The effects of reproduction on courtship, fertility and longevity within and between alternative male mating tactics of the horned beetle, Onthophagus binodis

Life history theory provides a powerful tool to study an organism's biology within an evolutionary framework. The notion that males face a longevity cost of competing for and displaying to females lies at the core of sexual selection theory. Likewise, recent game theory models of the evolution of ejaculation strategies assume that males face a trade-off between expenditure on the ejaculate and expenditure on gaining additional matings. Males of the dung beetle Onthophagus binodis adopt alternative reproductive tactics in which major males fight for and help provision females, and minor males sneak copulations with females that are guarded by major males. Minor males are always subject to sperm competition, and consistent with theoretical expectation, minor males have a greater expenditure on their ejaculate than major males. We used this model system to seek evidence that mating comes at a cost for future fertility and/or male expenditure on courtship and attractiveness, and to establish whether these traits vary between alternative mating tactics. We monitored the lifespan of males exposed to females and nonmating populations, and sampled males throughout their lives to assess their fertility and courtship behaviour. We found a significant longevity cost of reproduction, but no fertility cost. On average, males from mating populations had a lower courtship rate than those from nonmating populations. This small effect, although statistically nonsignificant, was associated with significant increases in the time males required to achieve mating. Minor males had lower courtship rates than major males, and took longer to achieve mating. Although we did not measure ejaculate expenditure in this study, the correlation between lower courtship rate and longer mating speed of minor males documented here with their greater expenditure on the ejaculate found in previous studies, is consistent with game theory models of ejaculate expenditure which assume that males trade expenditure on gaining matings for expenditure on gaining fertilizations.     

Effects of multiple mating on the fecundity of an invasive pest (Octodonta nipae): the existence of an intermediate optimal female mating rate

Multiple mating is found in many insect taxa where both of the sexes can mate more than once. For males, this leads to the advantage of increasing their paternity by fertilizing more females. However, there is a trade‐off of resource allocation between reproduction and other life‐history characters. In the present study, the impact of increased mating rate on reproductive fitness of the invasive nipa palm hispid beetle Octodonta nipae Maulik (Coleoptera: Chrysomelidae) is investigated. A series of mating frequencies (i.e. 1, 5, 10, 15, 20 times) is selected from video frame playback, ranking from the minimum to maximum mating rate observed under laboratory conditions over a given time period. Fecundity parameters such as lifetime egg production, egg‐hatching rate, effective oviposition period and longevity are investigated for the evaluation of reproductive efficiency. For female O. nipae, increased fecundity is correlated with the mating frequency. Females mating 15 times lay the largest number of eggs (138.82 ± 6.87) and have a hatching rate of 47.43 ± 4.08%. After mating 20 times, females suffer significant declines in oviposition (90.31 ± 8.38 eggs) and egg‐hatching rate (34.16 ± 4.93%). Moreover, the population growth rate reaches a maximum in the females that mate 15 times. The results show that multiple matings in O. nipae have an intermediate optimal range within which female reproductive success is enhanced, providing empirical evidence for the existence of a trade‐off between costs and benefits during copulation based on resource allocation.     

Mating and longevity in ant males

Across multicellular organisms, the costs of reproduction and self‐maintenance result in a life history trade‐off between fecundity and longevity. Queens of perennial social Hymenoptera are both highly fertile and long‐lived, and thus, this fundamental trade‐off is lacking. Whether social insect males similarly evade the fecundity/longevity trade‐off remains largely unstudied. Wingless males of the ant genus Cardiocondyla stay in their natal colonies throughout their relatively long lives and mate with multiple female sexuals. Here, we show that Cardiocondyla obscurior males that were allowed to mate with large numbers of female sexuals had a shortened life span compared to males that mated at a low frequency or virgin males. Although frequent mating negatively affects longevity, males clearly benefit from a “live fast, die young strategy” by inseminating as many female sexuals as possible at a cost to their own survival.     

Courtship and copulation, but not ejaculates, reduce the longevity of female field crickets (Gryllus bimaculatus)

Females of many taxa incur fitness costs from male sexual coercion and harassment leading to mating. Although male crickets cannot force copulations on females, female Gryllus bimaculatus in this study incurred significant reductions in longevity through being exposed to different levels of male courtship. Virgin females kept in isolation had the longest life spans. Reductions in longevity applied to females in sensory contact with males (without the opportunity to mate), females that courted and mated and females that mated but with fertilization being prevented. Females also incurred significant reductions in longevity when kept with other females, which may have been due to high levels of cannibalism. Consistent with previous studies, females appeared to incur no cost to longevity from receiving sperm or seminal fluid. It is known that female G. bimaculatus benefit genetically from multiple mating. However, this benefit could possibly be offset by the negative effect that male courtship and mating behaviour has on female longevity.     

