Dimorphic Structures Research Articles

Developmental fluoxetine exposure and prenatal stress alter sexual differentiation of the brain and reproductive behavior in male rat offspring

Depression during pregnancy and postpartum is a significant health problem and affects up to 20% of women. While selective serotonin reuptake inhibitor (SSRI) medications are the drug of choice for treatment of maternal depression, the combined effect of maternal depression and perinatal SSRI exposure on offspring development is poorly investigated. Our aim was to determine the role of exposure to fluoxetine during development on sexual behavior and sexually dimorphic brain structures in male offspring using a rodent model of maternal adversity. Sprague-Dawley rat dams were stressed during gestation and were chronically treated throughout lactation with either fluoxetine or vehicle beginning on postnatal day 1. Four groups of offspring were used: (1) Control+Vehicle, (2) Control+Fluoxetine, (3) Prenatal Stress+Vehicle, and (4) Prenatal Stress+Fluoxetine. We show here that developmental fluoxetine treatment decreases the anogenital distance in juvenile male offspring. In adult male offspring, maternal fluoxetine treatment results in a decrease in the number of intromissions, a longer latency to the first intromission, and a longer latency to the first ejaculation. Furthermore, developmental fluoxetine and/or prenatal stress decrease the area of the sexually dimorphic nucleus of the preoptic area (SDN-POA). Prenatal stress, but not exposure to developmental fluoxetine, decreases the number of tyrosine hydroxylase (TH)-positive cells in anteroventral periventricular nucleus (AVPv) and the volume of the posterior bed nucleus of the stria terminalis (pBST) in male offspring. These results provide important evidence for the long-term impact of maternal adversity and maternal fluoxetine use on the development of primary endocrinology systems in juvenile and adult male offspring.

Functional implications of ontogenetic and sexual dimorphic dentition in the eastern shovelnose ray Aptychotrema rostrata (Shaw & Nodder, 1794)

Unlike other elasmobranchs, batoids exhibit sexually dimorphic dentition. The functional implications of such dentition, however, remain understudied. For the present study, ontogenetic and sexual dimorphism in tooth and jaw structure, together with the functional implications of this dimorphism, were determined in the eastern shovelnose ray, Aptychotrema rostrata. Sexually dimorphic dentition and jaw structure was first observed in sub-adult age classes, with males developing a pronounced lower jaw at the symphysis. Monognathic heterodonty was prominent in mature males, with teeth in the symphyseal region developing significantly greater heights and sharpness ratios in comparison to females. Ex vivo mechanical grip strength tests were used to determine simulated bite-grip tenacity. The mean peak pull-out forces required to withdraw a section of a dissected pectoral fin from between jaws closed with a constant occlusal force was highest for mature males, intermediate for mature females and lowest for immature females and males. Although the species exhibits ontogenetic variations in diet, these were unrelated to sex. Rather, the larger and highly cuspidate teeth of mature males increased the bite-grip tenacity, which likely aids in copulation.

Testosterone production, sexually dimorphic morphology, and digit ratio in the dark-eyed junco

The hormonal environment an individual experiences during development can have lasting effects on behavior, morphology, and physiology. However, measuring endogenous hormone exposure during early embryonic development and relating it to adult phenotype has proved to be challenging. The relative length of digit 2 to digit 4 (2D:4D) in adults is thought to reflect the relative concentration of androgens and estrogens during development and has been used as a morphological proxy of developmental hormone exposure, enabling the exploration of the relationships between individual differences in hormone exposure and phenotype. Here, we use this approach and ask whether 2D:4D relates to the responsiveness of the adult hypothalamicpituitary-gonadal axis and to sexually dimorphic structures (wing, tail, and tarsus length) in a common songbird, the dark-eyed junco (Junco hyemalis). Among males, we found a negative relationship between 2D:4D and the ability to elevate testosterone in response to a physiological challenge, an injection of gonadotropin-releasing hormone. We also found age- and sex-specific relationships between 2D:4D and wing, tail, and tarsus length. We found a positive relationship between 2D:4D and body size measures in females, and second-year and older males, but a negative relationship in first-year males. We conclude that individual variation in exposure to developmental hormones, as reflected by 2D:4D, is correlated with adult hormone production ability and sexually dimorphic morphology in adulthood, suggesting that endogenous variation in steroid hormone exposure may have long-term consequences similar to those seen in experimental manipulations. Key wor ds: digit ratio, gonadotropinreleasing hormone, junco, maternal hormones, testosterone, 2D:4D. [Behav Ecol]

