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Concept: Gonad

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The neurohypophyseal hormone arginine vasotocin (AVT) mediates behavioral and reproductive plasticity in vertebrates, and has been linked to the behavioral changes associated with protogyny in the bluehead wrasse (Thalassoma bifasciatum). In this study, we sequenced full-length cDNAs encoding two distinct V1a-type AVT receptors (v1a1 and v1a2) from the bluehead wrasse, and examined variation in brain and gonadal abundance of these receptor transcripts among sexual phases. End point RT-PCR revealed that v1a1 and v1a2 transcripts varied in tissue distribution, with v1a1 receptor mRNAs at greatest levels in the telencephalon, hypothalamus, optic tectum, cerebellum and testis, and v1a2 receptor transcripts most abundant in the hypothalamus, cerebellum and gills. In the brain, v1a1 and v1a2 mRNAs both localized by in situ hybridization to the dorsal and ventral telencephalon, the preoptic area of the hypothalamus, the ventral hypothalamus and lateral recess of the third ventricle. Quantitative real-time RT-PCR revealed that relative abundance of these two receptor mRNAs varied significantly in brain and gonad with sexual phase. Relative levels of v1a2 mRNAs were greater in whole brain and isolated hypothalamus of terminal phase (TP) male wrasse compared to initial phase (IP) males or females. In the gonad, v1a1 mRNAs were at levels 2.5-fold greater in the testes of IP males - and 4-5-fold greater in the testes of TP males - compared to the ovaries of females. These results provide evidence that V1a-type AVT receptor transcript abundance in the hypothalamus and gonads of bluehead wrasse varies in patterns linked to sexual phase, and bestow a foundation for future studies investigating how differential expression of v1a1 and v1a2 teleost AVT receptors links to behavioral status and gonadal function in fish more broadly.

Concepts: Neuroanatomy, Hypothalamus, Brain, Testicle, Reproductive system, Gamete, Ovary, Gonad

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Abstract Background: Histopathologic findings of gonadal torsion in neonates and infants (GTNI) are poorly defined in the literature. We describe herein the histopathologic spectrum of gonadal torsion (GT) with emphasis on the pediatric population and on features specific for NI (<=1 year of age). Design: Twenty-five cases of GTNI (6 females/18 males), 35 cases of GT in older pediatric population (OPP) (19 females/14 males) and 33 cases in adults (25 females/8 males) were found in our pathology files between 2003 and 2011. Results: Our findings disclose two categories of GT: the group of NI as opposed to that of OPP and adults, the latter sharing similar presentation as acute hemorrhagic necrosis of the gonad. Although findings in NI were rather uniform, a few differences were demonstrated between the two genders. All GTNI revealed calcifications, fibrosis, siderophages and extensive necrosis. However, prominent necrotizing palisaded granulomata were seen in most (4/6) cases of ovarian torsion, but not in the testicular counterpart. Furthermore, complete gonad regression was encountered exclusively in neonatal testicular torsion cases. Conclusions: - Pathologic findings in GT are distinctly different between NI and OPP, the latter being more comparable to adults, presenting with acute hemorrhagic necrosis. - The distinctive findings in GTNI of both genders include calcifications, siderophages and fibrosis, in addition to background necrosis. - Of particular note, complete gonadal regression is seen only in the testis in GTNI. - Finally, necrotizing palisaded granulomata are unique to the ovarian subgroup and are often extensive, obscuring the nature of the process.

Concepts: Infant, Testicle, Reproductive system, Necrosis, Endocrine system, Ovary, Gonad, Testicular torsion

23

In most mammals, the sex of an individual is genetically determined by the Y chromosome-specific SRY gene. The presence of at least one functional copy of this gene determines the development of the primordial gonads into testes. However, testicular tissue does develop in the absence of SRY, albeit rarely, which is the case in testicular XX (SRY-negative) disorder of sex development (DSD). This condition is very important for studying the process of sexual determination because it allows the identification of genetic factors that are able to promote the male developmental pathway in the absence of SRY and thereby enables a better understanding of this process. Until now, this condition has been identified in various animal species but has never been reported in cat. In this study, we describe the first case of an XX (SRY-negative) DSD cat. The cat possesses a tortoiseshell coat associated with male-like external genitalia, including normal scrotum with 2 palpably normal testicles. Histological analysis confirmed the presence of the testes, and cytogenetic and genetic analyses showed a female karyotype associated with the absence of the SRY gene. Finally, sequencing of the RSPO1 gene revealed no mutation, and FISH analysis of the SOX9 locus did not reveal any large abnormalities.

