Sexually dimorphic responses to neonatal basal forebrain lesions in mice: II. Cortical morphology

Previous studies in the mouse have shown that neonatal lesions to the cholinergic basal forebrain (nBM) areas result in transient cholinergic depletion of neocortex and precipitate altered cortical morphogenesis. Lesion-induced morphological alterations in cortex persist into adulthood and are accompanied by behavioral changes, including spatial memory deficits. The current study investigated whether neonatal nBM lesions affect male and female mice differently in adulthood. Quantitative morphometry of cortical layer width was employed to assess alterations in cytoarchitecture in neonatally nBM-lesioned and littermate control mice of both sexes following behavioral testing. Our results showed significant decreases in cortical layer IV and V widths across somato/motor cortex in neonatally nBM lesioned mice of both sexes. Sexually dimorphic responses were observed in cortical layer II/III and total cortical width, limited to the area containing the “barrel cortex” representation of the whisker hairs. In lesioned females, layer II/III and total cortical width were decreased relative to female controls, and in lesioned males, layer II/III was increased relative to controls, whereas total cortical width was unchanged. In male but not female mice we observed significant correlations between decreased widths in layer IV and V and impaired performance on a spatial memory task. The current data further support a role of developing cholinergic cortical afferents in the modulation of cortical morphogenesis and cortical circuits involved in cognitive behaviors. In addition, our observations provide further evidence for sexually dimorphic development and function in cognitive centers of the rodent brain. © 1998 John Wiley & Sons, Inc. J Neurobiol 37: 595–606, 1998     

Relative growth,ontogeny, and sexual dimorphism in gorilla(Gorilla gorilla gorilla and G. g. beringei): Evolutionary and ecological considerations

Gorillas are the largest and among the most sexually dimorphic of all extant primates. While gorillas have been incorporated in broad-level comparisons among large-bodied hominoids or in studies of the African apes, comparisons between gorilla subspecies have been rare. During the past decade, however, behavioral, morphological, and molecular data from a number of studies have indicated that the western lowland (Gorilla gorilla gorilla) and eastern mountain (Gorilla gorilla beringei) subspecies differ to a greater extent than has been previously believed. In this study I compare patterns of relative growth of the postcranial skeleton to evaluate whether differences between subspecies result from the differential extension of common patterns of relative growth. In addition, patterns of ontogeny and sexual dimorphism are also examined. Linear skeletal dimensions and skeletal weight were obtained for ontogenetic series of male and female G.g. gorilla (n = 315) and G.g. beringei (n = 38). Bivariate and multivariate methods of analysis were used to test for differences in patterns of relative growth, ontogeny, and sexual dimorphism between sexes of each subspecies and in same-sex comparisons between subspecies. Results indicate males and females of both subspecies are ontogenetically scaled for postcranial proportions and that females undergo an earlier skeletal growth spurt compared to males. However, results also indicate that the onset of the female growth spurt occurs at different dental stages in lowland and mountain gorillas and that mountain gorillas may be characterized by higher rates of growth. Finally, data demonstrate lowland and mountain gorilla females do not differ significantly in adult body size, but mountain gorilla males are significantly larger than lowland gorilla males, suggesting mountain gorillas are characterized by a higher degree of sexual dimorphism in body size. Thus, although lowland and mountain gorillas do not appear to have evolved novel adaptations of the postcranium which correlate with differences in locomotor behavior, the present investigation establishes subspecies differences in ontogeny and sexual dimorphism which may be linked with ecological variation. Specifically, these findings are evaluated in the context of risk aversion models which predict higher growth rates and increased levels of sexual dimorphism in extreme folivores. Am. J. Primatol. 43:1–31, 1997. © 1997 Wiley-Liss, Inc.     

Sexual dimorphism and interspecific cranial form in two capuchin species: Cebus albifrons and C. apella

Ontogenetic patterns of sexual dimorphism and cranial form in two capuchin monkeys, Cebus albifrons and C. apella, are investigated by means of univariate, bivariate, and multivariate statistics. The analyses are based on 23 linear variables. Univariate analyses indicate that similar ontogenetic patterns of cranial sexual dimorphism are present; however, interspecific differences exist in timing. Ontogenetic scaling is present in both species' crania; however, it is more prevalent in C. albifrons. Several departures are present in cranial regions associated with orbital shape, the dental arcade, and the muscles of mastication. The latter two indicate that sexual differences in diet and/or foraging strategies may exist. Sexual selection is suggested as being the primary selective regime underlying the observed patterns of cranial sexual dimorphism in each species. Interspecific comparisons confirm that C. apella possesses a more dimorphic cranium than C. albifrons and that sexual dimorphism in C. apella begins earlier in development. Although interspecific ontogenetic scaling is present in some cranial variables, C. apella is not just a scaled-up version of C. albifrons. These sympatric congeners seem to be differentiated by variables related to the orbital region and the masticatory apparatus, as indicated by both departures from ontogenetic scaling and results of the discriminant function analysis. Ecological selection, rather than varying degrees of sexual selection, is likely to be responsible for this finding given that C. apella is known to consume hard-object foods. This is consistent with the predicted outcome of the competitive exclusion principle. Am J Phys Anthropol 104:487–511, 1997. © 1997 Wiley-Liss, Inc.     

