Intraclutch egg‐size variation in acanthosomatid bugs: adaptive allocation of maternal investment?

If there are differences in predation risk among the offspring within a clutch, parents may allocate less resources to the offspring facing higher risk. I examined parental investment in terms of egg size within clutches in five species of stink bugs (Heteroptera, Acanthosomatidae). In subsocial Elasmucha and Sastragala species, the female guards her eggs and first-instar nymphs against invertebrate predators by covering her clutch with her body. Large differences in survival from predation between offspring at the centre and offspring at the periphery of the clutch have been reported in such subsocial insects. I found that Elasmucha and Sastragala females laid significantly smaller eggs in the peripheral (and thus more vulnerable) part of the clutch. Phenotypic trade-offs between egg size and clutch size were detected in these subsocial species. Egg size was positively correlated with hatched first-instar nymph size: smaller nymphs hatched from smaller peripheral eggs. In asocial Elasmostethus humeralis , however, no significant difference in size was detected between the eggs at the centre of and those at the periphery of the clutch. Thus, in subsocial acanthosomatid bugs, females seem to allocate their resources according to the different predation risks faced by the offspring within the clutch.     

Temporal variation in reproductive allocation in a shield bug Elasmostethus interstinctus

We investigated changes in the reproductive output and the effect of female phenotype on reproductive parameters in a shield bug Elasmostethus interstinctus (L.) (Heteroptera: Acanthosomatidae) over the whole reproductive period. At the beginning and the middle of the reproductive period eggs were smaller than at the end of the period. Clutch mass and number of eggs per clutch decreased in laying sequence, first clutches being much larger than any of the later ones. Lifetime fecundity correlated positively with female size: large females produced more eggs and lived longer than small ones. Egg size did not vary with female size. Offspring survival until adulthood increased with egg weight. Individuals overwinter before reproduction, and because the nymphs from later-laid eggs have the least time to gather resources before overwintering, it may be important for later-laid eggs to be of high quality. Reproductive allocation varies during the reproductive period; females allocate resources relatively more to offspring number at the beginning of the reproductive period and more to offspring quality at the end of their life.     

Phenotypic selection and function of reproductive behavior in the subsocial bug Elasmucha putoni (Heteroptera: Acanthosomatidae)

To investigate the function of maternal care and determinantsof reproductive success in the subsocial bug Elasmucha putoni (Heteroptera: Acanthosomatidae), I used two different approaches,the measurement of phenotypic selection and female-removalexperiments under conditions differing in biotic-environmentalpressure. For two field populations, unattended eggs and youngernymphs consistently suffered severe predation pressure andattendance by parent females greatly enhanced their survival.In contrast, under enemy-excluded conditions, offspring performance was not reduced in broods without parent females, indicatingthat maternal care functions as a physical defense againstpredators. However, the determinant of female reproductivesuccess in E. putoni in the field was not the care behavioralone. Selection gradient analysis showed that early seasonoviposition and larger clutch size, as well as a longer durationof care by a female, was favored during the breeding episode.This study is the first to evaluate phenotypic selection onparental care and other reproductive traits in arthropods.     

Experiments with Elasmucha grisea L. (Heteroptera: Acanthosomatidae): does a female parent bug lay as many eggs as she can defend?

Females of the parent bug Elasmucha grisea L. (Acanthosomatidae,Heteroptera) defend eggs and small nymphs against invertebratepredators. Predation is the main mortality factor affectingoffspring numbersin this species. Since we found a positivecorrelation between female size and clutch size we tested thehypothesis that a female parent bug lays as many eggs as shecan defend. We manipulated clutch size by removing small andlarge females from their own eggs and giving them another clutch.Small femalesguarding large clutches lost significantly moreeggs than large females guarding small clutches or females inthe two control groups. Large females could defend, on average,16% more eggs against invertebrate predators (mainly ants) thancould small females. We conclude that an ecological factor (predation)limits lutch size in this species and the parent bug lays anoptimal clutch size as determined by the defending ability ofthe female.     

