Factors promoting maternal trophic egg provisioning in non-eusocial animals

The adaptive function of trophic egg-laying is generally regarded as extended parental investment to the offspring. However, the evolutionary factors promoting trophic egg-laying are still unclear, because the amount of maternal investment per offspring should be ideally equal between smaller offspring with trophic eggs and larger offspring without any additional investment. Several authors have suggested that trophic egg-laying should evolve only when egg size is constrained, but this hypothesis has not been evaluated. We investigated the evolutionary mechanisms of trophic egg-laying by two different approaches. First, we evaluated morphological constraints on egg size in two sibling ladybird species, Harmonia axyridis, which is known to produce trophic eggs, and H. yedoensis. Second, we theoretically predicted the optimal proportion of trophic eggs to total eggs and egg size in relation to environmental heterogeneity, predictability of environmental quality, and investment efficiency of trophic egg consumption. The intra- and interspecific morphological comparisons suggest that morphological constraints on the evolutionary determination of egg size are weak at best in the two ladybird species. Moreover, we theoretically showed that small egg size and trophic egg-laying are favoured in heterogeneous environments when mothers cannot adjust egg size plastically. We also showed that even a small reduction in investment efficiency makes a trophic egg strategy unlikely, despite relatively high environmental predictability. We conclude that trophic egg provisioning may be a flexible maternal adaptation to a highly heterogeneous environment rather than a response to a morphological constraint on egg size.     

Trophic-egg production in a subsocial bug: adaptive plasticity in response to resource conditions

Adomerus triguttulus (Heteroptera: Cydnidae) females provision host Lamium spp. seeds to their nymphs. Females also produce trophic eggs, which are inviable and usually function as a food supply for hatched nymphs. Here we report experimental evidence of the potentially adaptive maternal effects of this unusual resource investment. To investigate the effects of food-resource environments on trophic-egg production, we reared females under different resource conditions prior to oviposition and then compared the subsequent allocations of trophic eggs. Females that had been supplied with less-developed seeds produced fewer viable eggs than those supplied with well-developed seeds. However, there was no difference in the number of trophic eggs produced between the two treatments, and thus the trophic-egg ratio, i.e. the number of trophic eggs per viable egg, was higher in females supplied with less-developed seeds. Trophic-egg feeding by hatched nymphs enhances their growth or survival, and a higher trophic-egg ratio would be adaptive particularly under limited resource conditions. In A . triguttulus , adults and offspring depend on the same food resource, i.e. host seeds, and the resource conditions experienced by females prior to oviposition should be well correlated with those experienced later by the offspring. This may enable females to adjust the trophic-egg ratio in response to varying resource environments prior to oviposition.     

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.     

Deposition and longevity of oviposition-deterring pheromone in the cabbage seed weevil

Abstract The cabbage seed weevil ( Ceutorhynchus assimilis Payk.) lays eggs singly into pods of oilseed rape ( Brassica napus L.) through punctures bored with the mouthparts, preferring pods not recently used for oviposition. A simple new choice test has been used to test individual components of egg-laying behaviour for their effect on oviposition site selection. It is confirmed that an oviposition-deterring pheromone (ODP) is deposited during abdomen brushing of the pod which follows egg-laying. Neither pin punctures, weevil feeding punctures, oviposition punctures nor eggs had any deterrent effect. Pods walked on by female weevils were not avoided by those laying eggs. Observations suggest that the ODP is sensed by contact chemoreceptors on the antennae. The deterrent effect lasted only 1–2 h. The implications of these findings on the adaptive significance of the pheromone and its possible use in pest control are discussed.     

Adaptive egg size plasticity for larval competition and its limits in the seed beetle Callosobruchus chinensis

Life‐history theory predicts that females who experienced stressful conditions, such as larval competition or malnutrition, should increase their investment in individual offspring to increase offspring fitness (the adaptive parental hypothesis). In contrast, it has been shown that when females were reared under stressful conditions, they become smaller, which consequently decreases egg size (the parental stress hypothesis). To test whether females adjust their egg volume depending on larval competition, independent of maternal body mass constraint, we used a pest species of stored adzuki beans, Callosobruchus chinensis (L.) (Coleoptera: Chrysomelidae: Bruchinae). The eggs of females reared with competitors were smaller than those of females reared alone, supporting the parental stress hypothesis; however, correcting for female body size, females reared with competitors produced larger eggs than those reared in the absence of competition, supporting the adaptive parental hypothesis, as predicted. The phenotypic plasticity in females' investment in each offspring in stressful environments counteracts the constraint of body size on egg size.     

