The dynamic landscape of chromatin accessibility and active regulatory elements in the mediobasal hypothalamus influences the seasonal activation of the reproductive axis in the male quail under long light exposure.

BACKGROUND: In cold and temperate zones, seasonal reproduction plays a crucial role in the survival and reproductive success of species. The photoperiod influences reproductive processes in seasonal breeders through the hypothalamic-pituitary-gonadal (HPG) axis, in which the mediobasal hypothalamus (MBH) serves as the central region responsible for transmitting light information to the endocrine system. However, the cis-regulatory elements and the transcriptional activation mechanisms related to seasonal activation of the reproductive axis in MBH remain largely unclear. In this study, an artificial photoperiod program was used to induce the HPG axis activation in male quails, and we compared changes in chromatin accessibility changes during the seasonal activation of the HPG axis. RESULTS: Alterations in chromatin accessibility occurred in the mediobasal hypothalamus (MBH) and stabilized at LD7 during the activation of the HPG axis. Most open chromatin regions (OCRs) are enriched mainly in introns and distal intergenic regions. The differentially accessible regions (DARs) showed enrichment of binding motifs of the RFX, NKX, and MEF family of transcription factors that gained-loss accessibility under long-day conditions, while the binding motifs of the nuclear receptor (NR) superfamily and BZIP family gained-open accessibility. Retinoic acid signaling and GTPase-mediated signal transduction are involved in adaptation to long days and maintenance of the HPG axis activation. According to our footprint analysis, three clock-output genes (TEF, DBP, and HLF) and the THRA were the first responders to long days in LD3. THRB, NR3C2, AR, and NR3C1 are the key players associated with the initiation and maintenance of the activation of the HPG axis, which appeared at LD7 and tended to be stable under long-day conditions. By integrating chromatin and the transcriptome, three genes (DIO2, SLC16A2, and PDE6H) involved in thyroid hormone signaling showed differential chromatin accessibility and expression levels during the seasonal activation of the HPG axis. TRPA1, a target of THRB identified by DAP-seq, was sensitive to photoactivation and exhibited differential expression levels between short- and long-day conditions. CONCLUSION: Our data suggest that trans effects were the main factors affecting gene expression during the seasonal activation of the HPG axis. This study could lead to further research on the seasonal reproductive behavior of birds, particularly the role of MBH in controlling seasonal reproductive behavior.

Neural thyroid hormone metabolism integrates seasonal changes in environmental temperature with the neuroendocrine reproductive axis.

We asked if environmental temperature alters thyroid hormone metabolism within the hypothalamus, thereby providing a neuroendocrine mechanism by which temperature could be integrated with photoperiod to regulate seasonal rhythms. We used immunohistochemistry to assess the effects of low-temperature winter dormancy at 4 °C or 12 °C on thyroid-stimulating hormone (TSH) within the infundibulum of the pituitary as well as deiodinase 2 (Dio2) and 3 (Dio3) within the hypothalamus of red-sided garter snakes (Thamnophis sirtalis). Both the duration and, in males, magnitude of low-temperature dormancy altered deiodinase immunoreactivity within the hypothalamus, increasing the area of Dio2-immunoreactivity in males and females and decreasing the number of Dio3-immunoreactive cells in males after 8-16 weeks. Reciprocal changes in Dio2/3 favor the accumulation of triiodothyronine within the hypothalamus. Whether TSH mediates these effects requires further study, as significant changes in TSH-immunoreactive cell number were not observed. Temporal changes in deiodinase immunoreactivity coincided with an increase in the proportion of males exhibiting courtship behavior as well as changes in the temporal pattern of courtship behavior after emergence. Our findings mirror those of previous studies, in which males require low-temperature exposure for at least 8 weeks before significant changes in gonadotropin-releasing hormone immunoreactivity and sex steroid hormones are observed. Collectively, these data provide evidence that the neuroendocrine pathway regulating the reproductive axis via thyroid hormone metabolism is capable of transducing temperature information. Because all vertebrates can potentially use temperature as a supplementary cue, these results are broadly applicable to understanding how environment-organism interactions mediate seasonally adaptive responses.