Sex determination in beetles: Production of all male progeny by Parental RNAi knockdown of transformer

Sex in insects is determined by a cascade of regulators ultimately controlling sex-specific splicing of a transcription factor, Doublesex (Dsx). We recently identified homolog of dsx in the red flour beetle, Tribolium castaneum (Tcdsx). Here, we report on the identification and characterization of a regulator of Tcdsx splicing in T. castaneum. Two male-specific and one female-specific isoforms of T. castaneum transformer (Tctra) were identified. RNA interference-aided knockdown of Tctra in pupa or adults caused a change in sex from females to males by diverting the splicing of Tcdsx pre-mRNA to male-specific isoform. All the pupa and adults developed from Tctra dsRNA injected final instar larvae showed male-specific sexually dimorphic structures. Tctra parental RNAi caused an elimination of females from the progeny resulting in production of all male progeny. Transformer parental RNAi could be used to produce all male population for use in pest control though sterile male release methods.

Characterization of the G‐protein‐coupled membrane‐bound estrogen receptor GPR30 in the zebra finch brain reveals a sex difference in gene and protein expression

Estradiol-induced structural dimorphisms exist in the songbird brain. However, how they arise is not clear since there is a scarce distribution of ERα and lack of ERβ in song control nuclei. This suggests that other receptors are involved. The G-protein coupled membrane-bound estrogen receptor, GPR30, is a candidate but has never been investigated in songbirds. In this study, we characterized its gene and protein in the zebra finch brain. Analysis of the putative GPR30 protein sequence revealed a strong similarity to avian and mammalian homologues. Quantitative PCR indicated that the gene was elevated in the telencephalon of both sexes from posthatching day (P) 15 to P45, with a male-biased sex difference at P21 and P30. In comparison, expression at younger posthatching ages and in adults was significantly less. At P21, GRP30 protein was widespread, nonuniform, and overlapped with song control nuclei. Of particular interest, the number of immunoreactive cells was greatest in HVC and RA, but less in LMAN and Area X. Labeling in HVC was also dimorphic; with more cells present in males than in females. In parallel with the gene, by adulthood, protein expression was reduced across most brain regions. Taken together these data suggest that GPR30 may contribute to differences in song system development by mediating dimorphic responses to estrogens. In addition, the extensive protein distribution indicates that it may also have a role in general brain development in both sexes.

Sex differences in cognition in healthy elderly individuals

ABSTRACT Sex differences in patterns of cognitive test performance have been attributed to factors, such as sex hormones or sexual dimorphisms in brain structure, that change with normal aging. The current study examined sex differences in patterns of cognitive test performance in healthy elderly individuals. Cognitive test scores of 957 men and women (age 67–89), matched for overall level of cognitive test performance, age, education, and depression scale score, were compared. Men and women were indistinguishable on tests of auditory divided attention, category fluency, and executive functioning. In contrast, women performed better than men on tests of psychomotor speed and verbal learning and memory, whereas men outperformed women on tests of visuoconstruction and visual perception. Our finding that the pattern of sex differences in cognition observed in young adults is observed in old age has implications for future studies of both healthy elderly individuals and of those with cognitive disorders.

