Oosorption in response to poor food: complexity in the trade-off between reproduction and survival

Plasticity in reproductive physiology is one avenue by which environmental signals, such as poor quality food, can be coordinated with adaptive responses. Insects have the ability to resorb oocytes that are not oviposited. Oosorption is proposed to be an adaptive mechanism to optimize fitness in hostile environments, recouping resources that might otherwise be lost, and reinvesting them into future reproductive potential. We tested the hypothesis that oosorption is an evolved mechanism by which females can reallocate resources from current reproductive effort to survival and future reproduction, when conditions for reproduction are poor, by examining the reproductive physiology and life-history outcome under poor quality food in populations of the milkweed bug (Oncopeltus fasciatus) that have adapted to live on sunflower seed. Females fed a diet of pumpkin seeds, known to be a poor host food, had higher levels of ovarian apoptosis (oosorption), lower reproductive output, but no reduction in life span under poor nutrition, as predicted under the oosorption hypothesis. However, the schedule of reproduction was surprising given the "wait to reproduce" assumption of oosorption as early fecundity was unaffected.     

Effects of mating delay and nutritional signals on resource recycling in a cyclically breeding cockroach

Ovarian apoptosis has been found to occur in the female cockroach Nauphoeta cinerea in response to lack of mates. It has been proposed that ovarian apoptosis in continuously breeding insects is an adaptive mechanism for recouping resources in poor conditions (oosorption). However, N. cinerea is a cyclically breeding insect and ovarian apoptosis may represent ageing and clearance of old unused oocytes. To test the hypothesis that oocyte resorption via apoptosis reflects the reclamation of resources, we delayed mating in combination with positive and negative nutritional signals. Females without access to food during sexual maturation invested less in reproduction and had elevated rates of ovarian apoptosis in the terminal oocyte. Starvation also induced apoptosis in non-vitellogenic oocytes of the vitellarium and germinarium, which would be used for future reproductive events. This is paradoxical as theory states that oosorption is an adaptive means of rerouting resources into investment in future reproduction, yet these oocytes do not represent a cache of resources and their loss could limit future reproduction.     

Phase-related differences in egg production of the migratory locust regulated by differential oosorption through microRNA-34 targeting activinβ

Outbreaks of locust plagues result from the long-term accumulation of high-density egg production. The migratory locust, Locusta migratoria, displays dramatic differences in the egg-laid number with dependence on population density, while solitarious locusts lay more eggs compared to gregarious ones. However, the regulatory mechanism for the egg-laid number difference is unclear. Herein, we confirm that oosorption plays a crucial role in the regulation of egg number through the comparison of physiological and molecular biological profiles in gregarious and solitarious locusts. We find that gregarious oocytes display a 15% higher oosorption ratio than solitarious ones. Activinβ (Actβ) is the most highly upregulated gene in the gregarious terminal oocyte (GTO) compared to solitarious terminal oocyte (STO). Meanwhile, Actβ increases sharply from the normal oocyte (N) to resorption body 1 (RB1) stage during oosorption. The knockdown of Actβ significantly reduces the oosorption ratio by 13% in gregarious locusts, resulting in an increase in the egg-laid number. Based on bioinformatic prediction and experimental verification, microRNA-34 with three isoforms can target Actβ. The microRNAs display higher expression levels in STO than those in GTO and contrasting expression patterns of Actβ from the N to RB1 transition. Overexpression of each miR-34 isoform leads to decreased Actβ levels and significantly reduces the oosorption ratio in gregarious locusts. In contrast, inhibition of the miR-34 isoforms results in increased Actβ levels and eventually elevates the oosorption ratio of solitarious locusts. Our study reports an undescribed mechanism of oosorption through miRNA targeting of a TGFβ ligand and provides new insights into the mechanism of density-dependent reproductive adaption in insects.     

Quantification and ultrastructure of oosorption in Eretmocerus eremicus (Hymenoptera: Aphelinidae)

The potential for and ultrastructure of oosorption were examined in Eretmocerus eremicus, a short-lived whitefly parasitoid that obligately produces anhydropic oocytes. In the absence of hosts, median egg load decreased by approximately 12% per day between 2 days and 8 days following eclosion. Parasitoid mating status had no significant effect on either egg load alone or the relationship between egg load and age. Yolk degradation in E. eremicus is autolytic, with the enzymes required for yolk sphere digestion apparently being derived from within the ooplasm. The exochorion appear to be digested by the follicular epithelium concurrent with the uniform degradation of the entire ooplasm. The potential adaptive benefits of this novel oosorption mechanism to E. eremicus females include a reduction in the total digestion time per oocyte and resorption of chorion remnants. Finally, to our knowledge, the results of this study provide the first unequivocal ultrastructural evidence of a purely autolytic oosorption mechanism in Insecta.     