Trophic niche width,offspring condition and immunity in a raptor species

Strategies developed by organisms to maximize foraging efficiency have a strong influence on fitness. The way in which the range of food resources is exploited has served to classify species, populations and individuals from more specialist (narrow trophic niche) to more generalist (broad trophic niche). Recent studies have provided evidence that many of the considered generalist species/populations are actually composed of different specialist individuals (individual specialization). Even the existence of generalism as an adaptive strategy has been questioned. In this study, we investigated the relationship between trophic niche width, individual quality and offspring viability in a population of common kestrel Falco tinnunculus during 4 years. We showed that the diet of kestrels varied significantly among years and that individuals of better quality fed their offspring with a higher diversity of prey species and a higher amount of food. Moreover, body condition and immune response of nestlings were positively correlated with diversity of prey delivered by parents. Our study suggests that generalism has the potential to increase fitness and that broadening the trophic niche may be an adaptive strategy in unpredictable environments.     

Effects of search experience in a resource-heterogeneous environment on the oviposition decisions of the seed beetle, Callosobruchus maculatus (F.)

Abstract.  1. This study investigates how female seed beetles, Callosobruchus maculatus , distribute their eggs on various-sized seeds when the size of seed was varied during the egg-laying period.
2. Beetles were allowed to lay eggs on one of three arrays of 64 adzuki beans ( Vigna angularis ). Each array contained four size classes of seed, ranging from small (5.0–5.5 mm diameter) to large (6.5–7.0 mm), but differed in how they were distributed within the environment. In the most heterogeneous condition (the 64-patch design), the four sizes were interspersed, while in the least heterogeneous condition (the four-patch design) they were grouped into four separate blocks. Thus, a beetle exploring the 64-patch design would frequently encounter all four seed sizes, whereas a beetle exploring the four-patch design would only rarely encounter a change in bean size.
3. Beetles experiencing greater seed size heterogeneity were more likely to lay eggs on larger seeds, whereas those in the blocked condition were more likely to oviposit on small seeds. Beetle responses to seed size heterogeneity suggest that the degree of preference for large seeds depends on a female's recent experience.
4. Female beetles exhibited size discrimination throughout their egg-laying process; however, there was a trade-off between seed size and egg discrimination (i.e. avoiding those seeds already containing developing eggs) in response to the change in fitness gained from either laying on larger seeds or lower egg-load seeds during the egg-laying process.
5. Our model provides the first evidence that evolving seed size discrimination ability is adaptive for the seed beetle with egg-discrimination ability.     

Neural inhibition of egg-laying in the locust, Locusta migratoria

The role of the oviducal nerves during egg-laying in Locusta migratoria has been examined. Section of the oviducal nerves did not inhibit egg-laying in any observable way. Electrical stimulation of the oviducal nerves resulted in a contraction of the common and lower lateral oviducts which propelled ovulated eggs up towards the ovaries. Recordings from oviducal nerves using chronically implanted electrodes showed that electrical activity was low during actual egg-laying, but high at times when egg-laying was not occurring (i.e. during digging behaviour, or following interruption of egg-laying). During these periods of high activity recurrent bursts of action potentials occurred. Similar patterns of electrical activity were recorded in semi-intact preparations using suction electrodes applied to exposed oviducal nerves of locusts which had been interrupted during the process of egg-laying. High frequency bursts of activity were recorded simultaneously from both left and right oviducal nerves.It is concluded that one function of the oviducal nerves is to inhibit egg-laying at inappropriate times, by inducing contractions of the oviducts which propel eggs back towards the ovaries. These nerves therefore provide a physiological basis for part of the adaptive ovipositional activities of locusts.     

Communal egg-laying behaviour and the consequences of egg aggregation in the brown anole (Anolis sagrei)