Horn growth rate and longevity: implications for natural and artificial selection in thinhorn sheep (Ovis dalli)

We used horn measurements from natural and hunted mortalities of male thinhorn sheep Ovis dalli from Yukon Territory, Canada, to examine the relationship between rapid growth early in life and longevity. We found that rapid growth was associated with reduced longevity for sheep aged 5 years and older for both the hunted and natural mortality data sets. The negative relationship between growth rate and longevity in hunted sheep can at least partially be explained by morphologically biased hunting regulations. The same trend was evident from natural mortalities from populations that were not hunted or underwent very limited hunting, suggesting a naturally imposed mortality cost directly or indirectly associated with rapid growth. Age and growth rate were both positively associated with horn size at death for both data sets, however of the two growth rate appeared to be a better predictor. Large horn size can be achieved both by individuals that grow horns rapidly and by those that have greater longevity, and the trade-off between growth rate and longevity could limit horn size evolution in this species. The similarity in the relationship between growth rate and longevity for hunted and natural mortalities suggests that horn growth rate should not respond to artificial selection. Our study highlights the need for the existence and study of protected populations to properly assess the impacts of selective harvesting.     

Hot and not‐so‐hot females: reproductive state and thermal preferences of female Arizona Bark Scorpions (Centruroides sculpturatus)

For ectotherms, environmental temperatures influence numerous life history characteristics, and the body temperatures (T_b) selected by individuals can affect offspring fitness and parental survival. Reproductive trade‐offs may therefore ensue for gravid females, because temperatures conducive to embryonic development may compromise females' body condition. We tested whether reproduction influenced thermoregulation in female Arizona Bark Scorpions (Centruroides sculpturatus). We predicted that gravid females select higher T_b and thermoregulate more precisely than nonreproductive females. Gravid C. sculpturatus gain body mass throughout gestation, which exposes larger portions of their pleural membrane, possibly increasing their rates of transcuticular water loss in arid environments. Accordingly, we tested whether gravid C. sculpturatus lose water faster than nonreproductive females. We determined the preferred T_b of female scorpions in a thermal gradient and measured water loss rates using flow‐through respirometry. Gravid females preferred significantly higher T_b than nonreproductive females, suggesting that gravid C. sculpturatus alter their thermoregulatory behaviour to promote offspring fitness. However, all scorpions thermoregulated with equal precision, perhaps because arid conditions create selective pressure on all females to thermoregulate effectively. Gravid females lost water faster than nonreproductive animals, indicating that greater exposure of the pleural membrane during gestation enhances the desiccation risk of reproductive females. Our findings suggest that gravid C. sculpturatus experience a trade‐off, whereby selection of higher T_b and increased mass during gestation increase females' susceptibility to water loss, and thus their mortality risk. Elucidating the mechanisms that influence thermal preferences may reveal how reproductive trade‐offs shape the life history of ectotherms in arid environments.     

Intentional multiple mating by females in a species where sneak fertilization circumvents female choice for parental males

This paper describes how individual female ocellated wrasse Symphodus ocellatus distribute their spawning among males and nests in space and time. It is based on previously collected genetic data of larvae from ten different nests (used to reconstruct half and full‐sibling groupings both within and among nests on multiple days) and behavioural data of marked females across the reproductive season. Both the genetic analyses and behavioural observations confirm that female S. ocellatus intentionally engage in multiple mating, by repeatedly spawning at the same nest on different days and at several different nests (up to 12 spawning events over 3 weeks), leading to mixed paternity among her young. The main benefit of such high and intentional multiple mating is probably insurance against brood failure due to nest predation, desertion or poor paternal care by the male. These findings reveal that even in systems where females attempt to avoid male‐controlled mixed paternity, they may still engage in intentional multiple mating due to these potential benefits.     

