Egg-laying tactic in Phyllomorpha laciniata in the presence of parasitoids

Female insects are expected to choose oviposition sites that have the best conditions for offspring development and survival. Natural enemies, such as predators and parasitoids, may have a strong influence on the selection of oviposition substrates by phytophagous insects. The golden egg bug, Phyllomorpha laciniata (Villers) (Heteroptera: Coreidae) has an unusual reproductive strategy. Females mainly use conspecifics, both males and other females, as egg-laying substrates, but occasionally they oviposit on plants as well. Survival of the eggs is higher when eggs are carried by conspecifics than when they are laid on plants, due to predation and parasitism. We investigated egg-laying behavior in the forced presence of the egg parasitoid Gryon bolivari (Giard) (Hymenoptera: Scelionidae). Specifically, we studied whether females provide egg protection by avoiding oviposition under the risk of egg parasitization. We expected a lower oviposition rate under parasitoid presence, and the eggs, if any, to be placed preferably on conspecifics and not on plants, thus ensuring higher survival of the progeny. The results show that P. laciniata 's egg-laying rate was lower when they were enclosed with parasitoids than when parasitoids were absent, especially when plants were the only substrate to oviposit on. Moreover, females showed strong preference for laying eggs on conspecifics rather than on plants. Egg-laying in P. laciniata appears to be not only influenced by the availability of conspecifics, but also by the presence of egg parasitoids. This indicates that females may be able to detect G. bolivari and avoid oviposition when parasitoids are present. We discuss the possibility of conspecifics as enemy-free space.     

Counterstrategy to Egg Dumping in a Coreid Bug: Recipient Individuals Discard Eggs from Their Backs

The golden egg bug, Phyllomorpha laciniata Vill. (Heteroptera: Coreidae), is the only terrestrial insect in which females oviposit on the backs of female and male conspecifics. Eggs do not survive unless carried by a bug. Herein, I report laboratory observations that egg-carrying individuals actively brush their backs against the host plant seemingly in an effort to rub off eggs. Egg scraping is more common among individuals carrying many eggs than among those carrying only a few eggs. The most recently received eggs were rubbed off first. Females did not avoid laying eggs on the backs of egg-loaded individuals, nor did bugs carrying several eggs resist oviposition attempts more often than unloaded ones. Some males were likely to have fertilized the eggs they scraped off their backs. Laboratory results of active egg removal correspond with egg loss in the field, suggesting that egg scraping may explain egg loss in nature. The data indicate a cost of egg carrying to an individual and an evolutionary arms race between oviposition and discarding behavior.     

Do Golden Egg Bugs (Phyllomorpha laciniata: Heteroptera, Coreidae) Require Conspecifics for Oviposition?

Golden egg bug (Phyllomorpha laciniata) females lay eggs on the bodies of conspecifics of both sexes. We investigated to what extent reproduction depended on the availability of conspecifics as oviposition substrate and the acceptability of the host plant as an alternative oviposition substrate in the absence of conspecifics. Mated females were placed in experimental enclosures each containing a sprig of fresh host plant. Each experimental female was subjected to one of three treatments: isolated from conspecifics (solitary), paired with another female, or paired with a male. Solitary females laid a few eggs on the host plant but then stopped laying eggs, and solitary females laid significantly fewer eggs than those enclosed with another female or a male. Females enclosed with a male laid no more eggs than those enclosed with a female. When two previously isolated females were later enclosed together, they soon renewed oviposition. Females in nature contained significantly more oviducal eggs than did females that were enclosed with other females for a short period. Thus the availability of suitable conspecifics as oviposition substrate stimulates the deposition of mature eggs, and reproduction depends on the presence of conspecifics of either sex as oviposition substrate.     

Host discrimination modulates brood guarding behaviour and the adaptive superparasitism in the parasitoid wasp Trissolcus semistriatus (Hymenoptera: Scelionidae)

Because hosts utilized by parasitoids are vulnerable to further oviposition by conspecifics, host guarding benefits female wasps. The present study aims to test whether female adults regulate brood guarding behaviour by host discrimination in a solitary parasitoid Trissolcus semistriatus by presenting an intact or parasitized host egg mass to a female adult. Virgin females without oviposition experience have host discrimination ability, which enables them to adjust the number of eggs laid in the hosts. Mating experience increases superparasitism by female adults, whereas mated females achieve a higher discrimination ability as a result of oviposition experience and show a lower superparasitism rate. As expected, females exhibit brood guard after parasitizing an intact host egg mass, whereas those females visiting a previously parasitized host egg mass, do not. Because the survival of eggs in superparasitized hosts is relatively low, regulating brood guarding behaviour by host discrimination is adaptive for female wasps.     

