Female Reproductive Maturation Research Articles

Reproductive Maturity of Cherry Fruit Fly (Diptera: Tephritidae) in Managed and Natural Habitats

We studied the timing of reproductive maturity of cherry fruit fly, Rhagoletis cingulata (Loew), a key pest of sweet and tart cherries in the eastern United States. To determine when cherry fruit fly females become reproductively mature in managed and natural habitats, we deployed traps in sweet and tart cherry orchards and nearby stands of the ancestral host tree, black cherry. Flies were removed from the traps and females were dissected to determine the presence of fully developed eggs. We found that capture of reproductively mature female flies occurred earlier in orchards that are not sprayed with insecticides than in sprayed orchards or in black cherry tree sites. In addition, the gap between the flights of immature and mature females in unmanaged sweet or tart cherry orchards was shorter than in managed orchards or black cherry tree sites. We also determined fruit color, size, and skin hardness to characterize the progression of fruit maturity. We found that fruit became mature earlier in sweet and tart cherry orchards than in black cherry tree sites. This study indicates that the timing of female reproductive maturity is plastic and varies among cherry fruit fly populations present in distinct habitats. Variation in the timing of reproductive maturity is related to the fruit maturity period of distinct host plant species and to orchard management.

Profiling the Reproductive Toxicity of Chemicals from Multigeneration Studies in the Toxicity Reference Database

Multigeneration reproduction studies are used to characterize parental and offspring systemic toxicity, as well as reproductive toxicity of pesticides, industrial chemicals and pharmaceuticals. Results from 329 multigeneration studies on 316 chemicals have been digitized into standardized and structured toxicity data within the Toxicity Reference Database (ToxRefDB). An initial assessment of data quality and consistency was performed prior to profiling these environmental chemicals based on reproductive toxicity and associated toxicity endpoints. The pattern of toxicity across 75 effects for all 316 chemicals provided sets of chemicals with similar in vivo toxicity for future predictive modeling. Comparative analysis across the 329 studies identified chemicals with sensitive reproductive effects, based on comparisons to chronic and subchronic toxicity studies, as did the cross-generational comparisons within the multigeneration study. The general pattern of toxicity across all chemicals and the more focused comparative analyses identified 19 parental, offspring and reproductive effects with a high enough incidence to serve as targets for predictive modeling that will eventually serve as a chemical prioritization tool spanning reproductive toxicities. These toxicity endpoints included specific reproductive performance indices, male and female reproductive organ pathologies, offspring viability, growth and maturation, and parental systemic toxicities. Capturing this reproductive toxicity data in ToxRefDB supports ongoing retrospective analyses, test guideline revisions, and computational toxicology research.

Preputialectomised and intact adult male mice exhibit an elevated urinary ratio of oestradiol to creatinine in the presence of developing females, whilst promoting uterine and ovarian growth of these females

Exposure to novel adult males and their urine can hasten the onset of sexual maturity in female mice. Some evidence implicates chemosignals from males' preputial glands, while other evidence suggests that male urinary steroids, especially 17beta-oestradiol, contribute to this effect. The present experiment was designed to determine whether preputial gland removal would influence the capacity of males to accelerate female sexual development, and to measure male urinary oestradiol and testosterone in the presence or absence of these glands. Juvenile females aged 28 days were housed for two weeks in isolation or underneath two outbred males that had undergone preputialectomy or sham surgery. Urine samples were collected non-invasively from males that were isolated or exposed to females, then assayed for oestradiol, testosterone and creatinine. Combined uterine and ovarian mass from females sacrificed at 43 days of age was increased by exposure to males, regardless of whether or not these males had been preputialectomised. Male urinary creatinine was reduced by exposure to developing females. Creatinine-adjusted oestradiol and testosterone were significantly greater in female-exposed than in isolated males, in both preputialectomised and intact males. These data suggest that the preputials are not necessary for the capacity of males to hasten female uterine and ovarian growth. As exogenous oestrogens can promote uterine growth and other parameters of female reproductive maturation, oestradiol in males' urine may contribute to earlier sexual maturity in male-exposed females.