Maternal effects across life stages: larvae experiencing predation risk increase offspring provisioning

1. Maternal provisioning can reduce offspring vulnerability to predators by promoting offspring growth and eliciting of antipredator behaviours. Mothers perceiving predation risk may improve offspring survival if producing larger, higher‐quality offspring. However, empirical evidence suggests that offspring quality is often reduced, probably reflecting predator‐induced physiological costs, or a selfish maternal strategy aimed at producing more offspring by sacrificing their quality. While perception and impact of predators can vary across the prey's life stage, a majority of studies have focused on understanding how reproductive allocation decisions are influenced by the risk of predation during adulthood. 2. In this study, Leptinotarsa decemlineata beetles were used to examine if the risk of predation during the larval stage: (i) impacts the mother's physiological condition, including body mass and metabolic rate; and (ii) alters maternal allocation of reproductive resources to offspring quantity versus quality. 3. Results revealed that L. decemlineata mothers responded to perceived predation risk by producing clutches with fewer but larger eggs, thus increasing offspring provisioning. Surprisingly, while females that had faced predation risk as larva emerged with a similar body mass to control females, they exhibited lower metabolic rates. 4. Although predation risk in L. decemlineata larvae is known to impair their ability to acquire and maintain energy resources, adult females appeared to ameliorate such costs by improving their metabolic efficiency and by allocating more of their limited reproductive resources to produce fewer but better‐quality offspring.     

Adaptive sex allocation in relation to hatching synchrony and offspring quality in house wrens

Increased variance in the reproductive success of males relative to females favors mothers that optimally allocate sons and daughters to maximize their fitness return. In altricial songbirds, one influence on the fitness prospects of offspring arises through the order in which nestlings hatch from their eggs, which affects individual mass and size before nest leaving. In house wrens (Troglodytes aedon), the influence of hatching order depends on the degree of hatching synchrony, with greater variation in nestling mass and size within broods hatching asynchronously than in those hatching synchronously. Early-hatching nestlings in asynchronous broods were heavier and larger than their later-hatching siblings and nestlings in synchronous broods. The effect of hatching order was also sex specific, as the mass of males in asynchronous broods was more strongly influenced by hatching order than the mass of females, with increased variation in the mass of males relative to that of females. As predicted, mothers hatching their eggs asynchronously biased first-laid, first-hatching eggs toward sons and late-laid, late-hatching eggs toward daughters, whereas females hatching their eggs synchronously distributed the sexes randomly among the eggs of their clutch. We conclude that females allocate the sex of their offspring among the eggs of their clutch in a manner that maximizes their own fitness.     

Effects of trophic-eggs on offspring performance and rivalry in a sub-social bug

Trophic eggs, which are inviable and usually function as a food supply for offspring, have been regarded as extended parental investment or the outcome of parent–offspring conflict in sibling oophagy. Adomerus triguttulus (Heteroptera: Cydnidae) is a sub-social bug showing a complex pattern of maternal care, including progressive provisioning of host seeds and trophic-egg production. To investigate the functions of trophic eggs, we removed trophic eggs from clutches under different resource conditions. The longevity of nymphs was greatly extended by feeding upon trophic eggs when seeds were excluded. When seeds were provided, trophic-egg feeding by nymphs enhanced their development, but there were no significant effects on brood survival. Some viable eggs were also fed upon by sibling nymphs. However, there was no difference in the proportion of viable eggs consumed between clutches with and without trophic eggs. Females lay viable eggs within the first oviposition day. The synchronous hatching resulting from this oviposition mode seems to prevent sib-cannibalism. The body size of females affected their relative investment in trophic eggs; larger females produced more viable eggs with relatively fewer trophic eggs. The functions and adaptive allocation of trophic eggs are discussed in light of the two hypotheses mentioned above.     