Ant predation and the cost of egg carrying in the golden egg bug: experiments in the field

Golden egg bug ( Phyllomorpha laciniata ) females lay eggs on the backs of both female and male conspecifics. Bugs receive eggs voluntarily and involuntarily, and even when males carry eggs, many eggs are not fertilised by the carrier. Carrying the eggs of another individual is unexpected, particularly if egg carrying bears a cost in survival. We examined the predation risk associated with egg carrying experimentally in the field. P . laciniata individuals were enclosed with workers of one of two ant species, Pheidole pallidula or Cataglyphis piliscapus, which co-occur with the bug in the wild. Pheidole pallidula workers preyed on golden egg bugs and their eggs, but Cataglyphis piliscapus workers did not . In P. pallidula enclosures, golden egg bugs carrying larger egg loads were eaten first. These results suggest that golden egg bugs experience high predation pressure and that egg carrying increases the risk of predation. Due to the direct survival costs associated with egg carrying and the lack of relatedness between the eggs and the carrier, we suggest the golden egg bug as the first known intraspecific parasite in which parasitism is not related to active parental care.     

Male brood care without paternity increases mating success

We investigate under which conditions we can expect the evolutionof costly male care for unrelated offspring, when the benefitof such care is in the form of increased mating success. Thisapplies to male helping behavior that cannot be explained aspaternal care because the male's own offspring does not benefitfrom his behavior. Our model shows that caring for others' offspringcan be a stable strategy for males, if a male that does not"help" loses mating opportunities, for example if females discriminateagainst non-helping males as mating partners. This is possiblewhen females are polyandrous. Increasing population densitydecreases the parameter region where male care is stable. Malecare is also more likely to be stable when male mortality rateis higher than that of females. We discuss the results withspecial reference to the golden egg bug Phyllomorpha laciniata,where females lay eggs on conspecifics, often on males beforemating. Males therefore carry mostly unrelated eggs. We investigatehow oviposition rate and female mating rate influences whenegg carrying is an evolutionary stable strategy. We concludethat in the golden egg bug, male egg carrying could be explainedas a form of mating investment.     

Oviposition strategies employed by the western spruce budworm: tests of predictions from the phylogenetic constraints hypothesis

1 Predictions from the Phylogenetic Constraints Hypothesis were tested for the first time in an eruptive forest Lepidopteran species, the western spruce budworm. 2 In previous work, we established that western spruce budworm females exhibit oviposition preferences with regard to tree age, tree vigour and host species. However, there was no evidence to support a link between oviposition preference and larval performance, which supports the Phylogenetic Constraints Hypothesis. 3 Our preference data led us to test whether female budworms use oviposition strategies to select the sites where they lay their egg masses. Our experiments were designed to make direct comparisons between latent and eruptive insect herbivores with respect to two oviposition behaviours: egg retention and avoidance of conspecifics. This type of research has not previously been conducted on any eruptive forest Lepidopteran. 4 Female budworms retained eggs instead of laying them on less preferred hosts in two of three experiments, but the percentage of eggs they retained was significantly less compared to latent insect herbivores. 5 In addition, female budworms actively avoided oviposition in areas with the highest density of conspecific egg masses, but they laid egg masses in all the other locations provided. This contrasts with the pattern seen in latent insect herbivores, which consistently avoid laying their eggs near any sites already used by conspecifics. 6 Our research indicates that there are extreme differences between latent and eruptive insect herbivores with respect to egg retention and avoidance of conspecifics, thus supporting the Phylogenetic Constraints Hypothesis.     