Characterization of heat shock protein 90 in the shrimp Metapenaeus ensis: Evidence for its role in the regulation of vitellogenin synthesis

Estrogen hormones play a vital role in the regulation of female reproductive maturation. In oviparous vertebrates, the synthesis of vitellogenin (VTG) is tightly controlled by estrogen hormone signal transduction pathway, which is mediated by estrogen receptor and heat shock protein 90 (Hsp90). In order to investigate whether a similar mechanism exists in crustaceans, the Hsp90 gene was cloned and isolated from the shrimp Metapenaeus ensis by homology cloning strategy. The Hsp90 is 2,524 bp in length, containing an open reading frame of 2,163 bp that encodes a 720 amino acid polypeptide (83 kD). The Hsp90-coding region is interrupted by four introns. MeHsp90 is differentially expressed in eyestalk, ovary, and hepatopancreas at different ovarian maturation stages, and consistently expressed in other tissues including heart, gill, gut, muscle, and central nervous system. In vitro ovary explant assay reveals that MeHsp90 expression in immature ovary can be induced by the addition of exogenous estradiol-17beta, but expression in fully mature ovary exhibits no response to estradiol-17beta treatment. In situ hybridization shows that MeHsp90 is highly expressed in previtellogenic oocytes and its expression decreases with the progress of maturation, and finally stops in late-vitellogenic oocytes. Our results indicate a strong correlation between estrogen hormones and Hsp90 expression in shrimp, suggesting that the expression of VTG may be under the regulation of estrogen hormones through a mechanism similar to that in vertebrates. The result provides insights on the control of vitellogenesis in invertebrates.

Mating-increases trypsin in female Drosophila hemolymph

Male-derived accessory gland proteins (Acps) are transferred to the female reproductive tract during mating and affect female reproductive maturation and behavior. Some Acps subsequently enter the female hemolymph. We hypothesized that humoral proteases are the primary effectors of Acp bioactivity by processing (activating) and/or degrading them. To test this hypothesis we examined the fate of one Acp, Drosophila melanogaster Sex Peptide (Acp70A, DrmSP), which possesses several putative serine-protease cleavage sites, in hemolymph of unmated and mated females. In D. melanogaster, DrmSP induces post-mating non-receptivity and enhances oogenesis. To determine if serine proteases regulate the duration of DrmSP activity in mated females, we performed kinetic analysis of cleavage of a synthetic N-terminal truncated DrmSP 8–36 (T-SP) with hemolymph of unmated versus mated females. We found that T -SP is cleaved more rapidly and completely in mated female hemolymph. Using LC-MS/MS analyses, we identified its primary cleavage sites, indicating that trypsin was the major endopeptidase regulating T-SP in hemolymph. This was verified in vitro by utilizing specific chromogenic serine-protease substrates and inhibitors. We propose that post-mating cleavage of DrmSP in the female hemolymph regulates the duration of the rapidly induced post-mating responses in D. melanogaster and that this is a specific example of Acp bioactivity regulated by hemolymph serine proteases.

Latitudinal Variation in Population Structure and Reproductive Pattern of the Endemic South American Shrimp Artemesia Longinaris (Decapoda: Penaeoidea)

Population structure and reproductive maturity of females were investigated in the shrimp Artemesia longinarisBate, 1888 from coastal waters of northern São Paulo State (Brazil, |$23^\circ {\rm{S}}$|⁠) and Mar del Plata (Argentina, |$38^\circ {\rm{S}}$|⁠) from June 2001 to May 2002. Monthly collections were taken by commercial shrimp fishing boats equipped with bottom trawl nets. Population parameters from size frequency distributions and size (carapace length = CL) of female reproductive maturity were analyzed and compared from the two sampling areas. Latitudinal trends in reproductive parameters of A. longinaris were shown in overall body size and size of reproductive maturity, both of which were smaller in females from the tropical location than those from the cold-temperate sampling area. Largest females |$( \gt \;30\;{\rm{mm}}\;{\rm{CL}})$| were collected in Argentina, while Brazilian specimens reached maximum size at |$27\;{\rm{mm}}\;{\rm{CL}}$|⁠. The smallest size of female sexual maturity was estimated at |$13.6\;{\rm{mm}}\;{\rm{CL}}$| in Brazilian samples compared to |$22.1\;{\rm{mm}}\;{\rm{CL}}$| calculated for those from Argentina. Populations from both regions exhibited a bimodal size distribution in the spring, with the peak at small body size probably corresponding to recent recruits and the peak at larger body size to reproductive females or shrimps migrating in from deeper waters or other latitudinal regions. In late spring and summer, an intrusion of the cold South Atlantic Coastal Water mass was observed which lowered water temperature and stimulated plankton production, the primary food source for the larvae of a typically cold-temperate species such as A. longinaris. The trend of increasing body size and delay of sexual maturity with increasing latitude appears to be correlated with the decreasing water temperature and increasing plankton productivity at higher latitudes.