Cell adhesion and immune response, two main functions altered in the transcriptome of seasonally regressed testes of two mammalian species.

In species with seasonal breeding, male specimens undergo substantial testicular regression during the nonbreeding period of the year. However, the molecular mechanisms that control this biological process are largely unknown. Here, we report a transcriptomic analysis on the Iberian mole, Talpa occidentalis, in which the desquamation of live, nonapoptotic germ cells is the major cellular event responsible for testis regression. By comparing testes at different reproductive states (active, regressing, and inactive), we demonstrate that the molecular pathways controlling the cell adhesion function in the seminiferous epithelium, such as the MAPK, ERK, and TGF-ß signaling, are altered during the regression process. In addition, inactive testes display a global upregulation of genes associated with immune response, indicating a selective loss of the "immune privilege" that normally operates in sexually active testes. Interspecies comparative analyses using analogous data from the Mediterranean pine vole, a rodent species where testis regression is controlled by halting meiosis entry, revealed a common gene expression signature in the regressed testes of these two evolutionary distant species. Our study advances in the knowledge of the molecular mechanisms associated to gonadal seasonal breeding, highlighting the existence of a conserved transcriptional program of testis involution across mammalian clades.

The Photoperiod-Driven Cyclical Secretion of Pineal Melatonin Regulates Seasonal Reproduction in Geese (Anser cygnoides).

The photoperiod is the predominant environmental factor that governs seasonal reproduction in animals; however, the underlying molecular regulatory mechanism has yet to be fully elucidated. Herein, Yangzhou geese (Anser cygnoides) were selected at the spring equinox (SE), summer solstice (SS), autumn equinox (AE), and winter solstice (WS), and the regulation of seasonal reproduction via the light-driven cyclical secretion of pineal melatonin was investigated. We show that there were seasonal variations in the laying rate and GSI, while the ovarian area decreased 1.5-fold from the SS to the AE. Moreover, not only did the weight and volume of the pineal gland increase with a shortened photoperiod, but the secretory activity was also enhanced. Notably, tissue distribution further revealed seasonal oscillations in melatonin receptors (Mtnrs) in the pineal gland and the hypothalamus-pituitary-gonadal (HPG) axis. The immunohistochemical staining indicated higher Mtnr levels due to the shortened photoperiod. Furthermore, the upregulation of aralkylamine N-acetyltransferase (Aanat) was observed from the SS to the AE, concurrently resulting in a downregulation of the gonadotrophin-releasing hormone (GnRH) and gonadotropins (GtHs). This trend was also evident in the secretion of hormones. These data indicate that melatonin secretion during specific seasons is indicative of alterations in the photoperiod, thereby allowing for insight into the neuroendocrine regulation of reproduction via an intrinsic molecular depiction of external photoperiodic variations.

Potential Role of Anti-Müllerian Hormone in Regulating Seasonal Reproduction in Animals: The Example of Males.

Seasonal reproduction is a survival strategy by which animals adapt to environmental changes to improve their fitness. Males are often characterized by a significantly reduced testicular volume, indicating that they are in an immature state. Although many hormones, including gonadotropins, have played a role in testicular development and spermatogenesis, research on other hormones is insufficient. The anti-Müllerian hormone (AMH), which is a hormone responsible for inducing the regression of Müllerian ducts involved in male sex differentiation, was discovered in 1953. Disorders in AMH secretion are the main biomarkers of gonadal dysplasia, indicating that it may play a crucial role in reproduction regulation. A recent study has found that the AMH protein is expressed at a high level during the non-breeding period of seasonal reproduction in animals, implying that it may play a role in restricting breeding activities. In this review, we summarize the research progress on the AMH gene expression, regulatory factors of the gene's expression, and its role in reproductive regulation. Using males as an example, we combined testicular regression and the regulatory pathway of seasonal reproduction and attempted to identify the potential relationship between AMH and seasonal reproduction, to broaden the physiological function of AMH in reproductive suppression, and to provide new ideas for understanding the regulatory pathway of seasonal reproduction.