Egg-dumping lace bugs preferentially oviposit with kin

Egg dumping, or abandoning eggs and young to the care of other conspecifics, results in an extreme form of alloparental care. It is unclear, however, if egg dumpers discriminate among kin and nonkin egg recipients. In the lace bug Gargaphia solani (Heteroptera: Tingidae), some females with eggs (guards) also accept and defend eggs of conspecifics. Other females (egg dumpers) abandon their offspring after oviposition, leaving a single guard as the caregiver. We asked if egg dumpers preferentially dump their eggs among unguarded eggs of kin or nonkin. When given a choice between dumping among eggs of full siblings and eggs of nonsiblings, most eggs (67%) were dumped with full siblings' eggs. Furthermore, egg dumpers were just as likely to oviposit among eggs of kin with whom they had interacted on a shared host plant during juvenile development as they were to oviposit with kin reared on different host plants. Thus, egg dumpers discriminate kin by using cues associated with eggs, and such cues are not likely to be acquired through interaction on a common host plant environment. Copyright 2000 The Association for the Study of Animal Behaviour.     

Do male golden egg bugs carry eggs they have fertilized? A microsatellite analysis

In the golden egg bug, Phyllomorpha laciniata (Heteroptera,Coreidae), both males and females carry eggs on their back.Although females cannot carry their own eggs, males may carryeggs that they have fertilized. If males carry eggs they havefertilized, their behavior may be interpreted as paternal care.In this article, we provide genetic data for paternity assignmentof eggs carried by 40 males collected from the field. The malesand the eggs were typed by using four highly polymorphic microsatelliteDNA markers. Out of the 247 eggs typed, 87% were excluded fromthe father-offspring relationship based on single-locus (leastconservative exclusion) mismatches. Under the more conservative(exclusion by at least two single locus mismatches) method,78% of the eggs were nonpaternal. Relatedness estimates furthersupported our paternity analyses. The average relatedness ofthe eggs to the carrying males was low (b_em = -0.052 ±0.024 SE). Within the population, males were unrelated to eachother (b_mm = -0.004 ± 0.0002 SE), as were the eggs carriedby individual males (b_eggs = -0.004 ± 0.0001 SE). Thisfirst genetic study on the breeding system of the golden eggbugs did not find any support for the claim that egg carryingfunctioned as paternal care, nor did it support kin selectionas explanation for conspecific egg carrying.     

Paternity analysis in the golden egg bug using AFLPs: do the males preferentially accept their true genetic offspring?

Abstract.  1. The evolution of parental care and intraspecific parasitism involve conflicts of interest between mothers and other potential care givers who contribute to enhance offspring survival. In the golden egg bug, Phyllomorpha laciniata Villers (Heteroptera: Coreidae), females lay eggs on conspecifics and on plants. The adaptive significance of egg carrying in this species has been the subject of some controversy, which can only be resolved by determining the genetic relationship between the eggs and the adult who carries them. This study examined whether male acceptance of true genetic offspring occurs with a higher frequency than that expected from random oviposition on conspecifics.
2. Paternity analysis, using Amplified Fragment Length Polymorphism (AFLP) markers, was conducted on eggs carried by males housed with field-mated females.
3. Out of the total number of eggs sired by males in the experimental groups, the proportion of eggs carried by males that were their true genetic offspring was 30.8%.
4. Monte Carlo methods show that the probability of a male accepting an egg that is his true genetic offspring is higher than expected if females dumped eggs on males at random.
5. These results suggest that paternal care plays an important role in the maintenance of male egg carrying in this species. In addition, the methodology developed may become useful in determining true genetic parents in other species in which neither the father nor the mother can be determined by observational methods.     

Interpopulation variation in egg size in the winter cherry bug relative to oviposition site selection

To investigate whether or not oviposition on substrates other than host plants (e.g., non‐host plants, abiotic materials) would affect the evolution of egg size in phytophagous insects, we studied the winter cherry bug, Acanthocoris sordidus (Thunberg) (Heteroptera: Coreidae), as a model organism for its interpopulation variation in oviposition preference. The rate of oviposition off host plants is much higher in the Amami Island population than in either the Kyoto or Kochi populations. We compared egg size and number among the three local populations from Kyoto, Kochi, and Amami Island. In addition, to evaluate the adaptive significance of larger eggs for offspring in terms of searching for host plants, we examined the relationship between egg size and first‐instar body size. We also searched for a relationship between egg size and starvation tolerance in the second instars because first instars can develop to second instars without food intake, and thus the substantial host‐searching stage is the second instar, when females lay their eggs off host plants. Females from the Amami population produced fewer larger eggs than females from either the Kyoto or Kochi population. Regardless of the local population, the body size of first instars that emerged from larger eggs was larger, and the second instars originating from larger eggs had a higher starvation tolerance. The larger body size and higher starvation tolerance should enable nymphs to disperse further, which may enhance the probability of successfully reaching host plants. These results suggest that egg size in A. sordidus may be determined in relation to its oviposition habits to maximize reproductive success, resulting in interpopulation variation in egg size.     