Oosorption in the stink bug Plautia stali: role of Juvenile hormone in the induction of oosorption

To clarify the role of Juvenile hormone (JH) in the induction of oosorption in females of the stink bug Plautia stali Scott (Heteroptera: Pentatomidae), the effects of extirpation and implantation of the corpus cardiac‐corpus allatum complex (CC‐CA) are examined in fed and starved adults, respectively. Removal of CC‐CA induces oosorption in fed females, whereas CC‐CA implantation stimulates ovary development in starved females. Transection of the nervous connections between the brain and CC‐CA also exerts a stimulatory effect on ovary development. Uptake of yolk protein by the oocytes, assessed in terms of incorporation of a fluorescence dye, occurs on the day after food deprivation but ceases within 1 day after allatectomy. When females are deprived of food, beginning on day 3 of adult life, and treated with JH III skipped bisepoxide (JHSB₃) on the same day, their ovaries develop in a dose‐dependent fashion. Approximately half of the starved females that received JHSB₃ application on day 5 undergo oosorption in the terminal oocytes. This indicates that the critical starvation period for oosorption induction is approximately 2 days, and the earlier half of this period may reflect the time required for the brain to detect poor nutritional condition. During the latter half, in response to food deprivation, the brain inhibits JH biosynthesis by the corpus allatum through nervous connections, resulting in a low JH titre, which in turn induces oosorption.     

Ovary of the golden crab,Chaceon fenneri: I. Post-spawning and oosorption

Oosorption has been considered an important strategy in many invertebrate species which occurs in response to behavioral, ecological, or physiological factors. In crustaceans, the early light microscopic studies of the ovary attributed a role in oosorption to follicle cells, hemocytes, or phagocytes. In this study, ovaries were collected from female golden crabs following spawning and processed for examination by electron microscopy. Following spawning, several unspawned oocytes which had become dissociated from their follicle cells were found in the ovaries. They appeared to be lodged within the lumen. Such oocytes were observed undergoing various stages of autolysis. At no time were hemocytes or recognizable phagocytes found in the lumen of the ovaries or in contact with the degenerating oocytes. Follicle cells which had surrounded the oocytes prior to the time of spawning exhibited disrupted membranes. Resorption of unspawned eggs appears to occur by autolysis of the individual oocytes. Several of the females who had recently spawned had numerous sperm in their ovaries. Such sperm may have been pressed into the lumen at the time of spawning or during the fixation process.     

Preoviposition activation of cathepsin-like proteinases in degenerating ovarian follicles of the mosquito Culex pipiens pallens

Within developing ovaries of many insects, some developing follicles or oocytes usually degenerate (follicular atresia or oosorption), while the others may continue to grow to maturity, thus maintaining the balance between the number of eggs and reproductive circumstances such as available nutrients. To help clarify the phenomenon of follicular atresia during ovarian development, we examined cysteine proteinases stored in mosquito Culex pipiens pallens ovaries. First, analysis using synthesized substrates showed that cathepsin B- and L-like proteinases gradually accumulated in the developing ovaries after a blood meal, which required more than 10 min of preincubation under acidic conditions to reach their maximum activities. However, homogenates of degenerating follicles 3 days after feeding showed proteolytic activities without acid treatment, suggesting that the proteinases had already been activated, while the extract of normally developing follicles collected from the same ovaries required more than 10 min of acid preincubation to reach the optimum activities, suggesting that the enzymes remained as inactive forms. Chemical and immunohistochemical analyses showed that more proteinases are located in the cytoplasm, rather than being associated with yolk granules. Ovarian proteinases, which are believed to become activated at the onset of embryogenesis, should also be activated during oogenesis, presumably to enhance oosorption.     

Oosorption and oocyte loss in a terrestrial isopod under stressful conditions

An increased number of resorbed oocytes was observed in ovaries of terrestrial isopods which were kept under different experimental temperature and photophase regimes compared with those observed in the natural population. Regardless of the nature of the stimulus: high or low temperature or long and short photophases, the female always responded through oosorption. In an iteroparous species such as Porcellio ficulneus B.-L., recruitment of resources for future utilization could be its main response to adverse ambient conditions.     

