Brood ball size but not egg size correlates with maternal size in a dung beetle,Onthophagus atripennis

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The inhibition of milk synthesis by juvenile hormone in the viviparous cockroach, Diploptera punctata

The brood sac of the viviparous cockroach, Diploptera punctata, synthesizes a protein rich milk which nourishes developing embryos. Milk is first detected in the brood sac (by immunoelectrophoresis) when the embryos begin drinking and continues to increase in parallel with total protein of the brood sac. When embryos cease drinking, both total protein and milk decline in the brood sac. Premature decline in protein and milk content of the brood sac has been observed after treatment with juvenile hormone (from implanted active corpora allata) or a juvenile hormone analogue (ZR 512 applied topically). The fine structure of the brood sac 7 days after corpora allata implant is consistent with that of gland cells which are not actively synthesizing milk. The effect of ZR 512 is detected in decreased milk content of the brood sac after 24 hr of treatment.     

Matrotrophic viviparity constrains microbiome acquisition during gestation in a live‐bearing cockroach,Diploptera punctata

The vertical transmission of microbes from mother to offspring is critical to the survival, development, and health of animals. Invertebrate systems offer unique opportunities to conduct studies on microbiome‐development‐reproduction dynamics since reproductive modes ranging from oviparity to multiple types of viviparity are found in these animals. One such invertebrate is the live‐bearing cockroach, Diploptera punctata. Females carry embryos in their brood sac, which acts as the functional equivalent of the uterus and placenta. In our study, 16S rRNA sequencing was used to characterize maternal and embryonic microbiomes as well as the development of the whole‐body microbiome across nymphal development. We identified 50 phyla and 121 classes overall and found that mothers and their developing embryos had significantly different microbial communities. Of particular interest is the notable lack of diversity in the embryonic microbiome, which is comprised exclusively of Blattabacteria, indicating microbial transmission of only this symbiont during gestation. Our analysis of postnatal development reveals that significant amounts of non‐Blattabacteria species are not able to colonize newborn D. punctata until melanization, after which the microbial community rapidly and dynamically diversifies. While the role of these microbes during development has not been characterized, Blattabacteria must serve a critical role providing specific micronutrients lacking in milk secretions to the embryos during gestation. This research provides insight into the microbiome development, specifically with relation to viviparity, provisioning of milk‐like secretions, and mother–offspring interactions during pregnancy.     

Effects of maternal and embryo characteristics on post-fertilization provisioning in fishes of the genus <Emphasis Type="Italic">Gambusia</Emphasis>

Maternal provisioning of embryos in Gambusia (Poeciliidae) entails both production of large, yolky eggs and mother-to-embryo transfer of nutrients, the latter of which is readily quantified using injection of radiolabeled nutrients. We assayed patterns of nutrient transfer in broods of 26 Gambusia geiseri and 23 Gambusia affinis females, using injection of tritiated leucine. We examined maternal and embryo characteristics affecting the instantaneous rate of transfer and characterized the pattern of transfer to individual embryos within broods. Maternal (female size and condition) and brood characteristics (mean embryo size, developmental stage, brood size) did not predict the mean level of nutrient transfer to embryos in a brood for either species. Within broods, individual provisioning of embryos was not related to developmental stage, but was related to embryo mass in G. affinis with nutrient transfer higher to larger embryos. In addition, overall within-brood variation in nutrient transfer, measured as coefficient of variation in embryo radioactivity, was higher in G. affinis than in G. geiseri.     

The Nesting Behavior of Dawson's Burrowing Bee, Amegilla dawsoni (Hymenoptera: Anthophorini), and the Production of Offspring of Different Sizes

Females of Dawson's burrowing bees have a well-defined brood cell cycle involving cell construction, waxing, provisioning, egg laying, and cell capping. In one study population, nesting bees built smaller brood cells for offspring of lower weight and larger ones for heavier offspring, demonstrating their ability to anticipate the desired size of an offspring at the outset of a brood cell cycle. Furthermore, individual females varied the number of provisioning trips made per brood cell cycle by a factor of two or more, apparently exercising control over the amount of brood provisions supplied to an offspring. The size distribution of emerging males at two widely separated locations in 1997 was nearly identical to that recorded in 1995. These findings suggest that the production of small males (minors) is the result of active female control rather than the product of food shortages that force females to undersupply some brood cells. Female foraging decisions resulted in a bimodal distribution of weights of mature dormant larvae at one site in 1997. However, the times required to complete brood cell cycles at this site were not distributed bimodally. This result stemmed in part from daily variation among females in the duration of their provisioning trips as well as from seasonal variation in provisioning trip times. When provisioning trips lasted longer, females tended to make fewer trips per brood cell cycle, and so were presumably more likely to produce minor sons. As a result, the weight of an offspring was not tightly linked to the time investment required to produce it, making it difficult to compare the relative costs of minors and majors in terms of maternal time investments.     