Effect of host deprivation on egg quality,egg load,and oviposition in a solitary parasitoid,Chetogena edwardsii (Diptera: Tachinidae)

Solitary parasitoids are limited to laying one egg per host because larvae compete within hosts. If host encounter rate is low, females should not increase the number of eggs/host in response. The tachinid fly, Chetogena edwardsii,was used to evaluate the effect of host deprivation on egg accumulation, oviposition behavior, and egg quality in a solitary parasitoid. Females deprived of hosts for 2– 7 days accumulate about 1 day's supply of eggs. Egg output of deprived females once hosts are restored does not differ from that of control females. Deprived females retain one egg in the uterus where it undergoes embryogenesis. Maggots emerging from retained eggs are more likely to survive in hosts molting in 40 h or less after receipt of an egg than are maggots emerging from eggs fertilized shortly before oviposition. Egg retention is a consequence of host deprivation that permits females to broaden the range of hosts they can exploit to include soon-to-molt hosts and possibly multiply parasitized hosts.     

Sperm competition mechanisms,confidence of paternity,and the evolution of paternal care in the golden egg bug (Phyllomorpha laciniata)

Theoretical models predict how paternal effort should vary depending on confidence of paternity and on the trade-offs between present and future reproduction. In this study we examine patterns of sperm precedence in Phyllomorpha laciniata and how confidence of paternity influences the willingness of males to carry eggs. Female golden egg bugs show a flexible pattern of oviposition behavior, which results in some eggs being carried by adults (mainly males) and some being laid on plants, where mortality rates are very high. Adults are more vulnerable to predators when carrying eggs; thus, it has been suggested that males should only accept eggs if there are chances that at least some of the eggs will be their true genetic offspring. We determined the confidence of paternity for naturally occurring individuals and its variation with the time. Paternity of eggs fertilized by the last males to mate with females previously mated in the field has been determined using amplified fragment length polymorphisms (AFLPs). The exclusion probability was 98%, showing that AFLP markers are suitable for paternity assignment. Sperm mixing seems the most likely mechanism of sperm competition, because the last male to copulate with field females sires an average of 43% of the eggs laid during the next five days. More importantly, the proportion of eggs sired does not change significantly during that period. We argue that intermediate levels of paternity can select for paternal care in this system because: (1) benefits of care in terms of offspring survival are very high; (2) males have nothing to gain from decreasing their parental effort in a given reproductive event because sperm mixing makes it difficult for males to reach high paternity levels and males are left with no cues to assess paternity; (3) males cannot chose to care for their offspring exclusively because they can neither discriminate their own eggs, nor can they predict when their own eggs will be produced; and (4) males suffer no loss of further matings with other females when they carry eggs. Thus, our findings do not support the traditional view that paternal investment is expected to arise only in species where confidence of paternity is high. The results suggest that females maximize the chances that several males will accept eggs at different times by promoting a mechanism of sperm mixing that ensures that all males that have copulated with a female have some chance of fathering offspring, that this probability remains constant with time, and that males have no cues as to when their own offspring will be produced.     

Copulation Is Not a Prerequisite to Male Reception of Eggs in the Golden Egg Bug Phyllomorpha laciniata (Coreidae; Heteroptera)

Females of the golden egg bug, Phyllomorpha laciniata, lay eggs on the backs of conspecifics. Male response to female oviposition attempts is either passive or resistant. Passive males remain still during oviposition, while resistant males move repeatedly and thereby delay or avoid being encumbered. We investigated how previous mating experience affected male acceptance of eggs. Males from two Spanish populations, from Andalusia and Catalonia, were allowed to mate with single females repeatedly. These experimental pairs were then presented with either a single, nonmating male or a pair in copula. We expected mating partners to resist oviposition attempts less strongly than nonmating males but no differences were detected. However, there was a significant difference in behavior exhibited by males from the two populations; males from Catalonia were relatively passive but males from Andalusia routinely resisted encumbrance. Predation pressure and the availability of receptive females may explain the observed differences between the populations.     