Differential temperature effects on photoperiodism in female voles: A possible explanation for declines in vole populations.

Many mammalian species use photoperiod as a predictive cue to time seasonal reproduction. In addition, metabolic effects on the reproductive axis may also influence seasonal timing, especially in female small, short-lived mammals. To get a better understanding of how annual cycling environmental cues impact reproductive function and plasticity in small, short-lived herbivores with different geographic origins, we investigated the mechanisms underlying integration of temperature in the photoperiodic-axis regulating female reproduction in a Northern vole species (tundra vole, Microtus oeconomus) and in a Southern vole species (common vole, Microtus arvalis). We show that photoperiod and temperature interact to determine appropriate physiological responses; there is species-dependent annual variation in the sensitivity to temperature for reproductive organ development. In common voles, temperature can overrule photoperiodical spring-programmed responses, with reproductive organ mass being higher at 10°C than at 21°C, whereas in autumn they are less sensitive to temperature. These findings are in line with our census data, showing an earlier onset of spring reproduction in cold springs, while reproductive offset in autumn is synchronized to photoperiod. The reproductive organs of tundra voles were relatively insensitive to temperature, whereas hypothalamic gene expression was generally upregulated at 10°C. Thus, both vole species use photoperiod, whereas only common voles use temperature as a cue to control spring reproduction, which indicates species-specific reproductive strategies. Due to global warming, spring reproduction in common voles will be delayed, perhaps resulting in shorter breeding seasons and thus declining populations, as observed throughout Europe.

Mechanisms of temperature modulation in mammalian seasonal timing.

Global warming is predicted to have major effects on the annual time windows during which species may successfully reproduce. At the organismal level, climatic shifts engage with the control mechanism for reproductive seasonality. In mammals, laboratory studies on neuroendocrine mechanism emphasize photoperiod as a predictive cue, but this is based on a restricted group of species. In contrast, field-oriented comparative analyses demonstrate that proximate bioenergetic effects on the reproductive axis are a major determinant of seasonal reproductive timing. The interaction between proximate energetic and predictive photoperiodic cues is neglected. Here, we focused on photoperiodic modulation of postnatal reproductive development in common voles (Microtus arvalis), a herbivorous species in which a plastic timing of breeding is well documented. We demonstrate that temperature-dependent modulation of photoperiodic responses manifest in the thyrotrophin-sensitive tanycytes of the mediobasal hypothalamus. Here, the photoperiod-dependent expression of type 2 deiodinase expression, associated with the summer phenotype was enhanced by 21°C, whereas the photoperiod-dependent expression of type 3 deiodinase expression, associated with the winter phenotype, was enhanced by 10°C in spring voles. Increased levels of testosterone were found at 21°C, whereas somatic and gonadal growth were oppositely affected by temperature. The magnitude of these temperature effects was similar in voles photoperiodical programmed for accelerated maturation (ie, born early in the breeding season) and in voles photoperiodical programmed for delayed maturation (ie, born late in the breeding season). The melatonin-sensitive pars tuberalis was relatively insensitive to temperature. These data define a mechanistic hierarchy for the integration of predictive temporal cues and proximate thermo-energetic effects in mammalian reproduction.

Role of Melatonin in Temperature-Induced Activation of the Neuroendocrine Reproductive Axis in Garter Snakes.