Heat knockdown resistance and chill‐coma recovery as correlated responses to selection on mating success at high temperature in Drosophila buzzatii

Reproduction and related traits such as mating success are strongly affected by thermal stress. We tested direct and correlated responses to artificial selection in replicated lines of Drosophila buzzatii that were selected for mating success at high temperature. Knockdown resistance at high temperature (KRHT) and chill‐coma recovery (CCR) were tested as correlated selection responses. Virgin flies were allowed to mate for four hours at 33°C in three replicated lines (S lines) to obtain the selected flies and then returned at 25°C to lay eggs. Other three replicated lines were maintained at 25°C without any selection as control (C lines). After 15 selection generations, KRHT and CCR were measured. Both traits were assessed in flies that did not receive any hardening pretreatments as well as in flies that were either heat or cold hardened. Thermotolerance traits showed significant correlated responses with higher KRHT in S than in C lines, both with a heat‐hardening pretreatment and without a heat‐hardening pretreatment. CCR time was longer in S than in C lines both with a cold‐hardening pretreatment and without a cold‐hardening pretreatment. Hardening treatments improved both KRHT and CCR in all cases excepting KRHT in C lines. Overall, KRHT and CCR showed an antagonistic pattern of correlated responses to our selection regime, suggesting either pleiotropy or tightly linked trait‐specific genes partially affecting KRHT and CCR.     

Effect of male and female multiple mating on the fecundity, fertility, and longevity of diamondback moth, Plutella xylostella (L.)

Abstract:  The effect of diamondback moth (DBM), Plutella xylostella (Lep., Plutellidae) male and female multiple mating on fecundity, fertility, and longevity was studied. Males could mate for five times with virgin females during scotophase. The successful copulation rates, fecundity of female, and longevity of both females and males decreased when male mating times increased, whereas copulation duration increased. Correlation coefficient between copulation duration and male mating times was significant ( r  = 0.7358, P = 0.0001, spearman rank-order correlation). There were linear relationships between mating history of males and longevities of males and females, and regression relationships between them were significant. Mated females had similar daily reproductive pattern, which laid the most eggs on the first day after mating in spite of their mates' mating history. Virgin females laid some infertile eggs before they died. Most of the females mated once during their lifespan but 19.9% of females mated twice when one female kept with one male during scotophase. There were no significant differences in the fecundity, fertility and longevity between the single- and twice-mated females. Correlation coefficient between copulation duration and female mating times was not significant ( r  = 0.0860, P = 0.8575). Results suggested that DBM females may be monandrous. Multiple mating did not increase male or female mating fitness.     

Copulation reduces male but not female longevity in Saltella sphondylli (Diptera: Sepsidae)

Mating more than once is extremely costly for females in many species, making the near ubiquity of polyandry difficult to understand. However, evidence of mating costs for males is much rarer. We investigated the effects of copulation on longevity of male and female flies (Saltella sphondylli). We also scrutinized potential fecundity and fertility benefits to females with differing mating history. Copulation per se was found to decrease the longevity of males but not that of females. However, when females were allowed to lay eggs, females that mated died earlier than virgin females, indicating costs of egg production and/or oviposition. Thus, although longevity costs of copulation are higher for males, reproduction is nevertheless costly for females. We also found no differences in fecundity or fertility relative to female mating history. Results suggest that polyandry may be driven by minor costs rather than by major benefits in this species.     

Cost of reproduction in Callosobruchus maculatus: effects of mating on male longevity and the effect of male mating status on female longevity

One of the most studied life-history trade-offs is that resulting from the cost of reproduction: a trade-off arises when reproduction diverts limited resources from other life-history traits. We examine the cost of reproduction in male, and the effect of male mating status on female Callosobruchus maculatus seed beetles. Cost of reproduction for male C. maculatus was manifested as reduced longevity. There was also a positive relationship between male body size and male longevity. Females mated to males that had already copulated twice did not live as long as females mated to males that had copulated once or not at all. The third copulation of males also lasted longer than the two previous ones. We conclude that even though the cost of reproduction for males has been studied much less than that in females, there is growing evidence that male reproductive effort is more complex than has traditionally been thought.     

Flight during oviposition reduces maternal egg provisioning and influences offspring development in Pararge aegeria (L.)

As a result of increased habitat fragmentation in anthropogenic landscapes, flying insects may be required to travel over larger distances in search of resources such as suitable host plants for oviposition. The oögenesis–flight syndrome hypothesis predicts that physiological constraints caused by an overlap in the resources used by thoracic muscles during flight and during oögenesis (e.g. carbohydrates, lipids and water) result in a resource trade‐off, with any resources used during flight no longer available for reproduction. Increased flight costs could therefore potentially result in a decrease in maternal provisioning of eggs. In the present study, the speckled wood butterfly Pararge aegeria (L.) is used to investigate whether increased flight during oviposition results in changes in maternal investment in eggs and whether this contributes to variation in the development of offspring in subsequent life stages. Forcing females to fly during oviposition directly influences egg size and embryonic development time, and indirectly influences (through changes in egg size) egg hatching success and larval development time. These effects are mediated through ‘selfish maternal effects’, with mothers forced to fly maximizing their fecundity at the expense of investment to individual egg size. The present study demonstrates that a change in maternal provisioning as a result of increased flight during oviposition has the potential to exert nongenetic cross‐generational fitness effects in P. aegeria. This could have important consequences for population dynamics, particularly in fragmented anthropogenic landscapes.     