Egg maturation,oosorption, and wing wear in Gonatocerus ashmeadi (Hymenoptera: Mymaridae), an egg parasitoid of the glassy-winged sharpshooter,Homalodisca vitripennis (Hemiptera: Cicadellidae)

Egg maturation and oosorption in Gonatocerus ashmeadi were investigated in the laboratory and the relationship between hind tibia length (HTL) and <12 h egg load, and wing wear and parasitoid age were determined. G. ashmeadi given access to honey-water and hosts, on average, matured 77 eggs in excess of those they were born with. The number of mature eggs in female G. ashmeadi provided honey-water with no hosts significantly declined after 163 degree-days eggs, while the number of ‘dissolved’ eggs (partially disintegrated mature eggs) increased by nine eggs after 163 degree-days. These results are consistent with oosorption. There was a significant positive correlation between HTL and <12 h egg load. The ovigeny index (the number of mature eggs at female emergence divided by potential lifetime fecundity) for G. ashmeadi was calculated as 0.22 indicating that this parasitoid is a syn-ovigenic species when studied under laboratory conditions. There was a significant positive correlation between wing wear (measured as the number of broken setae per wing) and parasitoid age in the laboratory. The practical implications of these results for G. ashmeadi on the biological control of Homalodisca vitripennis are discussed.     

Lymphocyte Response Depressive Factor in Multiple Sclerosis

Normal serum contains a lymphocyte response depressive factor and this is more active against the lymphocytes of the blood from which the serum was obtained than against lymphocytes from a different normal blood. The suppressive factor is thus “tailor-made” to its own lymphocytes though cross-reactivity with other lymphocytes does occur. The significance of this is discussed. The suppressive factor has a higher titre in serum from patients with multiple sclerosis or other destructive neurological disease than in normal serum. This may be an instance of a general phenomenon in which lymphocyte sensitization is ordinarily accompanied by production of a suppressor factor able to damp down response so that this is controlled by an “acceleratorbrake” mechanism. The possibilities of imbalance in the pathogenesis of disease and therapeutic manipulation of the level of suppressor substance are briefly discussed.     

Oosorption in the stink bug,Plautia crossota stali: induction and vitellogenin dynamics

Oosorption, resorption of developing oocytes in the ovary, in P. c. stali is characterized by changes in appearance of oocytes from opaque greyish green or orange to transparent, degeneration of yolk granules and disappearance of oocyte contents. Starvation and virginity were indicated to be factors that induce oosorption. SDS PAGE/Western blotting analysis using anti-vitellogenin antiserum detected two major and many minor bands in haemolymph samples. Egg extracts showed a more complicated set of positive bands in the same analysis. Yolk protein, vitellin, therefore, seemed to be formed after complicated processing of vitellogenin following its uptake by the oocytes. In starved, oosorption-induced females, vitellogenin concentration in the haemolymph was lower than that of fed females, and Western blotting failed to detect either oosorption-specific or ovary-specific peptide fragments in haemolymph samples collected from those females. These results suggest that once oosorption was induced vitellogenin/vitellin in oocytes was degraded rapidly and released into the haemolymph in the form of amino acids or small peptides too small to be recognized by the anti-vitellogenin antiserum.     

A model for the prestalk/prespore patterning in the slug of the slime mold Dictyostelium discoideum

Abstract. We propose that the prestalk/prespore pattern in Dictyostelium is generated in two steps: In a first process, an intermingled, non-position dependent prestalk/prespore pattern is generated by a cell-restricted autocatalysis and the antagonistic action of a long-ranging substrate which becomes depleted during this autocatalysis. By computer simulations we show that the assumed interaction accounts for several experimentally observed features of the prestalk/ prespore pattern: The size-independent ratio of both cell types, the pattern regulation after removal of one cell type, the development towards one or the other pathway before the slug obtains its final shape or even before aggregation is completed. Our hypothetical substrate may be identical with an experimentally found differentiation-inducing factor (DIF). Alternative molecular realizations of the basic mechanism are discussed. A second process leads to the aggregation of the prestalk cells in a particular region of the aggregate, the future tip region. Interactions which en-able tip formation and the coupling between the prestalk/prespore and the tip-forming system are discussed. Our model shows that the formation of a single large patch of differentiated cells and its size regulation requires conflicting parameters. By a separation into a mechanism which determines the position and a second one which determines the size of a structure, each mechanism can be optimized individually without requiring compromises for the other. Such a separation also seems to occur in other developmental systems.     

The degeneration of asexual haploid populations and the speed of Muller's ratchet

The accumulation of deleterious mutations due to the process known as Muller's ratchet can lead to the degeneration of nonrecombining populations. We present an analytical approximation for the rate at which this process is expected to occur in a haploid population. The approximation is based on a diffusion equation and is valid when N exp(-u/s) > 1, where N is the population size, u is the rate at which deleterious mutations occur, and s is the effect of each mutation on fitness. Simulation results are presented to show that the approximation estimates the rate of the process better than previous approximations for values of mutation rates and selection coefficients that are compatible with the biological data. Under certain conditions, the ratchet can turn at a biologically significant rate when the deterministic equilibrium number of individuals free of mutations is substantially >100. The relevance of this process for the degeneration of Y or neo-Y chromosomes is discussed.     