Reproductive parameters of Bering-Chukchi-Beaufort Seas bowhead whales

Data from Bering-Chukchi-Beaufort Seas bowhead whales (Balaena mysticetus), harvested during 1973–2021 by aboriginal subsistence hunters, were used to estimate reproductive parameters: length at sexual maturity (LSM), age at sexual maturity (ASM), pregnancy rate (PR), and calving interval. Sexual maturity (N = 187 females) was determined from the presence/absence of corpora in the ovaries, or a fetus. Using sampling bias-corrected logistic regression, LSM was estimated at 13.5 m, 95% CI [13.0, 13.8]. There was a downward trend in LSM over time, statistically significant with one method but marginal with another. A growth model translated this estimate to an ASM estimate of 23.5 years, 95% CI [20.4, 26.7]. Pregnancy rate was determined from mature females (N = 125), and from a subset limited to certain autumn-caught whales (n = 37) to reduce bias. The PR was estimated at 0.46 globally, 95% CI [0.36, 0.55] and 0.38 for the autumn sample, 95% CI [0.20, 0.51]. Both estimated PRs are consistent with a 3-year calving interval, because the larger estimate includes two cohorts of pregnant whales harvested in spring, and bowhead whale gestation is longer than 12 months. These analyses represent the most conclusive empirical estimates of ASM, LSM, and PR for this bowhead whale stock from the largest available data sets to date.     

Beyond illness: Variation in haemosporidian load explains differences in vocal performance in a songbird

In animal communication, signals are expected to evolve to be honest, so that receivers avoid being manipulated by signalers. One way that signals can evolve to be honest is for them to be costly, with only high‐quality individuals being able to bear the costs of signal expression. It has been proposed that parasites can introduce costs that affect the expression of sexually selected traits, and there is evidence to support the role of parasitism in modulating animal behavior. If host infection status or intensity is found to relate to differences in signal expression, it may indicate a fitness cost that mediates honesty of signals. Birdsong is a good model for testing this, and physically challenging songs representing complex motor patterns provide a good example of sexually selected traits indicating individual condition. We performed a field study to evaluate the relationship between song performance and avian malaria infection in a common songbird. Previous work on this subject has almost always evaluated avian malaria in terms of binary infection status; however, parasitemia—infection intensity—is rarely assessed, even though differences in parasite load may have profound physiological consequences. We estimated parasitemia levels by using real‐time PCR. We found that birds with higher parasitemia displayed lower vocal performance, providing evidence that this song trait is an honest signal of parasitic load of haemosporidian parasites. To our knowledge, this study links parasite load and the expression of a sexually selected trait in a way that has not been addressed in the past. Studies using song performance traits and parasitemia offer an important perspective for understanding evolution of characters via sexual selection.     

Extra-pair paternity is not repeatable between years in Pied Flycatchers (Ficedula hypoleuca): a role for social context

Extra-pair paternity (EPP) is the consequence of the interactions between a social pair and extra-pair males during the female's fertile phase in a specific social context and ecological environment. Although EPP occurs in many avian species, there is a lack of understanding of how environmental factors may impact its frequency. Accordingly, the relative importance of individual characteristics on the one hand, and of their immediate social environment on the other, may affect EPP repeatability and thereby the capacity of this trait to respond to selection. If EPP is an individual genetically based trait that may respond to selection, we expect it to be repeatable across breeding seasons. To check this possibility, we analysed the within-individual repeatability in EPP of breeding males and females in two natural populations of Pied Flycatchers Ficedula hypoleuca in central Spain during three field seasons. We then studied the relationship between EPP and individual male and female traits (only some of which were themselves repeatable), as well as key context variables such as breeding synchrony and population density. Our results showed no repeatability for EPP in either sex. We found a positive association with laying date and stronger associations of EPP with male plumage and morphological traits than with female characteristics. We suggest that the variable social environment is an important modulator of EPP patterns, and that differences between field EPP studies in this respect may explain contradictory results in the same species, even in the same populations in different years.     