Dark-Enhanced Startle Responses and Heart Rate Variability in a Traumatized Civilian Sample

Trauma is associated with increased risk for anxiety disorders such as posttraumatic stress disorder (PTSD). To further understand biologic mechanisms of PTSD, we examined the dark-enhanced startle response, a psychophysiological correlate of anxiety, and heart rate variability (HRV) in traumatized individuals with and without PTSD. The associations of these measures with PTSD may be sex-specific because of their associations with the bed nucleus of the stria terminalis, a sexually dimorphic brain structure in the limbic system that is approximately 2.5 times larger in men than in women. The study sample (N = 141) was recruited from a highly traumatized civilian population seeking treatment at Grady Memorial Hospital in Atlanta, Georgia. Psychophysiological responses during a dark-enhanced startle paradigm task included startle magnitude, assessed by eyeblink reflex, and measures of high-frequency HRV, during light and dark phases of the startle session. The startle magnitude was higher during the dark phase than the light phase (mean ± standard error = 98.61 ± 10.68 versus 73.93 ± 8.21 μV, p < .001). PTSD was associated with a greater degree of dark-enhanced startle in women (p = .03) but not in men (p = .38, p interaction = .48). Although HRV measures did not differ between phases, high-frequency HRV was greater in men with PTSD compared with men without PTSD (p = .02). This study demonstrates that the dark-enhanced paradigm provides novel insights into the psychophysiological responses associated with PTSD in traumatized civilian sample. Sex differences in altered parasympathetic and sympathetic function during anxiety regulation tasks may provide further insight into the neurobiological mechanisms of PTSD.

Sex-specific gene interactions in the patterning of insect genitalia

Genitalia play an important role in the life histories of insects, as in other animals. These sexually dimorphic structures evolve rapidly and derive from multiple body segments. Despite the importance of insect genitalia, descriptions of their genetic patterning have been limited to fruit flies. In this study, we report the functions, interactions and regulation of appendage patterning genes (e.g. homothorax, dachshund, and Distal-less) in two insects: the milkweed bug Oncopeltus fasciatus, and the red flour beetle Tribolium castaneum. These species differ in the anatomical complexity of their genitalia. Females of T. castaneum have a terminal ovipositor ending in short styli, while O. fasciatus have a multi-jointed subterminal ovipositor. Male O. fasciatus have a genital capsule consisting of large gonocoxopodites and claspers; T. castaneum males have relatively simple genitalia. The requirement of appendage-patterning genes in males differed between the two species: No defects were observed in T. castaneum male genitalia, and while the male claspers of O. fasciatus were affected by depletion of appendage-patterning genes, the proximal gonocoxopodite was not, suggesting a non-appendicular origin for this structure. Only the styli of the T. castaneum ovipositor were affected by RNAi depletion of appendage-patterning genes (14 genes in all). The posterior Hox genes ( abdominal-A and Abdominal-B) were required for proper genital development in O. fasciatus and regulated Distal-less and homothorax similarly in both sexes. Distal-less and dachshund were regulated differently in male and female O. fasciatus. Knockdown of the sex determination gene intersex produced a partial female-to-male transformation of abdominal and genital anatomy and also resulted in abrogation of female-specific regulation of these genes. These results provide developmental genetic support for specific anatomical hypotheses of serial homology. Importantly, these gene functions and interactions describe the developmental patterning of sexually dimorphic structures that have been critical to the diversification of these species-rich insect groups.

Complex Interplay of Evolutionary Forces in the ladybird Homeobox Genes of Drosophila melanogaster

Tandemly arranged paralogous genes lbe and lbl are members of the Drosophila NK homeobox family. We analyzed population samples of Drosophila melanogaster from Africa, Europe, North and South America, and single strains of D. sechellia, D. simulans, and D. yakuba within two linked regions encompassing partial sequences of lbe and lbl. The evolution of lbe and lbl is highly constrained due to their important regulatory functions. Despite this, a variety of forces have shaped the patterns of variation in lb genes: recombination, intragenic gene conversion and natural selection strongly influence background variation created by linkage disequilibrium and dimorphic haplotype structure. The two genes exhibited similar levels of nucleotide diversity and positive selection was detected in the noncoding regions of both genes. However, synonymous variability was significantly higher for lbe: no nonsynonymous changes were observed in this gene. We argue that balancing selection impacts some synonymous sites of the lbe gene. Stability of mRNA secondary structure was significantly different between the lbe (but not lbl) haplotype groups and may represent a driving force of balancing selection in epistatically interacting synonymous sites. Balancing selection on synonymous sites may be the first, or one of a few such observations, in Drosophila. In contrast, recurrent positive selection on lbl at the protein level influenced evolution at three codon sites. Transcription factor binding-site profiles were different for lbe and lbl, suggesting that their developmental functions are not redundant. Combined with our previous results on nucleotide variation in esterase and other homeobox genes, these results suggest that interplay of balancing and directional selection may be a general feature of molecular evolution in Drosophila and other eukaryote genomes.

