Seasonal Reproductive Development Research Articles

Advanced seasonal reproductive development in a male urban bird is reflected in earlier plasma luteinizing hormone rise but not energetic status

Urban animals inhabit an environment considerably different than do their non-urban conspecifics, and to persist urban animals must adjust to these novel environments. The timing of seasonal reproductive development (i.e., growth of gonads and secondary sex organs) is a fundamental determinant of the breeding period and is frequently advanced in urban bird populations. However, the underlying mechanism(s) by which birds adjust the timing of reproductive development to urban areas remain(s) largely unknown. Here, we compared the timing of vernal reproductive development in free-ranging urban and non-urban male Abert’s Towhees, Melozone aberti, in Phoenix, Arizona, USA, and tested the non-mutually exclusive hypotheses that earlier reproductive development is due to improved energetic status and/or earlier increase in endocrine activity of the reproductive system. We found that urban birds initiated testicular development earlier than non-urban birds, but this disparity was not associated with differences in body condition, fat stores, or innate immune performance. These results provide no support for the hypothesis that energetic constraints are responsible for delayed reproductive development of non-urban relative to urban male Abert’s Towhees. Urban birds did, however, increase their plasma luteinizing hormone, but not plasma testosterone, earlier than non-urban birds. These findings suggest that adjustment to urban areas by Abert’s Towhees involves increases in the endocrine activity of the anterior pituitary gland and/or hypothalamus earlier than non-urban towhees.

Food availability, energetic constraints and reproductive development in a wild seasonally breeding songbird.

Summary In many organisms, food availability is a proximate cue that synchronizes seasonal development of the reproductive system with optimal environmental conditions. Growth of the gonads and secondary sexual characteristics is orchestrated by the hypothalamic–pituitary–gonadal (HPG) axis. However, our understanding of the physiological mechanisms by which food availability modulates activity of the HPG axis is limited.It is thought that many factors, including energetic status, modulate seasonal reproductive activation. We tested the hypothesis that food availability modulates the activity of the HPG axis in a songbird. Specifically, we food‐restricted captive adult male Abert's Towhees Melozone aberti for 2 or 4 weeks during photoinduced reproductive development. A third group (control) received ad libitum food throughout. We measured multiple aspects of the reproductive system including endocrine activity of all three levels of the HPG axis [i.e. hypothalamic gonadotropin‐releasing hormone‐I (GnRH‐I), plasma luteinizing hormone (LH) and testosterone (T)], and gonad morphology. Furthermore, because gonadotropin‐inhibitory hormone (GnIH) and neuropeptide Y (NPY; a potent orexigenic peptide) potentially integrate information on food availability into seasonal reproductive development, we also measured the brain levels of these peptides.At the hypothalamic level, we detected no effect of food restriction on immunoreactive (ir) GnRH‐I, but the duration of food restriction was inversely related to the size of ir‐GnIH perikarya. Furthermore, the number of ir‐NPY cells was higher in food‐restricted than control birds. Food restriction did not influence photoinduced testicular growth, but decreased plasma LH and T, and width of the cloacal protuberance, an androgen‐sensitive secondary sexual characteristic. Returning birds to ad libitum food availability had no effect on plasma LH or T, but caused the cloacal protuberance to rapidly increase in size to that of ad libitum‐fed birds.Our results support the tenet that food availability modulates photoinduced reproductive activation. However, they also suggest that this modulation is complex and depends upon the level of the HPG axis considered. At the hypothalamic level, our results are consistent with a role for the GnIH and NPY systems in integrating information on energetic status. There also appears to be a role for endocrine function at the anterior pituitary gland and testicular levels in modulating reproductive development in the light of energetic status and independently of testicular growth.

