We then estimated reproductive fitness as the number of offspring (reproductive success) and the number of mates (mating success) using genetic parentage analysis (>5,000 offspring). Sea age is significantly and positively correlated with reproductive and mating success of both sexes whereby older and larger individuals gained the highest reproductive fitness benefits (females: 62.2% increase in offspring/SW and 34.8% increase in mate number/SW; males: 201.9% offspring/SW and 60.3% mates/SW). Younger freshwater age was significantly related to older sea age and thus increased reproductive fitness, but only among females (females: ?33.9% offspring/FW and ?32.4% mates/FW). This result implies that females can obtain higher reproductive fitness by transitioning to the marine environment earlier. In contrast, male mating and reproductive success was unaffected by freshwater age and more males returned at a younger age than females despite the reproductive fitness advantage of later sea age maturation. Our results show that the timing of transitions between juvenile and adult phases has a sex‐specific consequence on female reproductive fitness, demonstrating a life history trade‐off between maturation and reproduction in wild Atlantic salmon.     

Repeatability of dispersal behaviour in a common dwarf spider: evidence for different mechanisms behind short‐ and long‐distance dispersal

Abstract 1. The response of dispersal towards evolution largely depends on its heritability for which upper limits are determined by the trait’s repeatability. 2. In the Linyphiid spider E. atra, we were able to separate long‐ and short‐distance dispersal behaviours (respectively ballooning and rappelling) under laboratory conditions. By performing repeated behavioural trials for females, we show that average dispersal trait values decrease with increasing testing days. By comparing mated and unmated individuals during two periods (before and after mating for the mated group, and the same two periods for the unmated group), we show that mating has no effect on the mean displayed dispersal behaviour or its within‐individual variation. Repeatabilities were high and consistent for ballooning motivation, but not for rappelling. 3. Ballooning motivation can be regarded as highly individual‐specific behaviour, while general pre‐dispersal and rappelling behaviours showed more individual variation. Such difference in repeatability between long‐ and short‐distance dispersal suggests that short‐ and long‐distance dispersal events are triggered by different ecological and evolutionary mechanisms.     

Humidity‐controlled cold storage of Neoseiulus californicus (Acari: Phytoseiidae): effects on male survival and reproductive ability

Humidification can suppress water loss from an organism and has great potential for improving the cold storage of short‐lived arthropods, such as predatory mites. The effectiveness of humidity‐controlled cold storage was recently verified for Neoseiulus californicus (McGregor) females but was not examined for males. Combining both males and females in one storage protocol might increase the predator population because it would enhance the opportunity for multiple mating, which is necessary for females to maximize their egg production. Newly emerged adult males were stored at an air temperature of 5°C and relative humidity (RH) of 100% or 80%. The median survival time (LT₅₀) was 32 days at 100% RH and 14 days at 80% RH; the survival curves differed significantly. Males stored at 100% RH for 0, 10, 20 and 30 days were introduced to virgin females for mating at 25°C to evaluate their reproductive ability. The pre‐oviposition period was significantly prolonged in the females mated with males stored for ≥20 days. No negative effects of storage were observed on the oviposition period, total number of eggs or net reproduction rate (R₀) in the females mated with males stored for ≤20 days or on the mean generation time (T) for those stored for 30 days. A slight decrease in the intrinsic rate of increase (r_m) was observed in the females mated with males stored for ≥20 days. Our storage method can preserve N. californicus males for 20 days with only a minor reduction in their survival and reproductive ability.     

A Behavioral Syndrome in the Adzuki Bean Beetle: Genetic Correlation Among Death Feigning,Activity, and Mating Behavior

When studying animal behavior, it is often necessary to examine traits as a package, rather than as isolated units. Evidence suggests that individuals behave in a consistent manner across different contexts or over time; that is, behavioral syndromes. We compared locomotor activity levels and mating success between beetles derived from two regimes artificially selected for the duration of death‐feigning behavior in the adzuki bean beetle, Callosobruchus chinensis. The two selection regimes comprised strains with higher (L) and lower (S) intensity (frequency and duration) of death‐feigning behavior, respectively. We found that S strains had higher activity levels than L strains for both sexes, i.e., there is a negative genetic correlation between death feigning and activity. In addition, we found that S strains had higher mating success than L strains, presumably due to higher activity, in males but not in females. We thus demonstrate that death feigning is genetically correlated to mating behavior in males but not females in this species, suggesting that behavioral correlations may not always reflect in the same way in both sexes.     