Ineffective Maternal Care of a Subsocial Bug against a Nymphal Parasitoid: a Possible Consequence of Specialization to Predators

In the subsocial bug Elasmucha putoni, females lay egg masses on leaves of fruit-bearing wild mulberry trees. Parent females invariably remained straddling their offspring until the offspring moulted to the second instar on natal leaves. Thereafter, the females usually settled on the stem of shoots which harboured second-or-later-instar nymphs feeding on fruit or aggregating on leaves, and faced toward the base of the shoot. To evaluate the effectiveness of maternal attendance on parasitism of nymphs by a braconid wasp, I divided the boughs of each mulberry tree into two experimental groups: a single bough which was isolated from the others by Tanglefoot treatments and on which guarding females were removed from broods before the second instar, and other boughs on which broods were left intact as controls. The experiments showed that nymphal parasitism was not affected by the presence of females. The position and orientation of females attending second-or-later-instar nymphs is probably effective for detecting predators approaching the nymphs by walking along the stem; however, this posture may prevent the females from detecting parasitoids, which fly and land directly on plant parts close to the nymphs. The ineffectiveness of the females in providing defence against the parasitoid is possibly associated with a specialization of the attending posture to pedestrian predators: a parental defensive behaviour specific to these predators may make the offspring more vulnerable to the parasitoid.     

Load Lightening in Southern Lapwings: Group‐Living Mothers Lay Smaller Eggs than Pair‐Living Mothers

Females of some cooperative‐breeding species can decrease their egg investment without costs for their offspring because helpers‐at‐the‐nest compensate for this reduction either by feeding more or by better protecting offspring from predation. We used the southern lapwing (Vanellus chilensis) to evaluate the effects of the presence of helpers on maternal investment. Southern lapwings are cooperative (some breeding pairs are aided by helpers), chick development is precocial, thus adults do not feed the chicks, and adults offer protection from predators through mobbing behaviors. We tested whether southern lapwing females reduced their reproductive investment (i.e. load‐lightening [LL] hypothesis) or increased their investment (i.e. differential allocation hypothesis) when breeding in groups when compared with females that bred in pairs. We found that increased group size was associated with lower egg volume. A significant negative association between the combined egg nutritional investment (yolk, protein, and lipid mass) and group size was observed. Chicks that hatched from eggs laid in nests of groups were also smaller than chicks hatched in nests of pairs. However, there was no relationship between the body mass index of chicks, or clutch size and group size, which suggests that such eggs are, simply, proportionally smaller. Our results support the LL hypothesis even in a situation where adults do not feed the chicks, allowing females to reduce investment in eggs without incurring a cost to their offspring.     

Cascading costs of reproduction in female house wrens induced to lay larger clutches

In many species, females produce fewer offspring than they are capable of rearing, possibly because increases in current reproductive effort come at the expense of a female's own survival and future reproduction. To test this, we induced female house wrens (Troglodytes aedon) to lay more eggs than they normally would and assessed the potential costs of increasing cumulative investment in the three main components of the avian breeding cycle – egg laying, incubation and nestling provisioning. Females with increased clutch sizes reared more offspring in the first brood than controls, but fledged a lower proportion of nestlings. Moreover, nestlings of experimental females were lighter than those of control females as brood size and prefledging mass were negatively correlated. In second broods of the season, when females were not manipulated, experimental females laid the same number of eggs as controls, but experienced an intraseasonal cost through reduced hatchling survival and a lower number of young fledged. Offspring of control and experimental females were equally likely to recruit to the breeding population, although control females produced more recruits per egg laid. The reproductive success of recruits from broods of experimental and control females did not differ. The manipulation also induced interseasonal costs to future reproduction, as experimental females had lower fecundity than controls when breeding at least 2 years after having their reproductive effort experimentally increased. Finally, females producing the modal clutch size of seven eggs in their first broods had the highest lifetime number of fledglings.     

Maternal investment in a spider with suicidal maternal care, Stegodyphus lineatus (Araneae, Eresidae)

Providing parental care is costly for the parent, but generally beneficial for the young whose survival, growth and reproductive value can be increased. Selection should strongly favour an optimal distribution of parental resources, depending on the relationship between the costs and benefits for parents and their offspring. Parental care is characterized by trade offs in investment, for example between egg size and number of young or providing resources at the egg stage versus the post-hatching stage. Females of the spider Stegodyphus lineatus (Eresidae) produce a single small brood with small eggs and provide the young with regurgitated fluid and later, with their body contents via matriphagy. We asked whether females adjust the investment of resources differentially into eggs, regurgitation feeding and matriphagy, and how maternal investment affects the size of the young at dispersal. We followed the growth of young of broods in the lab and in the field and manipulated brood size in order to determine the pattern of resource allocation. We found that brood size was positively correlated with body mass: larger females had larger broods. Females provided 95% of their body mass to the young, allocating more resources to regurgitation than to matriphagy. Females provided regurgitated food to the young according to the brood size, providing less food when the brood was reduced. Maternal resources had a large influence on offspring mass at dispersal, which is likely to affect their future fitness. The study shows the importance of the female's body mass and her resource allocation decisions for her reproductive outcome.     