Automated Analysis of Craniofacial Morphology Using Magnetic Resonance Images

Quantitative analysis of craniofacial morphology is of interest to scholars working in a wide variety of disciplines, such as anthropology, developmental biology, and medicine. T1-weighted (anatomical) magnetic resonance images (MRI) provide excellent contrast between soft tissues. Given its three-dimensional nature, MRI represents an ideal imaging modality for the analysis of craniofacial structure in living individuals. Here we describe how T1-weighted MR images, acquired to examine brain anatomy, can also be used to analyze facial features. Using a sample of typically developing adolescents from the Saguenay Youth Study (N = 597; 292 male, 305 female, ages: 12 to 18 years), we quantified inter-individual variations in craniofacial structure in two ways. First, we adapted existing nonlinear registration-based morphological techniques to generate iteratively a group-wise population average of craniofacial features. The nonlinear transformations were used to map the craniofacial structure of each individual to the population average. Using voxel-wise measures of expansion and contraction, we then examined the effects of sex and age on inter-individual variations in facial features. Second, we employed a landmark-based approach to quantify variations in face surfaces. This approach involves: (a) placing 56 landmarks (forehead, nose, lips, jaw-line, cheekbones, and eyes) on a surface representation of the MRI-based group average; (b) warping the landmarks to the individual faces using the inverse nonlinear transformation estimated for each person; and (3) using a principal components analysis (PCA) of the warped landmarks to identify facial features (i.e. clusters of landmarks) that vary in our sample in a correlated fashion. As with the voxel-wise analysis of the deformation fields, we examined the effects of sex and age on the PCA-derived spatial relationships between facial features. Both methods demonstrated significant sexual dimorphism in craniofacial structure in areas such as the chin, mandible, lips, and nose.

Encephalization and Brain Organization of Mobulid Rays (Myliobatiformes, Elasmobranchii) with Ecological Perspectives

In the present study the brain mass to body mass ratio and external morphological features of the brain of Mobula japanica, Mobula thurstoni and Manta birostris (devilrays) are described. The Mobulids extended the upper boundary of the minimum convex polygon described earlier by other authors for batoids, which is plotted on a double logarithmic scale of brain to body mass, causing some change in the allometric coefficient. The encephalization quotient of Mobulas was higher than unity, therefore it can be concluded that the actual brain mass is greater than expected by the given body mass. M. japanica had the highest percentage (61%) of telencephalic mass from all batoids, while the brain mass of M. birostris was the highest of all fish studied so far. The gross morphology of the enlarged Mobulid telencephalon and cerebellum prominently resembled to that of Sphyrna mokarran (great hammerhead shark). A structural dimorphism of the highly foliated cerebellum was detected between genders of the M. japanica, albeit with a small sample size. No such gender-related dimorphism was detected in brain mass/body mass ratio. Other brain parts were similar to those of other elasmobranch species. The data are discussed in terms of their ecological and evolutionary significance

A human-mouse conserved sex bias in amygdala gene expression related to circadian clock and energy metabolism

BackgroundMajor depression affects twice as many women as men, but the underlying molecular mechanisms responsible for the heightened female vulnerability are not known. The amygdala, composed of heterogeneous subnuclei, participates in multiple functional circuits regulating emotional responses to stress. We hypothesized that sex differences in molecular structure may contribute to differential mood regulation and disease vulnerability.FindingsUsing gene arrays followed by quantitative PCR validation, we compared the transcriptome profiles between sexes in human and mouse amygdala. We now report sexually dimorphic features of transcriptomes in the basolateral nucleus of the amygdala, and these features are highly conserved across species. A functional analysis of differential gene expression showed that mitochondrial-related gene groups were identified as the top biological pathways associated with sexual dimorphism in both species.ConclusionsThese results suggest that the basolateral amygdala is a sexually dimorphic structure, featuring a regulatory cascade of mitochondrial function and circadian rhythm, potentially linked through sirtuins and hormone nuclear receptors. Hence, baseline differences in amygdalar circadian regulation of cellular metabolism may contribute to sex-related differences in mood regulation and vulnerability to major depression.