Differential sperm expenditure reveals a possible role for post‐copulatory sexual selection in a lekking moth

Male reproductive success in the lesser wax moth Achroia grisella is strongly determined by pre‐copulatory mate choice, during which females choose among males aggregated in small leks based on the attractiveness of ultrasonic songs. Nothing is known about the potential of post‐copulatory mechanisms to affect male reproductive success. However, there is evidence that females at least occasionally remate with a second male and that males are unable to produce ejaculates quickly after a previous copulation. Here we investigated the effects of mating history on ejaculate size and demonstrate that the number of transferred sperm significantly decreased from first (i.e., virgin) to second (i.e., nonvirgin) copulation within individual males. For males of identical age, the number of sperm transferred was higher in virgin than in nonvirgin copulations, too, demonstrating that mating history, is responsible for the decrease in sperm numbers transferred and not the concomitant age difference. Furthermore, the number of transferred sperm was significantly repeatable within males. The demonstrated variation in ejaculate size both between subsequent copulations as well as among individuals suggests that there is allocation of a possibly limited amount of sperm. Because female fecundity is not limited by sperm availability in this system, post‐copulatory mechanisms, in particular sperm competition, may play a previously underappreciated role in the lesser wax moth mating system.     

Spermatophore and Sperm Allocation in Males of the Monandrous Butterfly Pararge aegeria: the Female’s Perspective

In insects, spermatophore production represents a non‐trivial cost to a male. Non‐virgin males have been shown to produce small spermatophores at subsequent matings. Particularly in monandrous species, it may be an issue to receive a sufficiently large spermatophore at the first and typically only mating. Females of the monandrous Speckled wood butterfly Pararge aegeria (L.) produce fewer offspring after mating with a non‐virgin male. After mating, females spend all their active time selecting oviposition sites and typically ignore other males. Here, we show that females did not discriminate between a virgin male and a recently mated male in our laboratory experiments. We demonstrate that the number of eupyrene sperm bundles relative to spermatophore mass differed with subsequent male matings. Males transferred a significantly smaller spermatophore after the first copulation, but the spermatophore mass did not decrease further with subsequent matings. However, the number of eupyrene sperm bundles decreased linearly. Therefore, there was proportionally more eupyrene sperm in the male’s second spermatophore compared with the first and the later spermatophores. Such a pattern has been shown in polyandrous species. Hence, it suggests that differences in sperm allocation strategy between polyandrous and monandrous butterflies may be quantitative rather than qualitative. There was also a tendency for females that had mated with a recently mated male to have higher propensity to remate than did females that had mated with a virgin male. We discuss the results relative to the mating system in P. aegeria, including female remating opportunities in the field and male mate‐locating behaviour.     

Oxidative damage and plasma antioxidant capacity in relation to body size,age, male sexual traits and female reproductive performance in the collared flycatcher (<Emphasis Type="Italic">Ficedula albicollis</Emphasis>)

The study of oxidative stress is a potential tool for studying the functional interactions among life history traits, sexual traits and physiological status in animals. In this study, we investigated relationships between measures of plasma oxidative status and male sexual traits, female reproductive investment and three other life history traits, in a wild population of collared flycatchers (Ficedula albicollis). Flycatcher males with a larger white forehead patch had higher level of plasma antioxidant capacity. For females, clutch size was not associated with plasma oxidative status, but egg size was positively correlated with antioxidant capacity. The relationship between age and levels of plasma oxidative damage remains controversial in this species: young female flycatchers showed higher levels of hydroperoxides compared to antioxidants, whereas age did not predict oxidative status of males. Males had higher levels of oxidative damage than females, although the concentration of antioxidant compounds was similar between the sexes. Females that mated with more ornamented males had higher plasma antioxidant capacity. Our results suggest that, for males and females, greater investment in sexual signal and reproduction, respectively, does not reduce the capacity for self-maintenance or avoidance of oxidative stress. Finally, our data support indirectly the occurrence of assortative mating in our species, since females with higher plasma antioxidant capacity mated with more ornamented males.     