Communal nesting is a behaviour that involves multiple females laying eggs in the same nest or nesting site. This behaviour may be a consequence of a shortage of preferable nest sites (constraint hypothesis) or an adaptation generated by fitness benefits associated with egg aggregation (adaptive hypothesis). Experimental tests of these hypotheses require information about maternal nest site choice and its fitness consequences. To address these, we studied a lizard (brown anole; Anolis sagrei) that produces single-egg clutches, but often aggregates eggs in nest sites. In a lab study, females were given the option of nesting in (a) soil previously used as nest substrate vs. fresh soil and (b) soil with eggshells vs. without eggshells. We also experimentally examined the effects of egg aggregation by incubating eggs singly, in groups of four, and in groups of nine. We recorded egg surface temperature, water uptake, and hatchling morphology. Females were more likely to nest in pots with used soil and with eggshells than in pots with fresh soil or without eggshells. We observed no effects of egg aggregation on egg survival, egg temperature, or most measures of hatchling morphology. However, singly-incubated eggs absorbed more water than eggs incubated in the four and nine egg aggregations and this resulted in offspring with greater body condition (i.e. heavier for their length) at hatching. The behavioural experiment demonstrates that females actively choose nest sites that have been used previously (as expected under the adaptive hypothesis), but the egg-aggregation experiment shows no benefits to offspring based on the variables measured. Thus, results of the behaviour study support the adaptive hypothesis; however, results from our egg-incubation study do not. Likely, the adaptive and constraint hypotheses are not mutually exclusive, and a diversity of factors influence the evolution of communal nesting behaviour.     

Nurse eggs form through an active process of apoptosis in the spionid Polydora cornuta (Annelida)

The production of nurse eggs is fundamental to poecilogony in some species of spionid annelids. In species such as Polydora cornuta, nurse-egg production varies among females and ingestion of nurse eggs varies among young, resulting in a form of poecilogony with divergent phenotypes for females (e.g., fecundity and per-offspring investment) as well as for larvae (e.g., trophic mode, size, and stage at hatching). We tested the hypothesis that nurse eggs of P. cornuta form through an active developmental process and specifically, through apoptosis. Results of a TUNEL assay indicate nuclear fragmentation occurs in a process that is characteristic of apoptosis. Cellular indicators of apoptosis in nurse eggs include activation of caspase-3, a positive Annexin V reaction indicating exposure of phosphatidylserine on the outer cell membrane, and invagination of the membrane to form yolk vesicles. These results indicate that formation of nurse eggs in this population of P. cornuta occurs through an active, adaptive process. Furthermore, while apoptosis also occurs in some cells of P. cornuta embryos, it was not detected until later in development. This suggests that nurse eggs originate through heterochrony in a developmental process (apoptosis) that is common to all young of P. cornuta.     

Transgenerational and within-generational induction of defensive morphology in Brachionus calyciflorus (Rotifera): importance of maternal effect

Maternal effects on the induction of defensive morphology are regarded as an adaptive strategy. For instance, a female can transmit environmental conditions related to predation risk to offspring of the same generation or succeeding generations. However, studies have presented limited information regarding such an adaptive maternal effect on monogonont rotifers. In the present study, the maternal effects on the spine development of rotifers were evaluated using Brachionus calyciflorus-Asplanchna models. Asplanchna can release soluble kairomones into the environments, thereby inducing B. calyciflorus to form defensive morphs (e.g., elongated posterolateral spines). Our empirical data supported the hypothesis that an amictic Brachionus-experienced Asplanchna kairomones could produce offspring with longer posterolateral spine in the current or succeeding generation than those of a non-experienced amictic female. On the basis of our data, we speculated that the maternal effect of B. calyciflorus may involve the transfer and dilution of inducers (e.g., hormone) within and between generations. On one hand, our results reinforced the within-generation maternal effects on induction of defensive morphology of rotifers; on the other hand, our results enhanced transgenerational inducible defense to other planktonic taxa that have been only observed in cladocera.     

No evidence that reproductive bumblebee workers reduce the production of new queens

Kin selection theory predicts potential conflict between queen and workers over male parentage in hymenopteran societies headed by one, singly mated queen, because each party is more closely related to its own male offspring. In ‘late-switching’ colonies of the bumblebee Bombus terrestris, i.e. colonies whose queens lay haploid eggs relatively late in the colony cycle, workers start to lay male eggs shortly after the queen lays the female eggs that will develop into new queens. It has been hypothesized that this occurs because workers recognize, via a signal given by the queen instructing female larvae to commence development as queens, that egg laying is now in their kin-selected interest. This hypothesis assumes that aggressive behaviour in egg-laying workers does not substantially reduce the production of new queens, which would decrease the workers' fitness payoff from producing males. We tested the hypothesis that reproductive activity inB. terrestris workers does not reduce the production of new queens. We used microsatellite genotyping to sex eggs and hence to select eight size-matched pairs of ‘late-switching’ colonies from a set of commercial colonies. From one colony of each pair we removed every egg-laying or aggressive worker observed. From the other colony, we simultaneously removed a nonegg-laying, nonaggressive worker. Removed workers were replaced with young workers from separate colonies at equal frequencies within the pair. There was no significant difference in queen productivity between colonies with reduced or normal levels of egg-laying or aggressive workers. Therefore, as predicted, reproductive B. terrestris workers did not significantly reduce the production of new queens.     