A review of the ecological parameters and implications of subsociality in Parastrachia japonensis (Hemiptera: Cydnidae), a semelparous species that specializes on a poor resource

Subsocial behavior or postovipositional parental care in insects has evolved in response to a variety of environmental stresses and ranges from briefly guarding eggs after oviposition to elaborate nidification and provisioning behaviors. Investment in parental care bears various costs, and should not continue beyond the point at which the costs to future reproductive success exceed the benefits to current reproductive effort. Progressive provisioning is a rare form of subsociality in insects. Females of the subsocial shield bug Parastrachia japonensis progressively provision their nymph-containing nests with drupes of the single resource, Schoepfia jasminodora, and this provisioning drastically enhances offspring survival. A female rears only one brood throughout her lifetime and continues provisioning the brood until about the third larval stadium, when the female dies. Thus, the female's entire reproductive effort is expressed in the success of that one brood, which suggests a reproductive strategy with enormous costs and risks. Why has such an extreme life history evolved in this species? Here, to answer that question and to contribute to our understanding of the evolutionary implications of subsocial behavior, in particular, progressive provisioning, we review what we have discovered about the ecological parameters of subsociality in this species during a long-term field study. We also discuss these parameters in P. japonensis in reference to other subsocial insects and related species and conclude with a suggestion that semelparity and progressive provisioning in this species are extreme adaptations to evolving complete dependency on an unreliable resource.     

An examination of surface epithelium structures of the embryo across the genus Poeciliopsis (Poeciliidae)

In viviparous, teleost fish, with postfertilization maternal nutrient provisioning, embryonic structures that facilitate maternal‐fetal nutrient transfer are predicted to be present. For the family Poeciliidae, only a handful of morphological studies have explored these embryonic specializations. Here, we present a comparative morphological study in the viviparous poeciliid genus, Poeciliopsis . Using microscopy techniques, we examine the embryonic surface epidermis of Poeciliopsis species that vary in their level of postfertilization maternal nutrient provisioning and placentation across two phylogenetic clades and three independent evolutionary origins of placentation. We focus on surface features of the embryo that may facilitate maternal‐fetal nutrient transfer. Specifically, we studied cell apical‐surface morphology associated with the superficial epithelium that covers the body and sac (yolk and pericardial) of embryos at different developmental stages. Scanning electron microscopy revealed common surface epithelial cells across species, including pavement cells with apical‐surface microridges or microvilli and presumed ionocytes and/or mucus‐secreting cells. For three species, in the mid‐stage embryos, the surface of the body and sac were covered in microvillus epithelium. The remaining species did not display microvillus epithelium at any of the stages examined. Instead, their epithelium of the body and sac were composed of cells with apical‐surface microridges. For all species, in the late stage embryos, the surface of the body proper was composed of apical‐surface microridges in a “fingerprint‐like arrangement.” Despite the differences in the surface epithelium of embryos across Poeciliopsis species and embryonic developmental stages, this variation was not associated with the level of postfertilization maternal nutrient provisioning. We discuss these results in light of previous morphological studies of matrotrophic, teleost fish, phylogenetic relationships of Poeciliopsis species, and our earlier comparative microscopy work on the maternal tissue of the Poeciliopsis placenta.     

Maternal provisioning, sibling rivalry and seed mass variability in the dioecious shrub Rhamnus alpinus

In this paper, we study the sources of variability in seed provisioning in Rhamnus alpinus, a dioecious shrub producing three-seeded fleshy fruits (range 1–4). Discarding position effects in access to resources as a source of variation, since pyrenes are radially oriented inside the fruit, we conducted a pollination experiment, in which different pollen donors were used to make single and mixed pollinations on different female plants. We found strong maternal effects on brood size and seed mass. Although we found no effects of pollen load or pollen source on fruit set, brood size or seed mass, all variables showed enhanced values after multiple pollination treatments. Furthermore, we found an increase of intra-brood variance in seed mass after multiple pollination, suggesting that multiple siring really occurs when multiple donors were involved in pollination, and that sibling rivalry could be a mechanism implicated in seed provisioning, discarding maternal choice as the alternative scenario. Our results on resource provisioning fits with a hierarchical model, since disparities in shares increased down the dominance rank, being the middle sized seed the least sensitive to resource partitioning, and the disparities were reduced when more resources were available in terms of fruit mass. Maternal effects, number of pollen donors, and sibling competition are therefore accounting for seed mass variability in R. alpinus.     