An animal's ability to respond optimally to changing environmental conditions is paramount to successfully reproducing and thus maximizing fitness. Studies on photoperiod-induced changes in neural thyroid hormone metabolism have conclusively linked environmental cues to the neuroendocrine reproductive axis of birds and mammals. Whether this conserved mechanism also transduces changes in environmental temperature, however, has not been fully addressed. We investigated whether the hormone melatonin mediates the effects of low-temperature dormancy on thyroid hormone metabolism within the hypothalamus of red-sided garter snakes (Thamnophis sirtalis parietalis). To address this question, we used immunohistochemistry to assess changes in thyroid-stimulating hormone (TSH) in the infundibulum of the pituitary and deiodinase 3 (Dio3) and gonadotropin-releasing hormone (GnRH) in the hypothalamus. We also asked if changes in TSH, Dio3, and/or GnRH immunoreactivity are associated with changes in male courtship behavior. In contrast to our predictions, 6 weeks of dormancy at 4°C significantly decreased the number of TSH-labeled cells in the infundibulum. It is possible that the observed decrease in TSH is related to the release of snakes from temperature refractoriness, but this idea needs further testing. Treatment of snakes with the melatonin precursor 5-hydroxytryptophan during dormancy at 4°C both reversed the temperature-induced change in TSH immunoreactivity and disrupted the temporal pattern of male courtship behavior. These results suggest that TSH cells within the infundibulum are both modulated by temperature and sensitive to changes in melatonin. As predicted, male snakes hibernated at an elevated temperature of 12°C for 6 weeks and treated with vehicle showed no change in TSH-, Dio3-, or GnRH-immunoreactive cell number. Treatment of snakes with the melatonin receptor antagonist luzindole was not sufficient in rescuing the effects of dormancy at 12°C on TSH immunoreactivity or courtship behavior. However, luzindole-treated snakes showed a significant increase in GnRH-immunoreactive cell number, suggesting that melatonin exerts an inhibitory effect on GnRH in garter snakes. In summary, our results provide critical insights into the mechanisms that mediate the effects of temperature on reproductive physiology and behavior.

Short communication: Photoperiod impacts ovarian extracellular matrix and metabolic gene expression in Siberian hamsters.

Ovarian cyclicity is variable in adult Siberian hamsters (Phodopus sungorus), who respond to long breeding season photoperiods with follicle development and ovulation, while short photoperiods typical of the non-breeding season induce gonadal atrophy. Recent RNAseq results identified ovarian matrix components and regulators of metabolism as differentially regulated by photoperiod; however, the impact of photoperiod across a full cycle of ovarian regression and recrudescence had not been explored for additional regulators of ovarian metabolism and extracellular matrix components. We hypothesized that matrix and metabolism-related genes would be expressed differentially across photoperiods that mimic breeding and non-breeding season daylengths. Hamsters were housed in one of four photoperiod groups: long day (16 h of light per day: 8 h of dark; LD, controls), short day regressed (8 L:16D; SD, regressed), and females exposed to SD then transferred to LD to stimulate return of ovarian function for 2 (early recrudescence), or 8 (late recrudescence) weeks. Plasma leptin concentrations along with expression of ovarian versican and liver-receptor homolog-1/Nr582 mRNA decreased in SD compared to LD and late recrudescence, while vimentin mRNA expression peaked in early and late recrudescence. Ovarian expression of fibronectin and extracellular matrix protein-1 was low in LD ovaries and increased in regressed and recrudescing groups. Expression of hyaluronidase-2, nectin-2, liver-X receptors-α and-ß, and adiponectin mRNA peaked in late recrudescence, with no changes noted for adiponectin receptor-1 and -2. The results offer a first look at the parallels between expression of these genes and the dynamic remodeling that occurs during ovarian regression and recrudescence.

Prolactin receptor regulates the seasonal reproduction of striped hamsters.

In this study, differential mRNA expression patterns of prolactin receptor (PRLR) in the hypothalamus and gonads, and the correlation with follicle stimulating hormone (FSH) and luteinizing hormone (LH) in striped hamster serum from spring, summer, autumn and winter were analyzed. Mature female and male striped hamsters in oestrus were used. Expression levels of PRLR in the hypothalamus, ovaries and testis from the summer and winter individuals were significantly higher compared with levels from the spring and autumn, whereas FSH and LH serum concentrations from summer and winter individuals were significantly lower compared with that from the spring and autumn. PRLR expression levels in hypothalamus, ovaries and testis were negatively correlated with FSH and LH serum concentrations, illustrating that PRLR might negatively regulate seasonal reproductive activity. PRLR expression levels in ovaries and testes were significantly higher compared with levels in the hypothalamus, suggesting that the regulative effects of PRLR in gonads might be significantly higher compared with that in the hypothalamus. Furthermore, PRLR expression levels from the spring, summer, autumn and winter seasons in the hypothalamus and gonads were significantly higher in females compared with levels in males, indicating that the regulative effect of PRLR might be sex dependent. Taken together, this study helps to understand in depth the seasonal regulative reproduction mechanism of striped hamsters to reasonably control population abundance.