Sex, Ecology and the Brain: Evolutionary Correlates of Brain Structure Volumes in Tanganyikan Cichlids

Analyses of the macroevolutionary correlates of brain structure volumes allow pinpointing of selective pressures influencing specific structures. Here we use a multiple regression framework, including phylogenetic information, to analyze brain structure evolution in 43 Tanganyikan cichlid species. We analyzed the effect of ecological and sexually selected traits for species averages, the effect of ecological traits for each sex separately and the influence of sexual selection on structure dimorphism. Our results indicate that both ecological and sexually selected traits have influenced brain structure evolution. The patterns observed in males and females generally followed those observed at the species level. Interestingly, our results suggest that strong sexual selection is associated with reduced structure volumes, since all correlations between sexually selected traits and structure volumes were negative and the only statistically significant association between sexual selection and structure dimorphism was also negative. Finally, we previously found that monoparental female care was associated with increased brain size. However, here cerebellum and hypothalamus volumes, after controlling for brain size, associated negatively with female-only care. Thus, in accord with the mosaic model of brain evolution, brain structure volumes may not respond proportionately to changes in brain size. Indeed selection favoring larger brains can simultaneously lead to a reduction in relative structure volumes.

Sexual dimorphism of gonadal structure and gene expression in germ cell-deficient loach, a teleost fish

Germ cell-deficient fish usually develop as phenotypic males. Thus, the presence of germ cells is generally considered to be essential for female gonadal differentiation or the maintenance of ovarian structure. However, little is known of the role of germ cells in the determination of the sexual fate of gonadal somatic cells. We have established an inducible germ cell deficiency system in the loach (Misgurnus anguillicaudatus, Cypriniformes: Cobitidae), a small freshwater fish, using knockdown of the dead end gene with a morpholino antisense oligonucleotide. Interestingly, loach lacking germ cells could develop as either phenotypic males or females, as characterized morphologically by the presence or absence of bony plates in the pectoral fins, respectively. The phenotypic males and females had testicular and ovarian structures, respectively, but lacked germ cells. Gene expression patterns in these male and female germ cell-deficient gonads were essentially the same as those in gonads of normal fish. Our observations indicate that sexually dimorphic gonads can develop in germ cell-deficient loach. In contrast to the situation in other model fish species, the gonadal somatic cells in phenotypic females autonomously differentiated into ovarian tissues and also played a role in the maintenance of gonadal structure. On the basis of our observations, we propose two possible models to explain the role of germ cells in sex determination in fish.

Retrotransposition and Structural Variation in the Human Genome

New assays are revealing that the diploid human genome contains extensive amounts of structural variation. Genome-wide approaches described in three papers in this issue (Beck et al., 2010; Huang et al., 2010; Iskow et al., 2010) paint a dynamic portrait of our genome, revealing a prominent role for repetitive sequences in shaping its structural variation.

Sexually dimorphic gall structures correspond to differential phytohormone contents in male and female wasp larvae

Abstract.Sexually dimorphic galls are rare among gall‐inducing insects and the reason for their occurrence is unknown. The pteromalid waspTrichilogaster acaciaelongifoliae, which induces galls onAcacia longifolia, is one such species. In the present study, the anatomical and physiological attributes of male and female galls ofT.acaciaelongifoliaeare examined and compared. Histological preparations are used to characterize anatomical differences between male and female gall chambers. Bioassays, high‐performance liquid chromatography‐mass spectrometry and an enzyme immunoassay are used to measure concentrations of auxin and cytokinin in normal buds, galled tissues, and larvae of both sexes. Female chambers are found to be 3.3‐fold larger, and are associated with 1.5‐fold more storage tissue and 3.5‐fold more vascular tissues than male chambers. Tissues from female chambers induce stronger cytokinin‐like bioactivity than tissues from male chambers. Female larvae have considerably higher concentrations of cytokinin free bases, ribosides, glucosides and monophosphates than male larvae; higher auxin‐like bioactivity than in normal or galled plant tissues; and almost twice the concentration of auxin than male larvae. Both male and female larvae contain much higher auxin concentrations than either galled or normal plant tissues. These findings suggest that differing levels of phytohormones are involved in the development of sexual dimorphism of gall structures in this species.