Social biology of the wood-feeding cockroach genus <Emphasis Type="Italic">Salganea</Emphasis> (Dictyoptera,Blaberidae, Panesthiinae): did ovoviviparity prevent the evolution of eusociality in the lineage?

Recent phylogenetic studies indicating that termites are eusocial cockroaches closely related to the genus Cryptocercus have generated fresh interest in wood-feeding Blattaria. Here we summarize the social biology of the wood-feeding genus Salganea (Blaberidae: Panesthiinae). As in Cryptocercus, Salganea exhibits long term, biparental care that includes the defense and feeding of young nymphs. Unlike Cryptocercus, however, Salganea is iteroparous: most studied species reproduce periodically over their lifetime. These divergent reproductive strategies are likely related to parental costs associated with their differing reproductive modes: Cryptocercus is oviparous, while Salganea is ovoviviparous. The pattern of parental investment associated with ovoviviparous reproduction may be one reason why Salganea and other ovoviviparous wood-feeding cockroach lineages did not evolve eusociality. Received 21 August 2007; revised 25 January 2008; accepted 22 Feburary 2008.     

Cuticular hydrocarbon synthesis and its maternal provisioning to embryos in the viviparous cockroach Diploptera punctata

Embryos of the viviparous cockroach Diploptera punctata accumulate large amounts of hydrocarbon (HC) of either maternal or embryonic origin. HC synthesis and its accumulation in maternal and embryonic tissues were measured over the course of gestation. Female abdominal integument was the only tissue that synthesized appreciable amounts of HC in vitro, and did so at an increasing rate from the time of mating to mid-pregnancy, when rates of synthesis declined. The embryos synthesized HC at rates <1% those of the female, showing that the majority of HC detected in and on embryos was of maternal origin. The brood sac that houses the developing embryos did not synthesize HC in vitro, indicating that HC must be transported from the female abdominal integument to the embryos. The mass of female epicuticular HC was constant at approximately 183 microg, while her internal HC increased fourfold from mating to mid-pregnancy, then declined until parturition. The decline in internal HC reflected both declining HC synthesis in the female and greater export to the embryos, as embryonic internal HC increased 250-fold prior to parturition. An external HC coating over the oothecal covering and chorion of the embryos increased to mid-pregnancy, then declined. Unlike oviparous cockroaches, D. punctata females fed throughout the reproductive cycle, reflecting the nutritional demands of continuously provisioning the developing embryos.     

Susceptibility of cockroaches (Gromphadorhina portentosa,Nauphoeta cinerea and Blaptica dubia) exposed to entomopathogenic nematodes

Cockroaches are major pests, vectors of pathogenic bacteria and induce allergies. Current control methods use chemical pesticides, but they can be ineffective and costly and there are reports of resistance in the field; hence new control methods are needed. There are conflicting reports about the susceptibility of cockroaches to entomopathogenic nematodes (EPNs); so we investigated if EPNs could kill several diverse cockroach species, including the Madagascan hissing roach (Gromphadorhina portentosa), the Lobster roach (Nauphoeta cinerea) and Blaptica dubia. Female adult cockroaches were exposed to either commercial products containing Steinernema kraussei or a combination of Heterorhabditis spp. and Steinernema spp. at 50 and 150 nematodes per cm² for 21 days. We also monitored feeding and the numbers of infective juveniles that were produced from each cockroach corpse. We found that S. kraussei were harmless to all cockroach species (at both doses) but when exposed to a mixture of Heterorhabditis spp. and Steinernema spp. B. dubia died after 6 days and its feeding was strongly inhibited. We also found that the mixture of Heterorhabditis spp. and Steinernema spp. could proliferate in the cadavers of B. dubia whilst S. kraussei could only reproduce in G. portentosa and B. dubia but not N. cinerea. In conclusion, S. kraussei was harmless to all three cockroach species but B. dubia was killed when exposed to Heterorhabditis spp. and Steinernema spp., highlighting the differences in the host range of EPNs.     