Mating-responsive genes in reproductive tissues of femaleDrosophila melanogaster

Male-derived accessory gland proteins that are transferred to females during mating have profound effects on female reproductive physiology including increased ovulation, mating inhibition, and effects on sperm utilization and storage. The extreme rates of evolution seen in accessory gland proteins may be driven by sperm competition and sexual conflict, processes that may ultimately drive complex interactions between female- and male-derived molecules and sperm. However, little is known of how gene expression in female reproductive tissues changes in response to the presence of male molecules and sperm. To characterize this response, we conducted parallel genomic and proteomic analyses of gene expression in the reproductive tract of 3-day-old unmated and mated female Drosophila melanogaster. Using DNA microarrays, we identified 539 transcripts that are differentially expressed in unmated vs. mated females and revealed a striking peak in differential expression at 6 h postmating and a marked shift from primarily down-regulated to primarily up-regulated transcripts within 3 h after mating. Combining two-dimensional gel electrophoresis and liquid chromatography mass spectrometry analyses, we identified 84 differentially expressed proteins at 3 h postmating, including proteins that appeared to undergo posttranslational modification. Together, our observations define transcriptional and translational response to mating within the female reproductive tract and suggest a bimodal model of postmating gene expression initially correlated with mating and the final stages of female reproductive tract maturation and later with the declining presence of male reproductive molecules and with sperm maintenance and utilization.

Social suppression of female reproductive maturation and infanticidal behavior in cooperatively breeding Mongolian gerbils

In several cooperatively breeding species, reproductively suppressed, nonbreeding females are attracted to infants and routinely provide alloparental care, while breeding females may attack or kill other females' infants. The mechanisms underlying the transition from alloparental to infanticidal behavior are unknown. In this study, we tested the hypothesis that this transition is associated with cessation of reproductive suppression and onset of ovarian activity in the Mongolian gerbil ( Meriones unguiculatus), a cooperatively breeding rodent. Young female gerbils were housed with their natal family (FH), with a female pairmate (PH) or singly (SH). When females were either 11–13 or 16–18 weeks of age, we characterized their behavioral responses to an unfamiliar pup, reproductive development, and plasma progesterone, cortisol, and prolactin concentrations. In both age groups, FH females were significantly less likely to attack pups than PH or SH females and in fact never did so. FH females also had smaller ovaries and uteri, less developed scent glands, and lower progesterone levels, and were more likely to be anovulatory than PH or SH females, especially in the 11- to 13-week-old age group. Prolactin concentrations did not differ with reproductive status but were significantly higher in females that did not attack pups than in those that did. We found no other significant associations, however, between reproductive or endocrine measures and behavioral responses to pups. These results suggest that cohabitation with the natal family inhibits both infanticidal behavior and reproductive maturation in young female gerbils but that these two effects may not be causally related.

Effects of early experience on female behavioural and reproductive development in rhesus macaques

A growing body of research on humans suggests that exposure to a stressful family environment or father absence from home during childhood is associated with early female puberty and greater interest in infants among adolescent girls. This effect may be mediated by early exposure to harsh and inconsistent maternal care, but the mechanisms by which maternal care affects female reproductive maturation are not known. The present study reports sex differences in interest in infants among juvenile rhesus macaques similar to those observed in human adolescents. Furthermore, juvenile females that were exposed to harsh and inconsistent maternal care in infancy showed higher interest in infants than controls. Evidence from cross-fostered females indicated that these effects resulted from early experience and not genetic inheritance from the mother. There were no significant differences in female age at first conception in relation to the quality of maternal care received during infancy. Macaque females exposed to harsh and inconsistent maternal care in infancy tended to have higher cortisol responses to stress and to corticotropin-releasing hormone than controls in the first three years of life. Furthermore, females with higher cortisol responses to stress exhibited higher interest in infants. These findings suggest that some of the effects of early parental care on female reproductive maturation may be mediated by developmental changes in the activity of the hypothalamic-pituitary-adrenal axis.