Defining Global Neuroendocrine Gene Expression Patterns Associated with Reproductive Seasonality in Fish

BackgroundMany vertebrates, including the goldfish, exhibit seasonal reproductive rhythms, which are a result of interactions between external environmental stimuli and internal endocrine systems in the hypothalamo-pituitary-gonadal axis. While it is long believed that differential expression of neuroendocrine genes contributes to establishing seasonal reproductive rhythms, no systems-level investigation has yet been conducted.Methodology/Principal FindingsIn the present study, by analyzing multiple female goldfish brain microarray datasets, we have characterized global gene expression patterns for a seasonal cycle. A core set of genes (873 genes) in the hypothalamus were identified to be differentially expressed between May, August and December, which correspond to physiologically distinct stages that are sexually mature (prespawning), sexual regression, and early gonadal redevelopment, respectively. Expression changes of these genes are also shared by another brain region, the telencephalon, as revealed by multivariate analysis. More importantly, by examining one dataset obtained from fish in October who were kept under long-daylength photoperiod (16 h) typical of the springtime breeding season (May), we observed that the expression of identified genes appears regulated by photoperiod, a major factor controlling vertebrate reproductive cyclicity. Gene ontology analysis revealed that hormone genes and genes functionally involved in G-protein coupled receptor signaling pathway and transmission of nerve impulses are significantly enriched in an expression pattern, whose transition is located between prespawning and sexually regressed stages. The existence of seasonal expression patterns was verified for several genes including isotocin, ependymin II, GABAA gamma2 receptor, calmodulin, and aromatase b by independent samplings of goldfish brains from six seasonal time points and real-time PCR assays.Conclusions/SignificanceUsing both theoretical and experimental strategies, we report for the first time global gene expression patterns throughout a breeding season which may account for dynamic neuroendocrine regulation of seasonal reproductive development.

Seasonal gonadal recrudescence in song sparrows: Response to temperature cues

Day length predicts changing of seasons at mid-latitudes, but additional environmental cues (e.g., temperature, rainfall) give more precise information about timing of food peaks critical for offspring survival. We tested the effects of temperature on seasonal reproductive development of male song sparrows ( Melospiza melodia morphna) from two populations: the Western Washington coast (3 m) and Cascade Mountains (500–1220 m). Previous work has shown that the timing of gonadal recrudescence can differ between the two sites in the field by as much as two months. However, in the laboratory under identical controlled conditions, testes grow at the same rate. To test whether temperature alone could account for a portion of the variation we measured in the field, we captured birds from each site and held them in temperature controlled environmental chambers that mimicked temperatures experienced either in the mountains or on the coast. We increased day length on a natural schedule, and measured testis volume, levels of circulating androgens and prolactin, and song rates. Increasing day length stimulated gonadal growth in all groups. We found only modest effects of temperature on reproductive development. In the mountain birds colder, montane temperatures slowed rates of growth, delaying the onset of growth by one month. Since temperature changes more markedly during the early winter months in the mountains than on the coast, increasing temperature may be a more relevant cue in timing of reproduction in the mountain population. These data suggest that while temperature helps to explain some of the variation in reproductive timing of free living sparrows, another as yet untested cue in the field may play a more important role. Furthermore, our data suggest that individuals within the same species may rely on different proximate cues for reproductive timing depending on the specific habitat in which they live.

Light-induced reduction of cytoplasmic free calcium in neurons proposed to be encephalic photoreceptors in chick brain

A population of cerebrospinal fluid-contacting neurons (CSFcn) in the lateral septal organ (LSO) may serve as encephalic photoreceptors (EPRs) functioning to signal the onset of seasonal reproductive development in birds. Previous studies on CSFcn in the LSO have focused on identification of retinal protein components in fixed brain tissue. In order to understand better the mechanisms underlying the light-induced photosexual response in birds, a physiological characterization is required. In this study, changes of intracellular free calcium concentration ([Ca 2+] i) were monitored during light stimulation of CSFcn in the LSO in live brain slices from embryonic chicks. Using the fluorescent calcium indicator fluo-4, a reduced [Ca 2+] i within CSFcn was recorded in response to photostimulation, which is consistent with what has been demonstrated in rods and cones following illumination. Results support the hypothesis that CSFcn in the LSO function as EPRs in the avian brain.