Female assessment of male functional fertility during mate choice in a promiscuous fish

Sexual selection should favour females that can assess the functional fertility of available sexual partners and avoid mating with recently mated, sperm‐depleted males. Our current understanding of the sensory mechanism(s) underlying female assessment of males based on their functional fertility and avoidance of sperm‐depleted males is incomplete. Female Trinidadian guppies (Poecilia reticulata) are known to avoid mating with males that they had previously observed mating with other females. Here, we investigated experimentally the proximate sensory cues that they use to distinguish between paired size‐ and colour‐matched mated and unmated males in the absence of visual public information on their prior mating histories. When only water‐borne chemical cues from the males were available, females avoided the previously mated male and preferred the unmated one, but they chose randomly when only male visual cues (and no chemical cues) were available. They also preferred unmated over mated males when freely swimming with them in a more sensorially complex environment with multiple male cues (i.e., visual, chemical and mechanical cues) concurrently available. Females exhibited no preference for either stimulus males when both were unmated, irrespectively of the sensory environment. These novel results suggest that, in the absence of prior visual public information on the recent mating histories of males, female guppies use olfactory cues putatively emitted by mated males to avoid mating with them. The source and nature of the implicated olfactory cues and the fitness benefits gained by female guppies in sexually preferring males that have not recently mated remain unknown and warrant further research.     

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.     

Diet and social conditions during sexual maturation have unpredictable influences on female life history trade‐offs

The trade‐off between gametes and soma is central to life history evolution. Oosorption has been proposed as a mechanism by which females can redirect nutrients invested in oocytes into survival when conditions for reproduction are poor. Although positive correlations between oocyte degradation and lifespan have been documented in oviparous insects, the adaptive significance of this process in species with more complex reproductive biology has not been explored. Further, environmental condition is a multivariate state, and combinations of environmental stresses may interact in unpredictable ways. Previous work on the ovoviviparous cockroach, Nauphoeta cinerea, revealed that females manipulated to mate late relative to sexual maturation experience age‐related loss in fecundity because of loss of viable oocytes via apoptosis. This loss in fecundity is correlated with a reduction in female mate choice. Food deprivation while mating is delayed further increases levels of oocyte apoptosis, but the relationship between starvation‐induced apoptosis and life history are unknown. To investigate this, virgin females were either fed or starved from eclosion until provided with a mate at a time known to be suboptimal for fertility. Following mating, females were fed for the duration of their lifespan. We measured lifetime reproductive performance. Contrary to predictions, under conditions of delayed mating opportunity, starved females had greater fecundity, gave birth to more high‐quality offspring and had increased longevity compared with that of fed females. We suggest that understanding proximal mechanisms underlying life history trade‐offs, including the function of oocyte apoptosis, and how these mechanisms respond to varied environmental conditions is critical.     

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.     

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.     

The influence of maternal age and mating frequency on egg size and offspring performance in Callosobruchus maculatus (Coleoptera: Bruchidae)

Maternal age influences offspring quality of many species of insects. This observed maternal age influence on offspring performance may be mediated through maternal age effects on egg size, which in turn may be directly influenced by the female's nutritional state. Thus, behaviors that influence a female's nutritional status will indirectly influence egg size, and possibly offspring life histories. Because males provide nutrients to females in their ejaculate, female mating frequency is one behavior which may influence her nutritional status, and thus the size of her eggs and the performance of her offspring. In this paper, I first quantify the influences of maternal age on egg size and offspring performance of the bruchid beetle, Callosobruchus maculatus. I then examine whether nutrients transferred during copulation reduce the magnitude of maternal age effects on egg size and larval performance when mothers are nutrient-stressed. Egg size and egg hatchability decreased, and development time increased, with increasing maternal age. Multiple mating and adult feeding by females both resulted in increased egg size. This increase in egg size of females mated multiply did not translate into reduced development time or increased body size and egg hatchability, but did correlate with improved survivorship of offspring produced by old mothers. Thus, it appears that because the influence of mating frequency on egg size is small relative to the influence of maternal age, the influence of nutrients derived from multiple mating on offspring life history is almost undetectable (detected only as a small influence on survivorship). For C. maculatus, female multiple mating has been demonstrated to increase adult female survivorship (Fox 1993a), egg production (Credland and Wright 1989; Fox 1993a), egg size, and larval survivorship, but, contrary to the suggestion of Wasserman and Asami (1985), multiple mating had no detectable influence on offspring development time or body size.