Within‐female plasticity in sex allocation is associated with a behavioural polyphenism in house wrens

Sex allocation theory assumes individual plasticity in maternal strategies, but few studies have investigated within‐individual changes across environments. In house wrens, differences between nests in the degree of hatching synchrony of eggs represent a behavioural polyphenism in females, and its expression varies with seasonal changes in the environment. Between‐nest differences in hatching asynchrony also create different environments for offspring, and sons are more strongly affected than daughters by sibling competition when hatching occurs asynchronously over several days. Here, we examined variation in hatching asynchrony and sex allocation, and its consequences for offspring fitness. The number and condition of fledglings declined seasonally, and the frequency of asynchronous hatching increased. In broods hatched asynchronously, sons, which are over‐represented in the earlier‐laid eggs, were in better condition than daughters, which are over‐represented in the later‐laid eggs. Nonetheless, asynchronous broods were more productive later within seasons. The proportion of sons in asynchronous broods increased seasonally, whereas there was a seasonal increase in the production of daughters by mothers hatching their eggs synchronously, which was characterized by within‐female changes in offspring sex and not by sex‐biased mortality. As adults, sons from asynchronous broods were in better condition and produced more broods of their own than males from synchronous broods, and both males and females from asynchronous broods had higher lifetime reproductive success than those from synchronous broods. In conclusion, hatching patterns are under maternal control, representing distinct strategies for allocating offspring within broods, and are associated with offspring sex ratios and differences in offspring reproductive success.     

One clutch or two clutches? Fitness correlates of coexisting alternative female life-histories in the European earwig

Whether to reproduce once or multiple times (semelparity vs. iteroparity) is a major life-history decision that organisms have to take. Mode of parity is usually considered a species characteristic. However, recent models suggested that population properties or condition-dependent fitness payoffs could help to maintain both life-history tactics within populations. In arthropods, semelparity was also hypothesised to be a critical pre-adaptation for the evolution of maternal care, semelparous females being predicted to provide more care due to the absence of costs on future reproduction. The aim of this study was to characterize potential fitness payoffs and levels of maternal care in semel- and itero-parous females of the European earwig Forficula auricularia. Based on 15 traits measured in 494 females and their nymphs, our results revealed that iteroparous females laid their first clutch earlier, had more eggs in their first clutch, gained more weight during the 2 weeks following hatching of the first clutch, but produced eggs that developed more slowly than semelparous females. Among iteroparous females, the sizes of first and second clutches were significantly and positively correlated, indicating no investment trade-off between reproductive events. Iteroparous females also provided more food than semelparous ones, a result contrasting with predictions that iteroparity is incompatible with the evolution of maternal care. Finally, a controlled breeding experiment reported full mating compatibility among offspring from females of the two modes of parity, confirming that both types of females belong to one single species. Overall, these results indicate that alternative modes of parity represent coexisting life-history tactics that are likely to be condition-dependent and associated with offspring development and specific levels of maternal care in earwigs.     

Variation of clutch size and trophic egg proportion in a ladybird with and without male-killing bacterial infection

Maternally inherited bacterial endosymbionts can kill male embryos of their arthropod hosts to enhance the transmission efficiency of the endosymbionts. The resources from killed male eggs can be reallocated to infected female hatchlings as additional maternal investment. As a result, the number of offspring per patch and the maternal investment per offspring are expected to differ from the original optimal values for the host mother. Thus, in response to infection, these trait values should be adjusted to maximize the lifetime reproductive success of host females and the fitness of inherited endosymbionts as well. Here, we examined clutch size, egg size, and the proportion of trophic eggs (i.e., production of unhatched eggs, a maternal phenotype) per clutch of host mothers infected with male-killing bacteria. First, we developed a mathematical model to predict the optimal clutch size and trophic egg proportion in uninfected and infected females. Next, we experimentally compared these life-history traits in a ladybird, Harmonia yedoensis, between females infected or uninfected with male-killing Spiroplasma bacteria. Consistent with our predictions, clutch size was larger, egg size was smaller, and trophic egg proportion was lower in infected H. yedoensis females, compared with uninfected females. To our knowledge, this is the first empirical demonstration of variation in these life-history traits depending on infection with bacterial endosymbionts.     