Concepts: Genetics, Biology, Sex, Testicle, Ovary, Scrotum, Gonad, Sex organ

9

Light pollution is known to affect important biological functions of wild animals, including daily and annual cycles. However, knowledge about long-term effects of chronic exposure to artificial light at night is still very limited. Here we present data on reproductive physiology, molt and locomotor activity during two-year cycles of European blackbirds (Turdus merula) exposed to either dark nights or 0.3 lux at night. As expected, control birds kept under dark nights exhibited two regular testicular and testosterone cycles during the two-year experiment. Control urban birds developed testes faster than their control rural conspecifics. Conversely, while in the first year blackbirds exposed to light at night showed a normal but earlier gonadal cycle compared to control birds, during the second year the reproductive system did not develop at all: both testicular size and testosterone concentration were at baseline levels in all birds. In addition, molt sequence in light-treated birds was more irregular than in control birds in both years. Analysis of locomotor activity showed that birds were still synchronized to the underlying light-dark cycle. We suggest that the lack of reproductive activity and irregular molt progression were possibly the results of i) birds being stuck in a photorefractory state and/or ii) chronic stress. Our data show that chronic low intensities of light at night can dramatically affect the reproductive system. Future studies are needed in order to investigate if and how urban animals avoid such negative impact and to elucidate the physiological mechanisms behind these profound long-term effects of artificial light at night. Finally we call for collaboration between scientists and policy makers to limit the impact of light pollution on animals and ecosystems.

Concepts: Sperm, Testicle, Reproductive system, Sertoli cell, Puberty, Ovary, Gonad, Epididymis

8

Across the animal kingdom, environmental light cues are widely involved in regulating gamete release, but the molecular and cellular bases of the photoresponsive mechanisms are poorly understood. In hydrozoan jellyfish, spawning is triggered by dark-light or light-dark transitions acting on the gonad, and is mediated by oocyte maturation-inducing neuropeptide hormones (MIHs) released from the ectoderm. We determined in Clytia hemisphaerica that blue-cyan light triggers spawning in isolated gonads. A candidate opsin (Opsin9) was found co-expressed with MIH within specialised ectodermal cells. Opsin9 knockout jellyfish generated by CRISPR/Cas9 failed to undergo oocyte maturation and spawning, a phenotype reversible by synthetic MIH. Gamete maturation and release in Clytia is thus regulated by gonadal photosensory-neurosecretory cells that secrete MIH in response to light via Opsin9. Similar cells in ancestral eumetazoans may have allowed tissue-level photo-regulation of diverse behaviours, a feature elaborated in cnidarians in parallel with expansion of the opsin gene family.

Concepts: Gene, Animal, Reproductive system, Gamete, Cnidaria, Jellyfish, Gonad, Hydrozoa

5

Mammalian sex determination is the unique process whereby a single organ, the bipotential gonad, undergoes a developmental switch that promotes its differentiation into either a testis or an ovary. Disruptions of this complex genetic process during human development can manifest as disorders of sex development (DSDs). Sex development can be divided into two distinct processes: sex determination, in which the bipotential gonads form either testes or ovaries, and sex differentiation, in which the fully formed testes or ovaries secrete local and hormonal factors to drive differentiation of internal and external genitals, as well as extragonadal tissues such as the brain. DSDs can arise from a number of genetic lesions, which manifest as a spectrum of gonadal (gonadal dysgenesis to ovotestis) and genital (mild hypospadias or clitoromegaly to ambiguous genitalia) phenotypes. The physical attributes and medical implications associated with DSDs confront families of affected newborns with decisions, such as gender of rearing or genital surgery, and additional concerns, such as uncertainty over the child’s psychosexual development and personal wishes later in life. In this Review, we discuss the underlying genetics of human sex determination and focus on emerging data, genetic classification of DSDs and other considerations that surround gender development and identity in individuals with DSDs.

Concepts: Gender, Testicle, Reproductive system, Developmental psychology, Puberty, Ovary, Gonad, Sex organ