Sympatric speciation: a simulation model

A model of mating and population growth dependent on competition that suggests circumstances under which sympatric speciation might occur is described. The model is similar to one in a companion paper by Rosenzweig in that a heterozygote genotype, involving a new allele, is first selected by virtue of its ability to exploit a new niche and is then eliminated through competition. The superior competitor, which eliminates the heterozygote, is the homozygote for the new allele. For this process to occur the heterozygote must be sufficiently fit to exploit and invade a new niche, but not so fit that a classical polymorphism results from heterozygous advantage. This process of speciation is most likely to occur when there are vacant niches. When and where these might occur are discussed.     

Effects of Five Naturally Occurring Sugars on the Longevity,Oogenesis, and Nutrient Accumulation Pattern in Adult Females of the Synovigenic Parasitoid Neochrysocharis formosa (Hymenoptera: Eulophidae)

Neochrysocharis formosa (Westwood) (Hymenoptera: Eulophidae), one of the dominant natural enemies of agromyzid leafminers, is a synovigenic parasitoid. We compared the longevity, oogenesis, and nutrient levels of female wasps provided with 10% solutions of five naturally occurring sugars. All five sugars significantly increased the longevity of female wasps, which was 6.5–9.3-fold higher than that of parasitoids provided with water only. We found no significant difference in longevity of female wasps fed on glucose versus fructose or trehalose versus melezitose, but longevity of wasps fed on glucose or fructose was significantly longer than those fed on trehalose or melezitose. Also, we examined the oosorption capability of wasps fed on the five sugars. Some mature eggs were present in the ovaries of newly emerged females, but these were fully reabsorbed within 72 h when wasps were starved. Once wasps were fed with any of the sugars, the number of mature eggs increased at first and then decreased due to oosorption. The longevity and oogenesis dynamics of female wasps fed on five sugars were related with their function of hydrolysis and digestion. As female wasps have no lipogenesis capability, by acquiring exogenous sugars for oogenesis, they can either maintain or exceed the original level of capital nutrients held on adult emergence because none of the wasps’ glycogen need be metabolized to burn as sugar.     

Do human eggs attract spermatozoa?

A key process in human fertilization is bringing the two gametes together, so that the complex molecular events involved in sperm and egg interaction can begin. Does nature allow fertilization to occur only as a consequence of a chance collision, or is there a precontact sperm-egg communication? This review summarizes the bioassays used in testing human spermatozoa for chemotaxis, emphasizing the necessity to distinguish between chemotaxis and other accumulation-causing processes, and the results obtained. It demonstrates that human sperm chemotaxis to a follicular factor(s) does occur, at least in vitro, and that only capacitated spermatozoa are chemotactically responsive. Substances that have been proposed as attractants for human spermatozoa are reassessed. The potential role of sperm chemotaxis in vivo is discussed. Faulty precontact sperm-egg communication may be one of the causes of male infertility, female infertility, or both. On the other hand, interfering with human sperm chemotaxis may represent an exciting new approach to contraception. BioEssays 21:203–210, 1999. © 1999 John Wiley & Sons, Inc.     

N-ethylmaleimide sensitive factor is required for fusion of the C. elegans uterine anchor cell

The fusion of the Caenorhabditis elegans uterine anchor cell (AC) with the uterine-seam cell (utse) is an excellent model system for studying cell-cell fusion, which is essential to animal development. We obtained an egg-laying defective (Egl) mutant in which the AC fails to fuse with the utse. This defect is highly specific: other aspects of utse development and other cell fusions appear to occur normally. We find that defect is due to a missense mutation in the nsf-1 gene, which encodes N-ethylmaleimide-sensitive factor (NSF), an intracellular membrane fusion factor. There are two NSF-1 isoforms, which are expressed in distinct tissues through two separate promoters. NSF-1L is expressed in the uterus, including the AC. We find that nsf-1 is required cell-autonomously in the AC for its fusion with the utse. Our results establish AC fusion as a paradigm for studying cell fusion at single cell resolution and demonstrate that the NSF ATPase is a key player in this process.     

An inhibin-like factor in the testes of fetal and newborn rats

A factor of protein nature that inhibits the proliferation of gonocytes and, probably, their ingress into meiosis and stimulates the development of some components of the blood-testicular barrier was isolated from the testis of 19-20-day-old fetuses and young rats of the first two weeks of life. It is assumed that the inhibin-like factor is formed in the testicular network. The time at which the receptors for the factor under discussion may occur in the cells of the testis of Wistar rat fetuses is discussed.