Fine structural description of the compound eye of the Madagascar 'hissing cockroach'Gromphadorhina portentosa (Dictyoptera: Blaberidae)

The compound eyes of the wingless adults of the Madagascar ‘hissing cockroach’Gromphadorhina portentosa Sachum, 1853 were examined by light and electron microscopy. Each eye contains 2 400‐2 500 mostly hexagonal facets. However, irregularities affecting both shape and size of the ommatidia are relatively common, especially towards the margins of the eye. An individual ommatidium of this eucone type of apposition eye contains eight retinula cells, which give rise to a centrally‐fused, tiered rhabdom. The distal end of the latter is funnel‐shaped and accommodates the proximal end of the cone in its midst. Further below, the rhabdom (then formed by the rhabdomeres of four retinula cells) assumes a squarish profile with microvilli aligned in two directions at right‐angle to each other. Cross sections through the proximal regions of the rhabdom display triangular rhabdom outlines and microvilli (belonging to 3‐4 retinula cells different from those involved in the squarish more distal rhabdom) that run in three directions inclined to one another by 120°. Overall the organization of the eye conforms to the orthopteroid pattern and particularly closely resembles that of the American cockroach Periplaneta americana. However, since G. portentosa possesses fewer ommatidia, this could be a consequence of its inability to fly. On the other hand, the large size of the facets and the voluminous rhabdoms suggest considerable absolute sensitivity and an ability to detect the plane of linearly polarized light. Based on the pattern of microvillus orientations in combination with the crepuscular lifestyle G. portentosa leads and the habitat it occurs in, the prediction is made that this insect uses its green receptors for e‐vector discrimination in the environment of down‐welling light that reaches the forest floor.     

The morphology and independent origin of ovoviviparity in Tiphobia and Lavigeria (Caenogastropoda: Cerithioidea: Paludomidae) from Lake Tanganyika

To better understand the diversification of the endemic thalassoid (i.e. marine-like) cerithioidean gastropods of Lake Tanganyika, as well as the origin and significance of brooding among lake species, we here redescribe the anatomy and ontogeny of the ovoviviparous Tiphobia horei from Lake Tanganyika and compare it to that of Lavigeria sp. A, representing another ovoviviparous lake clade that has acquired a uterine brood pouch independently. Within the phylogenetic framework provided by recent molecular analyses, the distant relation of these two taxa is corroborated by many external and internal anatomical differences. Comparison of the brood pouches demonstrates that they each bear unique features consistent with their independent modification for brooding. Despite representing functionally analogous structures, they also share several similarities in organization likely representing symplesiomorphies of the Lake Tanganyika species flock. The ontogeny is characterized by the presence of a velum and by delayed calcification producing a characteristically wrinkled embryonic cap. Comparison with other brooding cerithioideans reveals that T. horei and Lavigeria sp. A retain many more embryos than other freshwater cerithioideans of comparable size with a uterine brood pouch, possibly facilitated by the presence of longitudinal lamellae. Compartmentalization of the oviduct and delayed calcification is strongly linked to the brooding of embryos.     

Placentation and associated aspects of gestation in the bonnethead shark, Sphyrna tiburo

The left ovary of the bonnethead shark, Sphyrna tiburo, is rudimentary, and the right ovary supplies both oviducts which share a common ostium situated in the falciform ligament. Preceding ovulation the nidamental gland of each oviduct hypertrophies and the caudal two-thirds of each oviduct is modified to form a uterus. In the Florida-Caribbean area Sphyrna tiburo probably mates in March and 3–7 eggs are fertilized in the vicinity of the nidamental gland of each oviduct. The developing embryo is nourished during the first 3–4 months of gestation by yolk stored in its extensive yolk sac. Approximately three and one-half months after fertilization, the distal portion of the yolk sac becomes convoluted and interdigitates with deep folds in the uterine wall to form a yolk-sac placenta. As the placenta develops, the maternal uterine epithelium is reduced from columnar cells to squamous cells, and the foetal yolk-sac epithelium is reduced from columnar and cuboidal cells to squamous cells. Exchange between the maternal and foetal blood systems takes place through maternal endothelium, reduced maternal epithelium, egg-case membrane, reduced foetal epithelium, and foetal endothelium.     

Providing chicks with extra food lowers male but not female provisioning in the House Sparrow Passer domesticus

We assessed whether adult House Sparrows Passer domesticus adjusted their provisioning in response to an experimental increase in the nutritional condition of their nestlings. When we supplemented chicks directly with additional food, male parents, but not female parents, reduced their provisioning. The results for males, but not females, run contrary to a previous experiment in this species. In addition, female provisioning was positively associated with both brood size and the age of the brood. In contrast, whereas male provisioning was positively associated with brood size, males did not increase provisioning as their chicks grew older. Males, but not females, exhibited repeatability in their provisioning. Food supplementation had a larger positive effect upon nestling survival in smaller broods than in larger broods. Overall, there appear to be fundamental differences between males and females in how decisions regarding the level of parental investment in the current brood are made.     