Female courtship in the Banggai cardinalfish: honest signals of egg maturity and reproductive output?

Despite the vast literature on male courtship behaviour, little is known about the function and information content of female courtship behaviour. Female courtship behaviour may be important in many species, particularly where both sexes invest heavily in the offspring, and if such behaviours contain honest information regarding a female’s potential reproductive investment, they may be particularly important in male mate choice. Using observations of two female courtship behaviours (the “rush” and the “twitch”) from experimental pairings in the Banggai cardinalfish (Pterapogon kauderni), I addressed the question of whether these courtship behaviours contained information on female reproductive output (clutch weight) and egg maturity (proximity to spawning), traits commonly associated with male mate choice. I especially focused on the importance of these courtship behaviours in relation to other female characters, such as size and condition, using multiple regression. I found that one of these behaviours, the rush, was strongly associated with fecundity, whereas size, condition and the twitch were not. Further, I found that the “twitch” behaviour was associated with how close to actual spawning a female was. The results suggest that female courtship behaviour may convey highly important information in a mate choice context. I discuss the adaptive value of honest information in female courtship behaviour in light of these results.

Urinary free cortisol increases in adolescent caucasian females during perimenarche.

Urinary free cortisol (UFC) excretion has been thought to be constant during female reproductive maturation when normalized for body surface area. We sought to determine whether there are longitudinal changes in urinary free cortisol excretion during perimenarche in adolescent females. We performed a longitudinal study of 24-h UFC excretion obtained at 6-month intervals over a 4-yr period in a cohort of 112 adolescent non-Hispanic white perimenarchal females from south central Pennsylvania. The overall mean values (mean +/- SD) for UFC/24 h for all measurements between ages 12 and 17 yr was 67.4 +/- 43.8 micro g/24 h (to convert to nanomoles per day, multiply by 2.759). In our model, we found a significant positive association between UFC excretion with both gynecological age (P = 0.002) and chronological age (P = 0.0001). For every incremental increase in Tanner stage, the UFC/BSA increased by 3.0 microg/24 h per square meter. Correcting the UFC values by both creatinine and BSA creates a fairly constant number (6.3 +/- 3.1 microg/mg per square meter per 24 h) over the age range 12-17 yr represented in this study. An increase in cortisol excretion may be part of normal reproductive maturation.

Production of domestic bovine ( Bos taurus) × American bison ( Bison bison) F1 embryos by IVM-IVF

Bison from Yellowstone National Park (YNP) have an important genetic history. As one of the few wild herds of bison with no evidence of cattle DNA introgression and a large enough population to maintain genetic diversity, they are considered a conservation priority for the species. Unfortunately, there is a high prevalence of the zoonotic disease brucellosis in the herd. Part of the management strategy for controlling the disease and herd size in YNP is to remove bison from the population during the winter migration out of the park. This interagency management cull provides an opportunity to collect a large number of oocytes from a wild bison population for genetic banking and research purposes. During the winters of 2014–2018, which is the nonbreeding season for bison, oocytes were collected post mortem and used to determine the effects of donor reproductive maturity and pregnancy status on oocyte quality and in vitro fertilization (IVF) outcomes, and to demonstrate the feasibility of producing healthy offspring. Cumulus oocyte complexes (COCs) were placed into an in vitro embryo production (IVP) system, and on days 7, 7.5, and 8 of in vitro culture (Day 0 = day of in vitro fertilization) embryos were assessed for developmental stage and quality prior to vitrification. Embryos were then stored in liquid nitrogen until the breeding season when a subset were warmed, cultured for 6 h, evaluated for survival, and transferred to healthy bison recipients. There were no significant differences in the ability of recovered COCs to support blastocyst development based on female reproductive maturity or pregnancy status (juvenile 79/959 (8.2%) vs sexually mature 547/6544 (8.4%); non-pregnant 188/2302 (8.2%) vs pregnant 556/6122 (9.1%)). Following the transfer of 15 embryos to 10 recipients, one healthy female calf was born. This work demonstrates that live offspring can be generated from COCs collected from YNP bison post mortem in the non-breeding season, and that gamete recovery can be a valuable tool for conservation of valuable genetics for this species while mitigating diseases like brucellosis.