Repeated mating with the same male increases female longevity and fecundity in a polyandrous leaf beetle Galerucella birmanica (Coleoptera: Chrysomelidae)

Female multiple mating (polyandry) is widespread across Insecta, even if mating can be costly to females. To explain the evolution and maintenance of polyandry, several hypotheses, mainly focusing on the material (direct) and/or the genetic (indirect) benefits, have been proposed and empirically tested in many species. Considering only the direct benefits, repeatedly‐mated females are expected to exhibit the same fitness as multiply‐mated females under the same mating frequency. In the present study, we compare the fitness of females received monandrous repeated mating (MM) and polyandrous multiple mating (PM) in a polyandrous leaf beetle Galerucella birmanica and assess female mate preference with regard to polyandry or monandry. Our data indicate that the longevity and the egg‐laying duration of MM females are significantly longer than that of PM females. MM females produce significantly more hatched eggs than PM females over their lifetime under the same mating frequency, which results from the high hatching rate of eggs produced by MM females. PM females mated with novel virgin males in the second mating suffer decreased longevity and lifetime fecundity compared with PM females mated with novel mated males in the second mating. Once‐mated females are more likely to re‐mate with familiar males than novel males. By contrast to expectations, the results of the present study suggest that repeated mating provides females with more direct benefits than multiple mating in G. birmanica, and females prefer to re‐mate with familiar males. The possible causes of this finding are discussed.     

Flight dimorphism is related to survival,reproduction and mating success in the leaf beetle Oreina cacaliae

1. Alternative life histories may be maintained in populations due to variation in the costs and benefits of the underlying strategies. In this study, potential costs of dispersal by flight were investigated as an alternative life‐history strategy in the mountain‐living chrysomelid beetle Oreina cacaliae. 2. In this species, previous mark–recapture studies showed a dispersal dimorphism in both males and females. While a fraction of the population engages in flight in autumn and spring (in the following referred to as ‘flyers’), the other part does not fly (non‐flyers). Flyers emerge earlier than non‐flyers and feed on a spring host plant before the emergence of the main host plant. 3. In this study, the overwintering and dispersal locations were recorded over 7 years in the field, flyers from the spring host plant were collected, and morphology and lifetime reproductive output and survival of collected flyers and non‐flyers were compared. 4. A potential trade‐off between flight and life‐history traits was observed: flyers were smaller in size, lighter in body mass, had a lower lifetime fecundity and a higher mortality. 5. Mating experiments of field‐caught beetles in the laboratory showed that larger beetles had a higher (multiple) mating success, but there was no evidence for size‐assortative mating. It is hypothesized that one reason for small beetles to disperse by flight might be to escape competition for mates with larger non‐flyers. 6. The overwhelming quantity of beetles found on the spring host every year reveals that the flying strategy is successful, despite the costs and risks.     

Effects of delayed mating and male mating history on longevity and reproductive performance of the rice stem borer, Chilo suppressalis (Walker) (Lep., Pyralidae)

Abstract:  The mating potential, effects of delayed mating and male mating history on longevity and reproductive performance of female rice stem borer (RSB), Chilo suppressalis , were investigated under laboratory conditions. Given the opportunity, RSB males copulated an average of 2.7 times, while females generally mated only once. Females were more severely affected by mating delay than males in terms of female longevity and reproductive performance. With increasing age at mating, females' longevity increased, while oviposition period, fecundity and egg fertility decreased. Mean fecundity and egg fertility of females mated 1 and 7 days after emergence were 251.3% and 99.2%, and 96.2% and 75.5% respectively. Both were reduced significantly when female mating was delayed beyond 4 days after emergence. However, irrespective of the first mating age and different mating history of the males, the results indicated that both did not result in a significant difference in the quality of their contributions to female longevity and reproductive performance. The results obtained in this study are discussed in relation to the potential effect on pheromone control of RSB.     