3

Birds often adjust to urban areas by advancing the timing (phenology) of vernal gonad growth. However, the ecological and physiological bases of this adjustment are unclear. We tested whether the habitat-related disparity in gonad growth phenology of male Abert’s towhees, Melozone aberti, is due to greater food availability in urban areas of Phoenix, Arizona USA or, alternatively, a habitat-related difference in the phenology of key food types. To better understand the physiological mechanism underlying variation in gonad growth phenology, we compared the activity of the reproductive system at all levels of hypothalamo-pituitary-gonadal (HPG) axis. We found no habitat-associated difference in food availability (ground arthropod biomass), but, in contrast to the seasonal growth of leaves on desert trees, the leaf foliage of urban trees was already developed at the beginning of our study. Multiple estimates of energetic status did not significantly differ between the non-urban and urban populations during three years that differed in the habitat-related disparity in gonad growth and winter precipitation levels. Thus, our results provide no support for the hypothesis that greater food abundance in urban areas of Phoenix drives the habitat-related disparity in gonad growth phenology in Abert’s towhees. By contrast, they suggest that differences in the predictability and magnitude of change in food availability between urban and desert areas of Phoenix contribute to the observed habitat-related disparity in gonad growth. Endocrine responsiveness of the gonads may contribute to this phenomenon as desert - but not urban - towhees had a marked plasma T response to GnRH challenge.

Concepts: Biology, Ecology, Precipitation, City, Reproductive system, Leaf, Gonad, Desert

2

The scientific understanding of fear and anxiety-in both normal and pathological forms-is presently limited by a predominance of studies that use male animals and Pavlovian fear conditioning-centered paradigms that restrict and assess specific behaviors (e.g., freezing) over brief sampling periods and overlook the broader contributions of the spatiotemporal context to an animal’s behavioral responses to threats. Here, we use a risky “closed economy” system, in which the need to acquire food and water and the need to avoid threats are simultaneously integrated into the lives of rats, to examine sex differences in mitigating threat risk while foraging. Rats lived for an extended period (∼2 months) in enlarged chambers that consisted of a safe, bedded nest and a risky foraging area where footshocks could be delivered unpredictably. We observed that male and female rats used different strategies for responding to the threat of footshock. Whereas male rats increased the size of meals consumed to reduce the overall time spent foraging, female rats sacrificed their metabolic needs in order to avoid shocks. Ovarian hormone fluctuations were shown to exert slight but reliable rhythmic effects on risky decision-making in gonadally intact female rats. However, this did not produce significant differences in approach-avoidance trade-offs between ovariectomized and intact female groups, suggesting that male-female sex differences are not due to the activational effects of gonadal hormones but, rather, are likely to be organized during early development.

Concepts: Male, Sexual dimorphism, Gender, Sex, Reproductive system, Risk management, Gamete, Gonad

2

The aim of this study was to assess the cellular miRNA expression behaviour in testes with spermatogenic failure (SpF). We performed a high-throughput screen of 623 mature miRNAs by a quantitative RT-qPCR-based approach in histologically well-defined testicular samples with spermatogenic disruption at different germ-cell stages, which revealed altered patterns of miRNA expression. We focussed on the differentially expressed miRNAs whose expression correlated with the number of testicular mature germ-cells and described the combined expression values of a panel of three miRNAs (miR-449a, miR-34c-5p and miR-122) as a predictive test for the presence of mature germ-cells in testicular biopsy. Additionally, we determined decreased cellular miRNA content in developing germ-cells of SpF testis; this was more noticeable the earlier the stage of germ-cell differentiation was affected by maturation failure. Furthermore, we showed that the miRNA expression profile in mature sperm from mild SpF patients was widely altered. Our results suggest that the cellular miRNA content of developed germ-cells depends heavily on the efficacy of the spermatogenic process. What is more, spermatozoa that have fulfilled the differentiation process still retain the dysregulated miRNA pattern observed in the developing SpF germ-cells. This altered miRNA molecular signature may have functional implications for the male gamete.

Concepts: Male, Sperm, Cellular differentiation, Sex, Testicle, Sertoli cell, Puberty, Gonad

2

Mammalian sex determination initiates in the fetal gonad with specification of bipotential precursor cells into male Sertoli cells or female granulosa cells. This choice was long presumed to be irreversible, but genetic analysis in the mouse recently revealed that sexual fates must be maintained throughout life. Somatic cells in the testis or ovary, even in adults, can be induced to transdifferentiate to their opposite-sex equivalents by loss of a single transcription factor, DMRT1 in the testis or FOXL2 in the ovary. Here, we investigate what mechanism DMRT1 prevents from triggering transdifferentiation. We find that DMRT1 blocks testicular retinoic acid (RA) signaling from activating genes normally involved in female sex determination and ovarian development and show that inappropriate activation of these genes can drive sexual transdifferentiation. By preventing activation of potential feminizing genes, DMRT1 allows Sertoli cells to participate in RA signaling, which is essential for reproduction, without being sexually reprogrammed.

Concepts: Genetics, Human, Sex, Testicle, Reproductive system, Gamete, Ovary, Gonad