Reproductive development in the hermaphroditic freshwater snail Physa monitored with complementing albino lines

We estimated age and size at onset of functional outcross- and self-fertility in three isofemale lines of Physa heterostropha carrying the recessive, non-allelic genes, alb1 and alb2 . 9Experimental’ snails of these lines were reared from 2 weeks of age to adulthood and periodically introduced to mature, complementing 9challenge’ snails. The three lines differed significantly in the size at which they matured, but not the age, under our culture conditions. Male reproductive maturity was reached at a mean of 5.7 weeks and female reproductive maturity at 7.3 weeks ( n = 50). These ages correspond to mean shell lengths of 5.3—6.2 mm as male and 6.9—7.6 mm as female. Over all three lines, first production of viable offspring by self-fertilization occurred at a mean age of 22 weeks ( n = 113). Again a significant line effect on size at reproduction was detected, with mean size at onset of self-fertilization ranging from 8.1 mm to 8.7 mm. Autosterility in the three lines ranged from negligible to 44 %. Among autofertile snails, we identified cases of outcross male-sterility, outcross female-sterility, and outcross double-sterility. Of 46 individuals demonstrating male function before female, two passed through brief periods of self-fertilization before outcrossing as females. We also identified three individuals maturing simultaneously in both capacities and one individual that matured as female before male. So, although the situation is complex, we suggest that ‘simultaneous hermaphroditism’ provides the best description of the reproductive biology of Physa . The great diversity of reproductive allocation described here implies considerable potential for life-history evolution in these snails.

Sexual maturation in female gray short-tailed opossums, Monodelphis domestica, is dependent upon male stimuli.

The development of physiological responsiveness to male stimuli in peripubertal female gray short-tailed opossums was examined in this study. Prepubertal females were exposed directly or indirectly to male chemicals (odors) or to no male stimuli. All females exposed directly to deposited male stimuli (22/22) showed estrus at a mean (+/- SEM) age of 127 +/- 2 days. Only 59% (13/22) of females exposed indirectly showed estrus, and at an older mean age of 162 +/- 5 days (p less than 0.01). Vaginal estrus was not observed in any of the females isolated from male stimuli (0/11). Direct exposure of prepubertal females to male odors was associated with higher uterine weights compared to those of indirectly exposed and isolated females. Reproductive success, measured as litter production, of peripubertal females greater than 140 days old was comparable to adult reproductive success. This study has shown that reproductive maturation in pubertal female opossums requires male stimuli, that this stimulus appears to be pheromonal, and that direct exposure to deposited male odors is the most effective stimulus for female reproductive maturation.

Maturation of the male reproductive system and its endocrine regulation.

The production of spermatozoa in the male insect and the transfer of the seminal mass to the female require significant investments of biochemical resources and the temporal coordination of development in several organs. Maturation of the gonads and the secondary reproductive systems must be synchronized with the metamorphic acquisition of energetic, sensory, motor, and central nervous adaptations for mating. The developmental hormones that commit cells to new programs and that trigger and modulate their expression in molting cycles also affect the primary and secondary reproductive systems. Many studies have addressed the endocrine regulation of female reproductive maturation and physiology. In comparison, investigations of the male insect systems have lagged. But in the past few years, more laboratories have focused their activities on analyses of male reproduction and its control (9, 57, 58). A recent chapter in this series reviewed the male accessory gland systems (9). This review discusses some of the recent studies that enlarge our knowl­ edge of the special physiology of the male. Selected examples summarize investigations that show that the major hormones that control growth and metamorphosis of the epidermis also control the growth, differentiation, and physiological modulation of the male reproductive system. In addition, male