Relative influence of male and female care in determining nestling mass in a migratory songbird

Biparental care is common in birds, with the allocation of effort being highly variable between the sexes. In most songbird species, the female typically provides the most care early in the breeding cycle with both parents providing care when provisioning young. Food provisioning should be directly related to offspring quality; however, the relative influence each parent has on offspring quality has rarely been assessed at the nest level. Consequently, we were interested in assessing the relative influence male and female provisioning has on one measurement of offspring quality, nestling mass, in the black‐throated blue warbler Dendroica caerulescens. Over a six year period, 2003–2008, we collected information on average nestling mass per brood on day 6 of the nestling cycle and parental provisioning rates on day 7 of the nestling cycle from 182 first brood nests on three different study plots. We found that average nestling mass was directly related to male provisioning rate, while it was not related to female provisioning rate. On the other hand, estimated biomass provisioned had little influence on average nestling mass, calling into question its utility in assessing parental quality. Finally, there was some indication that parental influence on average nestling mass was dependent on the other parent's provisioning rate, suggesting that parents work in concert to influence nestling quality.     

Communication in the courtship of a madagascan hissing cockroach. I. Normal courtship

The hissing Madagascar cockroach, Gromphadorhina portentosa, has a prolonged and complex courtship involving signals in several sensory modalities. Courtship was described for 13 pairs of cockroaches and the frequencies and sequencing of 16 behavioural units were analysed. Particular attention was paid to the function and interactions of acoustic, chemical and tactile components. The results indicate that posturing and sound production by males, and antennation by both males and females, are important in courtship. They also suggest that courtship in G. portentosa, rather than depending on a rigid sequence of behaviour determined by a series of discrete releasers, is quite flexible, using ‘behavioural monologues’ by both sexes as a means of achieving transitions from one stage of courtship to the next.     

‘Milk’ secretion for embryogenesis in a viviparous cockroach

The brood sac of viviparous Diploptera punctata is a typical insect integumentary gland which secretes a ‘milk’ containing protein and carbohydrate to nourish the developing embryos. During gestation the secretory cells proliferate organelles of protein synthesis and secretion and brood sac wet weight, protein content, synthetic activity and secretory output increase five- to six-fold ; a maximum of 0.4 mg protein was collected in 24 hr from one brood sac in a later stage of gestation. Following parturition, when secretory activity ceases, these parameters fall markedly, and the secretory cells decrease their mass by autophagic regression. Acid phosphatase has been located histochemically in autolysomes and assayed in brood sac homogenates; activity reaches a maximum five days after parturition.     

Begging behaviour of nestlings and food delivery by parents: the importance of breeding strategy

Studies of begging behaviour and food provisioning have produced contradictory results. Here, I present a new idea that may explain these apparent contradictions based on the fact that in species with brood reduction (brood reducers) some chicks starve, but in species that adjust clutch size (clutch adjusters) all chicks typically survive to fledge. This suggests that parents adopting these different strategies may follow different provisioning rules. In clutch adjusters, parents tend to distribute food equitably among their chicks, preferentially feeding young that are in poorer condition, but in brood reducers parents selectively feed larger chicks independently of begging intensity. Received in revised form: 27 March 2001 Electronic Publication     

Relationships between brood size and offspring body size in an ovoviviparous fish: maternal effects and genetic trade-off

Maternal effects can form an important source of variation in offspring fitness and have important evolutionary and ecological consequences. To explore genetic control for body size of newborn offspring, the present study examined maternal brood size and offspring body size in 14 strains and performed cross experiments in an ovoviviparous fish, guppy. Correlation analyses among the strains indicated that the strains with larger brood size have smaller offspring body size. Diallel and reciprocal crosses among four strains revealed a large maternal, but no paternal, contribution to offspring body size. To examine whether offspring body size is determined by maternal genotypes and whether offspring body size correlates with albinism, backcrosses were performed between a wild-type strain with large offspring body size and an albino strain. Offspring body size differed from both the parental strains in one generation of backcrossing but was not significantly different from the paternal strains after three generations. In the backcross generations, the offspring yielded by albino individuals showed significantly smaller body size than those yielded by normal individuals. These results indicated that offspring body size is determined by maternal genotypes, suggesting that offspring body size is influenced by the maternal albinism gene or the maternal locus linked with the albinism locus. The significant negative correlation between maternal brood size and offspring body size detected through our experiments showed that the maternal genetic character of brood size strongly correlated with offspring body size, indicating genetic trade-off between maternal brood size and offspring body size in the guppy.