Individual Variation in Trophic Egg Production: Evidence for Maternal Manipulation in Response to Resource and Competition Levels

Females of the subsocial shield bug Parastrachia japonensis (Heteroptera: Parastrachiidae) incorporate trophic eggs (nutritive eggs) into their egg mass. Considerable variation occurs among females in trophic egg number and the proportion of an egg mass that is composed of trophic eggs. Because trophic eggs are essential to the development and survival of young, this variation could significantly impact female fitness. We tested the hypothesis that trophic egg abundance is induced by maternal phenotype (weight, body size) and resource exposure. We predicted that resource limitations would cause females to produce fewer fertile eggs and more trophic eggs and that larger and heavier females would produce more of each egg type. Females ovipositing early in the season are exposed to different resource conditions than those that oviposit late. Thus, we compared egg production patterns between these two groups and several other factors related to nesting. No correlation was seen between body size and trophic egg abundance, or, indeed, egg production, overall; however, heavier females produced heavier egg masses. Counter to our prediction, late females, which had greater access to food, produced significantly more total eggs, fewer fertile eggs, and more trophic eggs than early females. A binomial generalized linear model analysis indicated that the factors most correlated with the percentage of an egg mass destined to become trophic eggs were resource abundance, resulting from early or late oviposition, and distance of the nest from the host tree, with closer females producing more trophic eggs. The findings support our hypothesis that resource availability and, to a lesser extent, maternal phenotype affect trophic egg abundance.     

Paternity analysis in an egg‐carrying aquatic insect Appasus major (Hemiptera: Belostomatidae) using microsatellite DNA markers

The giant water bug Appasus major exhibits a peculiar reproductive behavior where females lay eggs on the backs of males. A male and female pair performs frequent repeat copulations during the oviposition behavior, and the male carries the deposited eggs until hatching. Such characteristic behaviors predict that the eggs are fertilized by the brooding males. If males carry eggs of other unrelated males, the egg carrying will drastically decrease the fitness of the carriers. In this study, we examined genetic relationships between the 489 eggs and nine males carrying them collected from the field, using microsatellite DNA markers. We revealed that in total, 28.4% of the eggs were of other male origin. This is the first report of frequent brood parasitism in an aquatic egg‐carrying hemipteran insect. The brood parasitism is adaptive for the females probably because it enables them to increase the chance of oviposition, or it can equalize motility risk of the eggs of each mate.     

Flexible oviposition behavior in the golden egg bug (Phyllomorpha laciniata) and its implications for offspring survival

Female golden egg bugs show unique flexibility in their oviposition behavior. Females can lay eggs on plants, where they are leftunattended, or on the back of conspecifics, where they remainuntil hatching. In this article we show that eggs have greatersurvival rates when carried by an adult than when laid on plants.The main causes of egg mortality are predators and a parasitoidwasp. Our results suggest that, although predation pressureis similar, fewer eggs are attacked by parasitoid wasps whencarried by an adult than when laid on plants. In addition,we show that, when given a choice, females prefer to lay eggson the backs of conspecifics than on plants. Thus, female ovipositionchoice is adaptive and minimizes individual offspring mortality.The factors that may maintain such behavioral variation in current populations are discussed.     

Oviposition and offspring survival within eggs of European corn borer: discrimination of the host embryo by female Trichogramma nubilale

Oviposition preference and offspring survival relative to the location of the host embryo was tested in the egg parasitoid Trichogramma nubilale on European corn borer host eggs. Females preferentially oviposited near to the embryo on hosts about 24 h old. Survival of Trichogramma was lower when females oviposited far from the embryo, and a higher proportion of host embryos hatched. Females did not show preferences for drilling or oviposition within very young hosts relative to where the embryo would develop, and these eggs did not produce wasps or host larvae. Female behavior was apparently adaptive in day-old hosts, not to very young hosts.     