Live birth of a gaur ( [formula omitted][formula omitted]) calf following nonsurgical embryo transfer to a holstein ( [formula omitted][formula omitted]) recipient

Bison from Yellowstone National Park (YNP) have an important genetic history. As one of the few wild herds of bison with no evidence of cattle DNA introgression and a large enough population to maintain genetic diversity, they are considered a conservation priority for the species. Unfortunately, there is a high prevalence of the zoonotic disease brucellosis in the herd. Part of the management strategy for controlling the disease and herd size in YNP is to remove bison from the population during the winter migration out of the park. This interagency management cull provides an opportunity to collect a large number of oocytes from a wild bison population for genetic banking and research purposes. During the winters of 2014–2018, which is the nonbreeding season for bison, oocytes were collected post mortem and used to determine the effects of donor reproductive maturity and pregnancy status on oocyte quality and in vitro fertilization (IVF) outcomes, and to demonstrate the feasibility of producing healthy offspring. Cumulus oocyte complexes (COCs) were placed into an in vitro embryo production (IVP) system, and on days 7, 7.5, and 8 of in vitro culture (Day 0 = day of in vitro fertilization) embryos were assessed for developmental stage and quality prior to vitrification. Embryos were then stored in liquid nitrogen until the breeding season when a subset were warmed, cultured for 6 h, evaluated for survival, and transferred to healthy bison recipients. There were no significant differences in the ability of recovered COCs to support blastocyst development based on female reproductive maturity or pregnancy status (juvenile 79/959 (8.2%) vs sexually mature 547/6544 (8.4%); non-pregnant 188/2302 (8.2%) vs pregnant 556/6122 (9.1%)). Following the transfer of 15 embryos to 10 recipients, one healthy female calf was born. This work demonstrates that live offspring can be generated from COCs collected from YNP bison post mortem in the non-breeding season, and that gamete recovery can be a valuable tool for conservation of valuable genetics for this species while mitigating diseases like brucellosis.

Biology of the striped chafer,Odontria striata(Coleoptera: Scarabaeidae) I. The adult, flight and ground surface activity, female reproductive maturation, and food-plant selection

Abstract Aspects of the biology of Odontria striata White included in this report are seasonal activity patterns, female reproductive development, and food-plant selection by adult beetles. Observations made during flights are noted. Flight activity commenced 30 min after sunset and lasted approximately 30 min; it was shown to be closely linked with air temperature, and a dusk temperature threshold of 6–7°C is suggested. Major flight periods were found to occur during April-May (soon after eclosion) and again in August-September. Males predominated in light-trap catches; females never exceeded 20% of the total. Pitfall trapping revealed autumn and spring peaks in above-ground activity. In March, males were predominant in pitfall trap catches; through April and May females outnumbered males by 2:1 or more, but in spring and summer the sex ratio was normally closer to unity. Reasons for this pattern and exceptions to it are discussed. The female reproductive system and timing of ovary maturation are describ...

Physical and reproductive characteristics of an expanding woodland caribou population (Rangifer tarandus caribou) in northern Labrador

One hundred and fifty-nine caribou (Rangifer tarandus caribou) were collected from the area of precalving distribution of the George River population in northern Labrador between April 3 and 15, 1980. The sample revealed that caribou of northern Labrador reach physical and reproductive maturity earlier than most other free-ranging caribou populations in North America. Females attained mature values for lean body weight and shoulder height by 34 months and for total body length, heart girth, and mandible length by 46 months. Pregnancy rates for females 22, 34, and 46 months and older were 43, 90, and 95%, respectively. Measurements of fat reserves showed George River females to be in superior physical condition during spring migration than caribou on mainland Northwest Territories. Fat reserves, however, were substantially less than comparable values for females collected from the same population in March, 1976. The calf: pregnant female ratio was 42:100, suggesting a 1st year rate of mortality of approximately 58%. The most common internal parasites were Cysticercus tenuicollis and Fascioloides magna. It is concluded that the recent growth of the George River population has resulted from early female physical and reproductive maturity, low adult mortality, and high survival of calves.