Effects of multiple mating and male eye span on female reproductive output in the stalk-eyed fly, Cyrtodiopsis dalmanni

Females of the stalk-eyed fly, Cyrtodiopsis dalmanni, mate repeatedly during their lifetime and exhibit mating preferencefor males with large eye span. How these mating decisions affectfemale fitness is not fully understood. In this study, we examinedthe effects of multiple mating and male eye span on short-termreproductive output in this species. Experiments that manipulatedthe number of copulations and partners a female received suggested that obtaining a sufficient sperm supply is an important benefitassociated with multiple mating. The average percentage offertile eggs laid by females increased as a function of matingfrequency and ranged from 40% for females mated once, to 80%for females mated continuously. In addition, a high proportionof copulations in this species appeared to be unsuccessful. One-third of all females mated once laid less than 10% fertileeggs. There was no significant difference in reproductive performancebetween females mated to multiple partners and females matedto a single partner. There was also no indication that femalesreceived any short-term reproductive benefits from mating withmales with large eye span. In fact, females mated to males with short eye span laid a higher percentage of fertile eggs thanfemales mated to large eye span males.     

Only helpful when required: a longevity cost of harbouring defensive symbionts

Maternally transmitted symbionts can spread in host populations if they provide a fitness benefit to their hosts. Hamiltonella defensa, a bacterial endosymbiont of aphids, protects hosts against parasitoids but only occurs at moderate frequencies in most aphid populations. This suggests that harbouring this symbiont is also associated with costs, yet the nature of these costs has remained elusive. Here, we demonstrate an important and clearly defined cost: reduced longevity. Experimental infections with six different isolates of H. defensa caused strongly reduced lifespans in two different clones of the black bean aphid, Aphis fabae, resulting in a significantly lower lifetime reproduction. However, the two aphid clones were unequally affected by the presence of H. defensa, and the magnitude of the longevity cost was further determined by genotype × genotype interactions between host and symbiont, which has important consequences for their coevolution.     

Effects of early resource limitation and compensatory growth on lifetime fitness in the ladybird beetle (Harmonia axyridis)

Acceleration of growth following a period of diet restriction may result in either complete or partial catch-up in size. The existence of such compensatory growth indicates that organisms commonly grow at rates below their physiological maxima and this implies a cost for accelerated growth. We examined patterns of accelerated growth in response to temporary resource limitation, and assayed both short and long-term costs of this growth in the ladybird beetle Harmonia axyridis. Subsequent to the period of food restriction, accelerated growth resulted in complete compensation for body sizes, although we observed greater larval mortality during the period of compensation. There were no effects on female fecundity or survivorship within 3 months of maturation. Females did not discriminate against males that had undergone compensatory growth, nor did we observe effects on male mating behaviour. However, individuals that underwent compensatory growth died significantly sooner when deprived of food late in adult life, suggesting that longer-term costs of compensatory growth may be quite mild and detectable only under stressful conditions.     

A cost of maternal care in the dung beetle Onthophagus taurus?

Parental care theory assumes that investment in current offspring will trade against future investment. A number of field studies on birds have used clutch size manipulations to demonstrate a survival cost to chick rearing. However, such studies do not account for costs accrued during earlier stages of reproduction because not all aspects of reproductive effort are manipulated by varying the number of nestlings. In this study, we investigate the effect of reproductive effort on female survival in the dung beetle, Onthophagus taurus. By experimentally manipulating mating status and dung availability, we demonstrate that virgin females survive longer than mated females and that the survival of mated females was negatively associated with the number of brood masses produced. Using a novel manipulation of the mating system, we separated the effects of egg production and maternal care on female survival. Previously, we have shown that females provisioning with the assistance of a major male provide relatively less care than unassisted females. However, paternal assistance did not alter the number of brood masses produced and hence the amount of reproductive effort that was allocated to egg production. Therefore, our finding that female survival was increased when receiving paternal assistance provides, to our knowledge, the first definitive evidence that maternal care reduces female lifespan. These results are of major importance to theoretical models on the evolution of parental care.     

Costs and Benefits of Mating in the Grasshopper Chorthippus parallelus (Caelifera: Acrididae)

Fitness consequences of different levels of mating benefits, viz., (1) virgin, (2) seldom mated, (3) free mating chances with the same male throughout the female's life span, and (4) free mating chances with three males always offered, were investigated in female meadow grasshoppers Chorthippus parallelus. No differences among the treatments were apparent in egg number per pod, total egg number per female, and hatching success of larvae. Seldom-mated females had offspring with the heaviest average larval dry weight. We did not find costs of mating in terms of reduced female longevity and residual dry weight between the treatments.