RFRP-3 synchronized with photoperiods regulates the seasonal reproduction of striped hamsters.

The purpose of this study was to investigate the effect of RFRP-3 synchronized with photoperiods on regulating the seasonal reproduction of striped hamsters. The striped hamsters were raised separately under long-day (LD; 16 h light/8 h dark), medium-day (MD; 12 h light/12 h dark) or short-day (SD; 8 h light/16 h dark) conditions for 8 weeks. RFRP-3 and gonadotropin-releasing hormone (GnRH) mRNA levels in the hypothalamus, testis or ovaries in three groups were detected using reverse transcription polymerase chain reaction (RT-PCR). Melatonin (MLT), follicle-stimulating hormone (FSH) and luteinizing hormone (LH) concentrations in serum were detected using enzyme-linked immunosorbent assay (ELISA). The correlation between RFRP-3 and GnRH mRNA and FSH and LH concentrations was also analyzed. MLT negatively regulated the expression of RFRP-3. Significant differences for RFRP-3 mRNA existed in the three groups, which positively correlated with the GnRH and the FSH and LH concentrations. RFRP-3 mRNA levels in the hypothalamus were significantly higher than those in ovaries or testis. RFRP-3 levels in the hypothalamus were significantly lower in female than in male under SD conditions, while those in ovaries were significantly higher than those in testes under LD conditions. MLT decreased RFRP neuron activity, and RFRP-3 regulated the reproduction of striped hamsters.

Morphometric and Myelin Basic Protein Expression Changes in Arcuate Nucleus Kisspeptin Neurons Underlie Activation of Hypothalamic Pituitary Gonadal-axis in Monkeys (Macaca Mulatta) during the Breeding Season.

INTRODUCTION: Kisspeptin is involved in the hypothalamic pituitary gonadal-axis' seasonal regulation in rodents and sheep. Studies of kisspeptin signaling in regulating the transition between breeding and nonbreeding seasons have focused on kisspeptin expression, myelin basic protein (MBP) expression around kisspeptin-ir cells, and quantifying the synaptic connections between kisspeptin and gonadotropin-releasing hormone (GnRH) neurons in various animal models; however, the role of kisspeptin in regulating the seasonal breeding of primates has not been explored yet. OBJECTIVE: This study investigated changes in kisspeptin signaling during breeding and a non-breeding season in a non-human primate model, the rhesus monkey. METHODS: Three adult male monkeys (n = 3) from the breeding season and two monkeys (n = 2) from the non-breeding season were used in this study. After measuring the testicular volume and collecting a single blood sample, all animals were humanely euthanized under controlled conditions, and their hypothalami were collected and processed. Two 20 µm thick hypothalamic sections (mediobasal hypothalamus) from each animal were processed for kisspeptin-MBP and kisspeptin-GnRH immunohistochemistry (IHC). One section from each animal was used as a primary antibody omitted control to check the nonspecific binding in each IHC. RESULTS: Compared to the non-breeding season, plasma testosterone levels and testicular volumes were significantly higher in monkeys during the breeding season. Furthermore, compared to the non-breeding season, increased kisspeptin expression and a higher number of synaptic contacts between kisspeptin fibers and GnRH cell bodies were observed in the arcuate nucleus of the breeding season monkeys. In contrast, enlarged kisspeptin soma and higher MBP expression were observed in non-breeding monkeys. CONCLUSION: Our results indicated enhanced kisspeptin signaling in primate hypothalamus during the breeding season. These findings support the idea that kisspeptin acts as a mediator for the seasonal regulation of the reproductive axis in higher primates.