Interaction between maternal effects and temperature affects diapause occurrence in the cricket Allonemobius socius

The induction of diapause can be adaptive for egg survival during unfavorable conditions, while direct development can be advantageous under favorable conditions by allowing additional generations to exploit abundant resources. Therefore, the physiological capability of a female to respond to environmental cues indicative of habitat quality by producing eggs of the appropriate developmental phenotype should be under strong selection. Additionally, developing embryos may alter the developmental trajectory initiated by the female in response to changing environmental conditions. In this study, we used a cross-fostering approach to isolate the maternal effects of parental diapause history (not previously studied) and egg-laying temperature from the influence of the incubation environment experienced by the developing embryo on the proportion of diapause eggs produced by the striped ground cricket, Allonemobius socius. We found that an interaction between egg-incubation temperature and parental diapause history strongly affected the proportion of diapause eggs produced and the proportion of eggs that hatched within a 16–18 day incubation period, while egg-laying temperature and all other interactions did not. These novel results indicate that embryos can respond directly to the environmental conditions they experience during development, but that their ability to do so is influenced by maternal effects such as parental diapause history. The results of this study not only provide evidence, for the first time, of parental diapause history affecting diapause proportions, but also raise additional questions about the mechanism by which environmental information is transmitted from parent to offspring and how offspring are able to respond to conditions experienced during their own development.     

Egg size variation in birds with asynchronous hatching: is bigger really better?

In many animals large size at birth enhances offspring survival, but comparative evidence remains equivocal for birds. Failure to consider asynchronous hatching (ASH) may have confounded previous analyses. We assessed effects of egg size and ASH on growth and survival of common grackle (Quiscalus quiscula) nestlings to test the hypothesis that females adjust the size of last-laid eggs to modify effects of ASH. Although positive, the effect of egg size on nestling growth and survival was overwhelmed by the effect of ASH, with late-hatched nestlings being most likely to starve. Egg size did significantly affect growth late in the nestling period, but only because starvation had greatly reduced hatching asynchrony among surviving nestlings. Similarly, in experimentally synchronized nests, egg size and hatching asynchrony both affected offspring growth early in the nestling phase. Our results suggest that there is unlikely to be an adaptive advantage to females from varying the size of last-laid eggs in species with substantial ASH and that studies to assess the effect of a given maternal effect (e.g., varying egg size) should be done in the context of other maternal effects that may be operating simultaneously (e.g., ASH).     

Reproductive biology, family conflict, and size of offspring in marine invertebrates

All organisms face two fundamental trade-offs in the allocation of energetic resources: one between many small versus a few large offspring, and the second between present and future reproduction. Nowhere are these trade-offs more apparent than in the vast range of variation in the sizes of eggs and offspring exhibited among species of marine invertebrates. It has become increasingly clear that, in many taxa of marine organisms, there is also substantial intraspecific variation in the size of eggs and hatchings. This variation has largely been attributed to adaptive maternal effects. In theory, however, the inevitable conflicts of interest that arise in families of sexually reproducing organisms over the optimal distribution of parental resources among siblings could also account for much of this variation in egg and offspring size. Here, we explore the potential impacts of family conflict on offspring traits by comparing the life histories of two exemplar species of marine organisms, the polychaete Boccardia proboscidea and the gastropod Solenosteira macrospira, emphasizing how differences in modes of fertilization and parental care might influence the phenotype and, consequently, the fitness of offspring.     

Life-history variation in selfing multilocus genotypes of the land slug Deroceras laeve (Pulmonata: Agriolimacidae)

The land slug Deroceras laeve shows an enormous variation inlife-history traits. Here, we compared several life-historycharacters (i.e. length of the prereproductive period, growthduring the egg-laying period, number of eggs, hatching success)within and among five selfing homozygous multilocus genotypes(MLG) and investigated a possible trade-off between the numberof eggs produced during the egg-laying period and growth duringthe egg-laying period. Life-history traits were highly variable.There was no significant correlation between slug size and fecundity.Slugs that matured early produced more eggs than slugs thatmatured later. Life-history traits were significantly differentamong MLGs, suggesting that genetic factors may affect and explainat least part of the variation in life-history traits in D.laeve. Finally, we found no evidence of a trade-off betweenthe number of eggs produced during the egg-laying period andgrowth during the egg-laying period. (Received 1 June 2005; accepted 28 October 2005)     

Interaction between maternal effects: onset of incubation and offspring sex in two populations of a passerine bird