Antennal courtship and functional morphology of tyloids in the parasitoid wasp Syrphoctonus tarsatorius (Hymenoptera: Ichneumonidae: Diplazontinae)

Courtship behaviour and associated morphological characters are believed to evolve under diversifying sexual selection. In Hymenoptera, sexually dimorphic antennal structures, the ‘tyloids’, show a large variability. Although crucial for functional interpretation, the link between tyloid morphology and courtship behaviour has gained only limited attention. Here, we investigate antennal morphology and antennal courtship in the parasitoid wasp Syrphoctonus tarsatorius (Hymenoptera: Ichneumonidae: Diplazontinae). We confirm the glandular nature of the tyloids by light and scanning electron microscopy. Moreover, we report a new form of antennation during courtship, antennal double-coiling, which links morphology and behaviour by bringing the tyloids in direct contact with the antennae of the female, thus probably facilitating the transfer of a contact pheromone. We show that a change in haemolymph pressure is the activator of the antennal movement and that it can be reproduced in the laboratory using amputated antennae. Investigations of antennal structure and movement in three additional hymenopteran species suggest that the number and location of tyloids coincide with the modality of antennal coiling. Our method for simulating antennal movement will enable retrieving information about courtship behaviour from museum specimens, thus leading to a better understanding of the evolution of courtship behaviour in Hymenoptera.

Effects of parity on pelvic size and shape dimorphism in Mus

The pelvis is a sexually dimorphic structure and although the causes of that dimorphism have long been studied, relatively little is known regarding the effects of partuitive events on the magnitude of that dimorphism. Here, we use a sample of Mus musculus domesticus to contrast dimorphism in body length and os coxae size and shape between males and parous and nulliparous females. We also test for correlations between relative litter size (L/M) and relative offspring size (O/M) with body length and os coxae size and shape in parous females. Males had greater body length than nulliparous females but were not different from parous females. Females as a whole had the largest os coxae, with parous females having the largest and males the smallest. Os coxae shape was also significantly different between groups and was most divergent between parous females and males than between nulliparous females and males. Os coxae shape differences between females are associated with differences in body length between females and O/M is correlated with os coxae shape in parous females such that females with the largest offspring have the most divergent shapes along the relative warp one axis. Pelvic shape differences between males and females were consistent with previous findings in other taxa which identify the pubo-ischial complex as the primary region of dimorphism.

The Age of Puberty Determines Sexual Dimorphism in Bone Structure: A Male/Female Co-Twin Control Study

Taller stature and larger bone size in males are attributed to more rapid growth than in females. However, comparing sexes of the same age mismatches by pubertal stage, so males will be less mature than females. Comparing sexes of the same pubertal stage mismatches by age, so males will be older than females. We hypothesized that sex differences in stature and bone structure are the result of sex differences in the duration but not the rate of prepubertal and pubertal growth. We measured bone dimensions in 90 male/female co-twin pairs aged 7-18 yr using anthropometry and dual x-ray absorptiometry. Forty-two pairs had follow-up assessments. Within-pair differences were expressed as a percentage of the pair mean. Thirty percent of the 1-1.5 sd sex difference in bone widths and midfemur bending strength observed in 11 postpubertal pairs was present in 43 prepubertal pairs. In prepubertal pairs, annual growth in leg length was about 1.5 times truncal growth, but neither rate differed by sex. During puberty, truncal growth in both sexes was higher than before puberty but did not differ by sex. The longer period of pre- and intrapubertal growth in males produced most of the sex difference in bone morphology observed in postpubertal twins. Sex differences in bone morphology are the result of the later onset of puberty in males, not more rapid growth. Differences in bone widths are partly established before puberty.

Sexual dimorphism in brain structure and function: General population versus neuropsychiatric disorders

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