Polymorphisms and association of GRM1, GNAQ and HCRTR1 genes with seasonal reproduction and litter size in three sheep breeds.

Litter size is one of the important economic traits of livestock. Seasonal oestrus, ovulation and lambing of sheep have severely restricted the development of sheep farming in Xinjiang, China. The purpose of this study was to investigate the polymorphisms and genetic correlation between GRM1, GNAQ and HCRTR1 genes and the seasonal reproduction and litter size in three sheep breeds. The DNA mixed pool sequencing and PCR-SSCP methods were used to detect single nucleotide polymorphisms (SNPs) of GRM1, GNAQ and HCRTR1 genes in seasonal oestrous (Kazakh and Chinese Merino [Xinjiang Junken type]) and perennial oestrous (Hu) sheep breeds. The association between genetic polymorphism and litter size was also analysed. The results showed that T945C in exon 2 of GRM1 gene, C589T in exon 2 of HCRTR1 gene and A191G in exon 2 of GNAQ gene were identified by Sanger sequencing, and three genotypes were existed in each SNP site, which all belonged to the synonymous mutation. GRM1 (CC), GNAQ (GA) and HCRTR1 (TC) were the dominant genotypes of seasonal reproduction and litter size in Kazakh sheep and Chinese Merino sheep, respectively, while, in perennial oestrous Hu sheep populations, the dominant genotypes were GRM1 (TC), GNAQ (GA) and HCRTR1 (TC), respectively, and association analysis also confirmed the results. The above results implied that GRM1, GNAQ and HCRTR1 genes are significantly associated with lambing traits in Kazakh, Chinese Merino and Hu sheep. Among them, the locus of GRM1 (T945C), GNAQ (A191G) and HCRTR1 (C589T) might be considered as a potential molecular marker, which controls seasonal reproduction and litter size in sheep.

Changes in histology, protein expression, and autophagy in dairy goat testes during nonbreeding season†.

Seasonal reproduction contributes to increased chances of offspring survival in some animals. Dairy goats are seasonal breeding mammals. In this study, adult male Guanzhong dairy goats (10-12 months old) were used. Testis size, semen quality, hormone level, apoptosis of germ cells, and autophagy of Sertoli cells were analyzed in dairy goats during the breeding (October) and nonbreeding (April) seasons. We found that, during the nonbreeding season for dairy goats, semen quality, follicle-stimulating hormone (FSH) levels, and testosterone levels were reduced, and the number of apoptotic germ cells increased. The proliferation with decrease activity of germ cells in dairy goat during the nonbreeding season was significantly affected. However, the testis size did not change seasonally. Interestingly, Sertoli cell autophagy was more active during the nonbreeding season. The expression levels of FSH receptor, wilms tumor 1, androgen binding protein, glial cell derived neurotrophic factor, and stem cell factor decreased in dairy goats during the nonbreeding season. In summary, our results indicate that spermatogenesis in dairy goats during the nonbreeding season was not completely arrested. In addition, germ cell apoptosis and the morphology of Sertoli cells considerably changed in dairy goats during the nonbreeding season. Sertoli cell autophagy is involved in the seasonal regulation of spermatogenesis in dairy goats. These findings provide key insights into the fertility and spermatogenesis of seasonal breeding animals.

Olfactory detection of trace amounts of plant volatiles is correlated with testosterone in a passerine bird.