Seasonal Growth of Song Control Nuclei Precedes Seasonal Reproductive Development in Wild Adult Song Sparrows

In seasonally breeding adult songbirds, the brain regions that control song undergo dramatic seasonal morphological changes. During late winter and early spring, increasing day length triggers an increase in circulating testosterone that ultimately causes several song nuclei to grow in volume. The timing of this growth relative to the seasonal development of the reproductive system is not known. This question was investigated in two populations of wild song sparrows (Melospiza melodia morphna). Both populations live at the same latitude (46°N), but breed at different altitudes. One population resides on the Pacific coast in Washington, and the other resides in the foothills of the Cascade Mountains. Both populations experienced the same photoperiodic conditions, but the timing of seasonal reproductive development differed between populations. Coastal birds initiated gonadal recrudescence approximately 2 weeks earlier than montane birds. Despite this temporal difference in reproductive development, there were no differences between these groups in the seasonal growth of two song control nuclei, HVc and RA. During late February, both groups had low circulatory levels of testosterone (mean for coastal birds was 1.01 ± 0.37 ng/ml; mean for montane birds was 1.41 ± 0.26 ng/ml) and fully recrudesced song nuclei (for example, mean HVc volume in coastal birds was 1.77 ± 0.08 mm3; mean HVc volume in montane birds was 1.76 ± 0.09). Also at this time, both populations were in the earliest stages of seasonal reproductive development as judged by the degree of gonadal recrudescence (mean gonad volume was less than 10% of typical breeding size in both populations). It is concluded that seasonal song system growth is completed before seasonal reproductive development in response to submaximal levels of circulating testosterone.

The effects of salinity on reproductive development, plasma steroid levels, fertilisation and egg survival in black bream Acanthopagrus butcheri

The effects of salinity of holding water of 5‰, 20‰ or 35‰ on seasonal reproductive development, plasma steroid levels, the efficacy of luteinizing hormone releasing hormone ethylamide (LHRHa) to stimulate ovulation, sperm motility, and egg fertility and development to hatching were investigated. Fish were captured from the wild from December to February, placed into salinity regimes in May and held until the normal times of spawning the following November. Blood samples were taken in August, September and November. Female fish were injected with saline or LHRHa (50 μg kg −1) in November and bled and checked for ovulation for 5 days. Gonadal maturation was unaffected by salinity in both sexes. In females, seasonal plasma steroid levels were unaffected by salinity, whereas in males, plasma levels of 17,20β-dihydroxy-4-pregnen-3-one (17,20βP) and 11-ketotestosterone were higher in fish held at 35‰ than in fish held at 5‰ in September, and in fish held at 5‰ and 20‰ in November, respectively. Plasma estradiol (E 2) and testosterone (T) levels in saline-injected fish, either remained low or were significantly suppressed. LHRHa treatment resulted in the short-term elevation of plasma E 2 and T levels at all salinities, whereas plasma 17,20βP levels were elevated over controls on days 1 and 2 post-injection in fish held in 20‰, but remained unchanged in fish held in 35‰ or 5‰. All but one fish ovulated in response to LHRHa, however, the number of ovulations and egg volumes was lowest in fish held at 5‰. Both fertilisation and sperm motility were significantly reduced at 5‰. Naturally fertilised eggs (35‰; 2–8 cell stage) were incubated to hatching at salinities of 0‰, 5‰, 10‰, 15‰, 20‰, 25‰, 30‰ or 35‰. Eggs hatched in all salinities except 0‰, but with lowered survival at 5‰ and 10‰. Larvae showed high levels of deformity at salinities below 15‰.

Changes in plasma sex steroid-binding protein levels associated with ovarian recrudescence in the spotted seatrout (Cynoscion nebulosus).

Adult spotted seatrout were sampled from the wild during the period of their yearly gonadal recrudescence to study the association of plasma sex steroid-binding protein (SBP) levels with seasonal reproductive development. Plasma SBP levels were estimated by Scatchard analysis of the binding of radiolabeled testosterone to seatrout plasma. Plasma SBP levels were lowest in regressed females, with a mean binding capacity of 310 +/- 18 nM. SBP levels increased slightly with the appearance of cortical alveolar-stage oocytes and continued increasing throughout the period of early and late vitellogenesis to reach peak values of 468 +/- 46 nM in fish undergoing final oocyte maturation. The steroid dissociation constant increased from 4.80 +/- 0.19 nM in fish with regressed ovaries to 6.58 +/- 0.76 nM in fish having completed ovarian recrudescence. The male sample size was too small to permit examination of stage-dependent changes in SBP levels during testicular recrudescence. However, neither the overall mean binding capacity nor mean binding affinity differed significantly between male (n = 14) and female fish (n = 81) in this study. Plasma SBP levels were not directly correlated with plasma levels of either testosterone or estradiol, but there was a strong correlation (r2 = 0.67, p < 0.001) between plasma testosterone binding capacity and the steroid dissociation constant. Changes in mean SBP levels were associated with changes in mean gonadosomatic index, hepatosomatic index, and plasma estradiol concentration, suggesting that the plasma SBP may have an important role in the reproductive cycle of the female spotted seatrout.