Maternal phenotype and maternal environment can profoundly affect the phenotype and fitness of offspring. Yet the causes of variation in such maternal effects are rarely known. Embryos in avian eggs cannot develop without being incubated and this creates an opportunity for maternal control of duration and onset of offspring development. However, females might adjust the start of incubation (e.g., coincident with the first egg or delayed until after egg-laying) in response to environmental conditions that they experience at the time of breeding. We studied two populations of the house finch ( Carpodacus mexicanus) that breed at the climatic extremes of the species' geographical range (Montana and Alabama) and found that in both populations, the timing of incubation onset was closely associated with the bias in the sequence in which male and female eggs were laid within a clutch. When females started incubation with the first egg, they produced sons and daughters in highly biased sequence, when females delayed the onset of incubation until after the egg-laying, the sequence of sons and daughters was not biased. Because in both populations, onset of incubation was associated with the ambient temperature, these results emphasize that maternal effects on offspring can be influenced by ecological conditions experienced by parental generation.     

FIELD STUDIES ON THE INFLUENCE OF WEATHER ON EGG-LAYING BY THE CABBAGE ROOT FLY, ERIOISCHIA BRASSICAE BCHÉ. II

Observations on the intensity and duration of egg-laying by Erioischia brassicae Bché were continued in 1953 on the same site as in 1952. Eggs were first observed on 31 April and the spring peak period of egg-laying lasted from 3 to 30 May with a daily average of 40 eggs/plant. The mean total in spring 1953 was 1287 eggs/plant. Summer peaks occurred on 1–20 July (average 17 eggs/day/plant) and 5–11 August (average 21 eggs/day/plant).
In the field the threshold of reproduction was approximately 60° F. The rate of egg-laying was highest at 65–70° F. and it declined during prolonged periods of higher temperatures.
The annual cycle of generations, as shown by egg counts and confirmed by the examination of puparia, consisted of two generations and a partial third. The spring generation developed without a prolonged diapause, and there was complete emergence during the summer. The overwintering puparia came from the second and third generations of larvae.     

Phylogenetic relationships of the Sparidae (Teleostei: Percoidei) and implications for convergent trophic evolution

A phylogenetic analysis of the majority of sparid genera and representatives of the sparoid families Centracanthidae, Lethrinidae and Nemipteridae is presented using 87 predominately osteological characters. The Sparidae constitute a monophyletic grouping, with the inclusion of the centracanthid Spicara smaris , which nests deep within the ingroup. The phylogeny was then used to investigate agreement with the most recent molecular study, taxonomic stability of subfamilial classification and the evolution of feeding strategies. Results show that the incongruence between morphological and molecular data appears largely to be an artifact of errors in rooting. However, there appears to be real and substantial conflict between the molecular tree and the morphological data, which is not attributable to the different positions of the least congruent taxa. The data support the molecular hypothesis that none of the subfamilial classification, based on dentition and trophic specialization, is monophyletic, and should be rejected pending further taxonomic revision. The phylogeny supports multiple independent origins of trophic types and it is suggested that the evolutionary plasticity of the oral teeth of sparids has been fundamental to the adaptive radiation of this family compared to their closest allies. ©2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 269–301.     

Eggs in autumn: responses to declining incubation temperatures by the eggs of montane lizards

Facultative hatching in response to environmental cues may increase the viability of offspring, if the cue that stimulates hatching also predicts the negative consequences of delayed emergence. Declining incubation temperatures might provide such a cue for montane lizards, because eggs that fail to hatch before winter will perish in the nest. I tested this idea by incubating eggs of an alpine scincid lizard ( Bassiana duperreyi ) in the laboratory. For the first half of the incubation period the eggs were kept at nest temperatures typical of those experienced in summer in the field (daily cycle of 18 ± 7.5°C). I then transferred eggs at weekly intervals into cooler regimes (either 15 ± 7.5°C; or with daytime temperatures unchanged but dropping to 0°C overnight). Contrary to prediction, the eggs did not hatch early. However, transfer to lower temperatures caused only a relatively short delay in hatching, because of a virtual temperature-independence of developmental rates late (but not early) in incubation. Decreasing incubation temperatures also modified hatchling running speeds and post-hatching growth rates, even if the thermal decrease occurred only shortly before the usual time of hatching. These processes plausibly affect hatchling fitness in cold-climate reptiles, and might be adaptations to montane habitats. Alternatively, they may prove to be widespread in other (warmer-climate) reptile taxa, in which case no adaptive hypothesis need be proposed. © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 76 , 71–77.