In response to damage by insects, plants release herbivore-induced plant volatiles (HIPVs) into the air. Insectivorous birds exploit these cues and, consequently, reduce the damages inflicted to the plants. However, little is known about whether they solely use HIPVs as foraging cues, or if they also use them to modulate traits linked to reproduction. As caterpillars are the primary food source required for insectivorous birds to raise offspring, their ability to locate and predict future peaks in caterpillar biomass using olfaction is likely to be advantageous. Therefore, we tested whether an insectivorous songbird that naturally inhabits oak dominated forests can be trained to detect early spring infestation by hatchling caterpillars, at a time when oaks begin bursting, and birds prepare to breed. Tree buds were either infested with caterpillars or left as a control and visually obscured in a Y-Maze choice test. Additionally, we measured testosterone and 17ß-estradiol as they influence olfactory perception in mammals and are linked to reproduction in vertebrates. After being trained to associate the presence of HIPVs with that of food, blue tits spent more time with, were more active around, and more frequently chose to first visit the infested trees, showing that blue tits can smell caterpillar activity. Males with higher testosterone spent more time around infested trees, suggesting that foraging behavior during the pre-breeding season is linked with a major reproductive signal. There was no relationship between foraging and estradiol in females. These results are an important foundation for further investigation of the role of hormones in avian olfaction and how smell may be useful for making breeding decisions that could improve reproductive success.

Breeding at higher latitude is associated with higher photoperiodic threshold and delayed reproductive development in a songbird.

Many seasonally breeding animals exhibit a threshold day length (critical photoperiod; CPP) for gonadal growth, and populations breeding at higher latitudes typically have a higher CPP. Much less is known about latitudinal variation in CPP in migratory population that winter away from their breeding range and must time their reproduction to match favorable conditions at their destination. To address the relationship between migration, breeding latitude, and CPP, we held two closely related songbird populations in a common environment. One population is resident (Junco hyemalis carolinensis), the other winters in sympatry with the residents but migrates north to breed (Junco hyemalis hyemalis). We gradually increased photoperiod and measured indices of readiness to migrate (fat score, body mass) and breed (cloacal protuberance volume, baseline testosterone, and gonadotropin releasing hormone challenged testosterone). To estimate breeding latitude, we measured hydrogen isotopes in feathers grown the preceding year. As we predicted, we found a higher CPP in migrants than residents, and a higher CPP among migrants deriving from higher as opposed to lower latitudes. Migrants also terminated breeding earlier than residents, indicating a shorter breeding season. To our knowledge, this is a first demonstration of latitudinal variation in CPP-dependent reproductive timing in bird populations that co-exist in the non-breeding season but breed at different latitudes. We conclude that bird populations appear to exhibit local adaptation in reproductive timing by relying on differential CPP response that is predictive of future conditions on the breeding ground.

Food and temperature change photoperiodic responses in two vole species.

Seasonal timing of reproduction in voles is driven by photoperiod. We hypothesized that a negative energy balance can modify spring-programmed photoperiodic responses in the hypothalamus, controlling reproductive organ development. We manipulated energy balance by the 'work-for-food' protocol, in which voles were exposed to increasing levels of food scarcity at different ambient temperatures under long photoperiod. We found that in common voles (Microtus arvalis) and tundra voles (Microtus oeconomus), photoperiod-induced pars tuberalis thyroid-stimulating hormone ß-subunit (Tshß) expression is reduced to potentially inhibit gonadal development when food is scarce. Reduction in gonadal size is more pronounced in tundra voles, in which anterior hypothalamic Kiss1 is additionally downregulated, especially in males. Low temperature additionally leads to decreased hypothalamic Rfrp expression, which potentially may facilitate further suppression of gonadal growth. Shutting off the photoperiodic axis when food is scarce in spring may be an adaptive response to save energy, leading to delayed reproductive organ development until food resources are sufficient for reproduction, lactation and offspring survival. Defining the mechanisms through which metabolic cues modify photoperiodic responses will be important for a better understanding of how environmental cues impact reproduction.

Central and peripheral actions of melatonin on reproduction in seasonal and continuous breeding mammals.