Hydrologic and behavioral constraints on oviposition of stream insects: implications for adult dispersal

The supply of recruits plays an important role in plant and animal population dynamics, and may be governed by environmental and behavioral constraints on animals. Mated females of the mayfly genus Baetis alight on rocks protruding from streams, crawl under water and deposit a single egg mass under a rock. We surveyed oviposition and emergence of a bivoltine population of B. bicaudatus in multiple stream reaches in one high-altitude watershed in western Colorado over 3 years to establish qualitative patterns at a regional scale (entire watershed), and quantitative patterns over six generations at a local scale (one stream reach). We also measured characteristics of preferred oviposition substrates, performed experiments to test hypotheses about cues used by females to select oviposition sites, and measured mortality of egg masses in the field. Our goals were to determine whether: (1) hydrologic variation necessitated dispersal of females to find suitable oviposition sites; (2) the local supply of females could provide the supply of local recruits; and (3) local recruitment determined the local production of adults. The onset of oviposition corresponded with the decline of spring run-off, which differed dramatically among years and among sites within years. However, eggs appeared before any adults had emerged in 8 of 22 site-years, and adults emerged 2-3 weeks before any eggs were oviposited in 3 site-years. Furthermore, the size distribution of egg masses differed from that predicted by the size distribution of females that emerged from seven of nine stream reaches. Protruding rocks and eggs appeared earlier each summer in smaller tributaries than in larger mainstream reaches, suggesting that hydrologic and behavioral constraints on oviposition may force females to disperse away from their natal reach to oviposit, and possibly explain the predominantly upstream flight of Baetis females reported in other studies. Local oviposition rates in one third-order stream-reach increased rapidly as soon as substrates protruded from the water surface, and females preferred large rocks that became available early in the flight season. However, females oviposited on <10% of all available rocks, and <65% of preferred rocks as determined by an empirical model. These data indicated that the timing of appearance of suitable oviposition sites determined the phenology of local recruitment, but that preferred oviposition sites were not saturated. Thus, the magnitude of local recruitment was not limited by the absolute abundance of preferred oviposition sites. Only 22% of egg masses observed in the field suffered mortality during their embryonic development, and per capita Baetis egg mass mortality was significantly lower on rocks with higher densities of egg masses. Thus, we suspect that specialized oviposition behavior may reduce the probability of egg mortality, potentially compensating for the costs of dispersal necessary to locate suitable oviposition sites. Finally, the number of adults that emerged at one stream reach was independent of the number of egg masses oviposited over six generations of Baetis; and local recruitment was not a function of the number of adults of the previous generation that emerged locally. The patterns of oviposition and emergence of Baetis found in this study are consistent with the following hypotheses. Recruitment of eggs in a stream reach is not limited by the local supply of adults, but is a function of the regional supply of dispersing adults, which are constrained by the spatial and temporal distribution of preferred oviposition habitat. Furthermore, subsequent local production of adults is not a function of the supply of recruits, arguing for post-recruitment control of local populations by processes operating in the larval stage (e.g., predation, competition, dispersal, disturbance). Processes affecting larval and adult stages of Baetis act independently and at different scales, thereby decoupling local population dynamics of successive generations.     

Predators induce egg retention in prey

To prevent predation on their eggs, prey often avoid patches occupied by predators. As a result, they need to delay oviposition until they reach predator-free patches. Because many species allocate energy to egg production in a continuous fashion, it is not clear what kind of mechanism prey use to delay oviposition. We used females of the phytoseiid mite Neoseiulus cucumeris to study these mechanisms. Females were placed in patches with pollen, a food source they use for egg production, and they were exposed to another phytoseiid mite, Iphiseius degenerans, which is an intraguild predator of N. cucumeris juveniles. We found that the oviposition of N. cucumeris females on patches with the predator was lower than on patches without the predator. Cues left by the intraguild predator were not sufficient to elicit such behaviour. Females of N. cucumeris reduced oviposition when exposed to the predator by retaining the egg inside their body, resulting in a lower developmental rate once these eggs were laid. Hence, females are capable of retaining eggs, but the development of these eggs continues inside the mother’s body. In this way, females gain some time to search for less risky oviposition sites.