Reproduction in Risky Environments: The Role of Invasive Egg Predators in Ladybird Laying Strategies

Reproductive environments are variable and the resources available for reproduction are finite. If reliable cues about the environment exist, mothers can alter offspring phenotype in a way that increases both offspring and maternal fitness (‘anticipatory maternal effects’—AMEs). Strategic use of AMEs is likely to be important in chemically defended species, where the risk of offspring predation may be modulated by maternal investment in offspring toxin level, albeit at some cost to mothers. Whether mothers adjust offspring toxin levels in response to variation in predation risk is, however, unknown, but is likely to be important when assessing the response of chemically defended species to the recent and pervasive changes in the global predator landscape, driven by the spread of invasive species. Using the chemically defended two-spot ladybird, Adalia bipunctata, we investigated reproductive investment, including egg toxin level, under conditions that varied in the degree of simulated offspring predation risk from larval harlequin ladybirds, Harmonia axyridis. H. axyridis is a highly voracious alien invasive species in the UK and a significant intraguild predator of A. bipunctata. Females laid fewer, larger egg clusters, under conditions of simulated predation risk (P+) than when predator cues were absent (P-), but there was no difference in toxin level between the two treatments. Among P- females, when mean cluster size increased there were concomitant increases in both the mass and toxin concentration of eggs, however when P+ females increased cluster size there was no corresponding increase in egg toxin level. We conclude that, in the face of offspring predation risk, females either withheld toxins or were physiologically constrained, leading to a trade-off between cluster size and egg toxin level. Our results provide the first demonstration that the risk of offspring predation by a novel invasive predator can influence maternal investment in toxins within their offspring.     

Effect of Population Density and Female Body Size on Number and Size of Offspring in a Species with Size‐Dependent Contests over Resources

When size‐dependent contests over resources influence reproductive success, the trade‐off between number and size of offspring depends on the frequency of contests. Under these circumstances, clutch size should decrease and offspring size should increase as contests become more frequent. We tested these predictions with the burying beetle Nicrophorus pustulatus through manipulation of rearing densities. Burying beetles reproduce on small vertebrate carcasses, a rare but high quality food source for the larvae. Large beetles are more likely to win contests over carcasses and gain exclusive access to a carcass. The winner of a contest kills eggs and larvae already present on a carcass. As a result of the rarity of carcasses, burying beetles are unlikely to breed more than once. As predicted, brood size of N. pustulatus decreased with increasing rearing density. Despite a negative correlation between brood size and larval mass, larval mass did not increase with increasing rearing density. This may be due to the special biology of N. pustulatus which can use snake eggs for reproduction. Potentially larger supply of resources and generally small population densities of N. pustulatus may weaken selection on body size and thus the correlation between brood size and larval mass. As size‐dependent constraints can limit reproductive phenotypes, we examined whether female size influenced reproductive phenotype. Small females produced larger broods with smaller, but more variable, offspring than large females. Mechanical constraints of egg size seem an unlikely explanation for the differences because burying beetles can compensate for small egg size through parental care. Energetic constraints may impact small females because body mass and brood size of small females decreased with increasing density. Yet, at all density levels small females produced larger, not smaller, broods than large females. The larger and more variable broods of small females seem to be in agreement with a bet‐hedging strategy.     