Under field conditions, especially for mammals that inhabit high latitudes, the regulation of seasonal breeding activity to ensure delivery of the young at the time most conducive to their survival is essential. This is most frequently accomplished by the annual reproductive cycle being linked to seasonal photoperiod changes which determine the nocturnal duration of the pineal melatonin signal. Mating can occur during any season that ensures spring/early summer delivery of the offspring. Thus, the season of mating is determined by the duration of pregnancy. The precise hormonal control of the annual cycle of reproduction by melatonin is accomplished at the level of the hypothalamo-pituitary axis which, in turn, determines the physiological state of the gonad and adnexa due to the regulation of pituitary gonadotrophin release. Many species are continuous rather than seasonal breeders. In these species, melatonin has a minor hormonal influence on the central regulation of reproduction but, nevertheless, its antioxidant functions at the level of the gonads support optimal reproductive physiology. Possibly like all cells, those in the ovary, e.g., granulosa cells and oocytes (less is known about melatonin synthesis by the testes or spermatogenic cells), synthesize melatonin which is used locally to combat free radicals and reactive nitrogen species which would otherwise cause oxidative/nitrosative stress to these critically important cells. Oxidative damage to the oocyte, zygote, blastocyst, etc., results in an abnormal fetus which is either sloughed or gives rise to an unhealthy offspring. The importance of the protection of the gametes (both oocytes and sperm) from oxidative molecular mutilation cannot be overstated. Fortunately, as a highly effective free radical scavenger and indirect antioxidant (by upregulating antioxidant enzyme), locally-produced melatonin is in the optimal location to protect the reproductive system from such damage.

Relationship between the seasonal changes in plasma testosterone and thyroxine concentrations with sperm cryoresistance in Gabon bucks.

Gabon buck is a breed with little marked seasonality in our latitude (Uruguay, 35° SL). The role of thyroid hormones on the regulation of their seasonal reproductive activity and sperm cryoresistance is unknown. Seasonal changes in testosterone concentration can affect sperm variables, but the influence of testosterone changes on sperm cryoresistance in other species determines that the recommended time for freezing sperm does not coincide with the period with greater sperm fresh quality. The objectives of the present work were to (i) describe the thyroxine seasonal pattern in bucks in a subtropical area, and its association with annual changes in sperm variables; (ii) relate the seasonal changes of testosterone and thyroxine concentrations with the sperm cryoresistance. For one year, semen of 10 adult Gabon bucks was collected by electroejaculation every two weeks. After sperm selection, the sample was frozen. Testosterone and thyroxine concentrations varied according to the month (P < 0.0001). Testosterone reached the greatest values in April (P < 0.0001) and May (P < 0.0001) and thyroxine reached minimum values (P < 0.0001) in the same months. During these months, a negative correlation ratio (CR) was found between testosterone concentration and CR-functional membrane (R = - 0.50; P < 0.0001). CR values for most sperm variables decreased during March-May, coinciding with the presence of maximum testosterone concentrations. In conclusion, high testosterone levels are associated with the worst sperm response to freezing-thawing process. Thyroxine concentrations have a strong seasonal pattern, but there was no relationship to sperm cryoresistance.

Evolution of Reproduction Periods in Seasonal Environments.

AbstractMany species are subject to seasonal cycles in resource availability, affecting the timing of their reproduction. Using a stage-structured consumer-resource model in which juvenile development and maturation are resource dependent, we study how a species' reproductive schedule evolves, dependent on the seasonality of its resource. We find three qualitatively different reproduction modes. First, continuous income breeding (with adults reproducing throughout the year) evolves in the absence of significant seasonality. Second, seasonal income breeding (with adults reproducing unless they are starving) evolves when resource availability is sufficiently seasonal and juveniles are more efficient resource foragers. Third, seasonal capital breeding (with adults reproducing partly through the use of energy reserves) evolves when resource availability is sufficiently seasonal and adults are more efficient resource foragers. Such capital breeders start reproduction already while their offspring are still experiencing starvation. Changes in seasonality lead to continuous transitions between continuous and seasonal income breeding, but the change between income and capital breeding involves a hysteresis pattern, such that a population's evolutionarily stable reproduction pattern depends on its initial one. Taken together, our findings show how adaptation to seasonal environments can result in a rich array of outcomes, exhibiting seasonal or continuous reproduction with or without energy reserves.