Reproduction of Darkblotched Rockfish off the Oregon Coast

Seasonal reproductive development, size and age at sexual maturity, and fecundity were described for darkblotched rockfish Sebastes crameri collected off the Oregon coast. Altogether, 1,060 fish captured by commercial groundfish and shrimp trawlers between July 1986 and July 1987 were examined. Reproductive events were protracted. Insemination of females occurred from August to December, and fertilization and parturition followed from December through March. Spermatozoa were observed within both vitellogenic and previtellogenic ovaries between July and November. Reproductive events in smaller males and females were delayed relative to those in larger individuals. Females attained 50% maturity at a greater size (36.5 cm total length) and age (8.4 years) than males (29.6 cm total length; 5A years). The unimodal development of eggs and larvae indicated one parturition per year. Most age-6, age-7, and age-8 females possessed ovaries in an intermediate “maturing” condition. Histological analysis revealed that most of these females were immature; ovaries showed no evidence of previous spawning, oocytes never developed beyond an early vitellogenic stage, and during months of parturition, many of these females were resorbing their advancing oocytes. Total fecundities ranged from 19,815 to 489,064 oocytes per ovary pair and increased exponentially with increasing fish length, linearly with fish weight, and asymptotically with fish age (6 to 66 years).

Decontamination of rat embryos and transfer to SPF recipients for the production of a breeding colony

The effects of salinity of holding water of 5‰, 20‰ or 35‰ on seasonal reproductive development, plasma steroid levels, the efficacy of luteinizing hormone releasing hormone ethylamide (LHRHa) to stimulate ovulation, sperm motility, and egg fertility and development to hatching were investigated. Fish were captured from the wild from December to February, placed into salinity regimes in May and held until the normal times of spawning the following November. Blood samples were taken in August, September and November. Female fish were injected with saline or LHRHa (50 μg kg−1) in November and bled and checked for ovulation for 5 days. Gonadal maturation was unaffected by salinity in both sexes. In females, seasonal plasma steroid levels were unaffected by salinity, whereas in males, plasma levels of 17,20β-dihydroxy-4-pregnen-3-one (17,20βP) and 11-ketotestosterone were higher in fish held at 35‰ than in fish held at 5‰ in September, and in fish held at 5‰ and 20‰ in November, respectively. Plasma estradiol (E2) and testosterone (T) levels in saline-injected fish, either remained low or were significantly suppressed. LHRHa treatment resulted in the short-term elevation of plasma E2 and T levels at all salinities, whereas plasma 17,20βP levels were elevated over controls on days 1 and 2 post-injection in fish held in 20‰, but remained unchanged in fish held in 35‰ or 5‰. All but one fish ovulated in response to LHRHa, however, the number of ovulations and egg volumes was lowest in fish held at 5‰. Both fertilisation and sperm motility were significantly reduced at 5‰. Naturally fertilised eggs (35‰; 2–8 cell stage) were incubated to hatching at salinities of 0‰, 5‰, 10‰, 15‰, 20‰, 25‰, 30‰ or 35‰. Eggs hatched in all salinities except 0‰, but with lowered survival at 5‰ and 10‰. Larvae showed high levels of deformity at salinities below 15‰.

The reproductive biology and diapause of the British fungal‐breeding Drosophila

Abstract. Seasonal reproductive development was investigated in four obligate fungivorous species, D.phalerata Meigen, D.transversa Fallen, D.cameraria Haliday and D.confusa Staeger. Samples of females taken from woodlands over a 2 year period were scored for reproductive status and fat content. Populations of D.phalerata and D.cameraria maintained in an outdoor insectary provided information on developmental time and adult mortality throughout the year. Experiments in controlled environmental chambers gave percentage diapause curves against day length for all four species. In D.phalerata the influence of temperature and fungus upon diapause behaviour was also investigated. In D.phalerata the optimal strategy for reproductive development can vary from month to month. Maturation of females may be immediate, dependent upon a fungal cue or completely prevented.