Effect of predators and host phenology on the maternal and reproductive behaviors ofGargaphia lace bugs (Hemiptera: Tingidae)

Lace bugs of the genus Gargaphia specialize on taxonomically and ecologically diverse host plants. To examine the impact of predation pressure and host phenology on Gargaphia subsocial and reproductive behavior, we compared G. tiliae, a woodland species restricted to riparian trees in the genus Tilia, and G. solani, a specialist on Solanum in early successional habitats. Both lace bug species exhibit maternal care of eggs and nymphs. Predator densities associated with Solanum were higher than those associated with Tilia and were correlated with higher levels of maternal aggression exhibited by G. solani. In both habitats, artificial exclusion of predators significantly increased nymphal survivorship over maternally guarded broods. Both species reduced the costs associated with maternal care by ovipositing into the egg masses of conspecifics. Gargaphia solani and G. tiliae differed most strikingly in voltinism and thus the potential for iteroparity. Leaf age determined the reproductive future of G. tiliae nymphs independent of photoperiod or temperature. Feeding on plants with young foliage was sufficient to trigger oviposition. Constraints imposed by host plants on life-history patterns and maternal options are discussed.     

Maternal hatching synchronization in a subsocial burrower bug mitigates the risk of future sibling cannibalism

Sibling cannibalism—the killing and consumption of conspecifics within broods—carries a high risk of direct and inclusive fitness loss for parents and offspring. We reported previously that a unique vibrational behavior shown by the mother of the subsocial burrower bug, Adomerus rotundus (Heteroptera: Cydnidae), induced synchronous hatching. Maternal regulation may be one of the most effective mechanisms for preventing or limiting sibling cannibalism. Here, we tested the hypothesis that synchronous hatching induced by maternal vibration in A. rotundus prevents sibling cannibalism. Mothers and their mature egg masses were allocated to three groups: synchronous hatching by maternal vibration (SHmv), synchronous hatching by artificial vibration (SHav), and asynchronous hatching (AH). We then investigated the influence of each hatching strategy on the occurrence of sibling cannibalism of eggs and early‐instar nymphs in the laboratory. No difference in the proportion of eggs cannibalized was observed among the three groups. However, the proportion of nymphs cannibalized was higher in the AH group than in the SHmv group. The difference in the number of days to first molting within clutch was significantly higher in the AH group than in the SHmv group. Junior nymphs were sometimes eaten by senior nymphs. However, immediately after molting, senior nymphs were at a high risk of being eaten by junior nymphs. Our results indicate that synchronous hatching of A. rotundus is necessary to mitigate the risk of sibling cannibalism.     

Females produce larger eggs for large males in a paternal mouthbrooding fish.

When individuals receive different returns from their reproductive investment dependent on mate quality, they are expected to invest more when breeding with higher quality mates. A number of studies over the past decade have shown that females may alter their reproductive effort depending on the quality/attractiveness of their mate. However, to date, despite extensive work on parental investment, such a differential allocation has not been demonstrated in fish. Indeed, so far only two studies from any taxon have suggested that females alter the quality of individual offspring according to the quality/attractiveness of their mate. The banggai cardinal fish is an obligate paternal mouth brooder where females lay few large eggs. It has previously been shown that male size determines clutch weight irrespective of female size in this species. In this study, I investigated whether females perform more courtship displays towards larger males and whether females allocate their reproductive effort depending on the size of their mate by experimentally assigning females to either large or small males. I found that females displayed more towards larger males, thereby suggesting a female preference for larger males. Further, females produced heavier eggs and heavier clutches but not more eggs when paired with large males. My experiments show that females in this species adjust their offspring weight and, thus, presumably offspring quality according to the size of their mate.     

Subsociality and female reproductive success in a mycophagous thrips: An observational and experimental analysis

Oviparous females of the haplodiploid, facultatively viviparous thrips Elaphrothrips tuberculatus(Thysanoptera: Phlaeothripidae) guard their eggs against female conspecifics and other egg predators. The intensity of maternal defense increases with clutch size. Field and laboratory observations indicate that cannibalism by females is an important selective pressure favoring maternal care. Experimental removals of guarding females showed that egg guarding substantially increases egg survivorship and that the survivorship of undefended eggs is higher in the absence of nonguarding female conspecifics than in their presence. The fecundity of viviparous females increases with the number of eggs cannibalized. The reproductive success of oviparous females increases with body size and local food density and decreases with local density of breeding females. Social behavior may not have advanced beyond maternal care in Elaphrothrips tuberculatusbecause, relative to Hymenoptera, capabilities for helping relatives are few or nonexistent, and the causes of variation in female reproductive success are not influenced easily by cooperation among females.