The evolution of the life cycle of brown seaweeds

The brown seaweeds (Phaeophyta) are well-suited for testing theories of the evolution of the sexual alternation of haploid and diploid generations because of the great diversity of life cycles within the phylum. Three theories are investigated in this paper. (1) Diploid growth evolves because it has the effect of complementing deleterious recessive mutations. This is rejected because (a) ancestral haplonty is not a parsimonious inference from current phylogenies; (b) the exaggeration of diploid growth does not evolve in a comb-like fashion; (c) forms with predominantly haploid growth have evolved from smaller isomorphic ancestors; and (d) there is no correlation between haploid growth and monoecy. (2) Diploid growth evolves when gamete dimorphism leads to intense sexual selection, favouring the production of genetically diverse gametes through meiosis. This is rejected because diere is no correlation between the dominance of the diploid generation and the degree of gamete dimorphism. It is possible to show that gamete dimorphism itself has evolved in the Phaeophyta through the increase in size of the macrogamete in forms that have evolved larger sporophytes. (3) Microthalli become specialized as gametophytes because fusion is promoted by releasing gametes into the boundary layer; macrothalli become specialized as sporophytes because dispersal is promoted by releasing zoospores into the water column. This is consistent with the sexual and reproductive biology of Phaeophyta. The classic sexual cycle can then be interpreted as evolving from an asexual alternation of microthallus and macrothallus, governed largely by environmental factors, through selection for the appropriate association of ploidy with vegetative size. The exceptions to this general rule are forms in which gametes are released from macrothalli, where a different suite of sexual characters has evolved.     

Effects of testosterone on the development of a sexually dimorphic neuromuscular system in ciliary neurotrophic factor receptor knockout mice

Motoneurons in the spinal nucleus of the bulbocavernosus (SNB) innervate the perineal muscles, bulbocavernosus (BC), and levator ani (LA). Testosterone regulates the survival of SNB motoneurons and BC/LA muscles during perinatal life. Previous findings suggest that effects of testosterone on this system may be mediated by trophic factors—in particular, by a factor acting through the ciliary neurotrophic factor α‐receptor (CNTFRα). To test the role of CNTFRα in the response of the developing SNB system to testosterone, CNTFRα +/+ and −/− mice were treated with testosterone propionate (TP) or oil during late embryonic development. BC/LA muscle size and SNB motoneuron number were evaluated on the day of birth. Large sex differences in BC and LA muscle size were present in newborn mice of both genotypes, but muscle volumes were reduced in CNTFRα −/− animals relative to same‐sex, wild‐type controls. Prenatal testosterone treatment completely eliminated the sex difference in BC/LA muscle size in wild‐type animals, and eliminated the effect of the CNTFRα gene deletion on muscle size in males. However, the effect of TP treatment on BC and LA muscle sizes was blunted in CNTFRα −/− females. SNB motoneuron number was sexually dimorphic in oil‐treated, wild‐type mice. In contrast, there was no sex difference in SNB motoneuron number in oil‐treated, CNTFRα knockout mice. Prenatal treatment with testosterone did not increase SNB motoneuron number in CNTFRα −/− mice, but also did not significantly increase SNB motoneuron number in newborn wild‐type animals. These findings confirm the absence of a sex difference in SNB motoneuron number in CNTFRα −/− mice. Moreover, the CNTFRα gene deletion influences perineal muscle development and the response of the perineal muscles to testosterone. Prenatal TP treatment of CNTFRα −/− males overcomes the effects of the gene deletion on the BC and LA muscles without a concomitant effect on SNB motoneuron number. © 1999 John Wiley & Sons, Inc. J Neurobiol 41: 317–325, 1999     

Androgen receptor mRNA expression in Xenopus laevis CNS: Sexual dimorphism and regulation in laryngeal motor nucleus

Using Northern analysis, in situ hybridization, and nuclease protection assays, the expression and regulation of androgen receptor messenger RNA (AR mRNA) was examined in the CNS of juvenile Xenopus laevis. Only one of the AR mRNA isoforms expressed in X. laevis is transcribed in the CNS as shown by Northern blot analysis. Nuclease protection assays demonstrate that the expression of AR mRNA is higher in the brain stem than in the telencephalon and diencephalon. Although expression of AR mRNA is widespread throughout the CNS, cells of cranial nerve nucleus IX-X (N. IX-X) and spinal cord display the highest in situ hybridization signals in their cytoplasm. Double labeling using horseradish peroxidase and digoxigenin labeled AR probes reveals that laryngeal and anterior spinal cord motor neurons express AR mRNA. More cells express AR mRNA in N. IX-X of males than of females. The number of AR expressing cells in N. IX-X decreases following gonadectomy in both sexes, and dihydrotestosterone (DHT) treatment for 1 month reverses this effect. Increased expression of AR mRNA in the brain of DHT treated animals is also apparent in nuclease protection assays. Sex differences in number of AR expressing cells and hormone regulation of AR mRNA expression in motor nuclei may influence neuromuscular systems devoted to sexually differentiated behaviors. © 1996 John Wiley & Sons, Inc.     

Sex difference among nonneuronal cells precedes sexually dimorphic neuron growth and survival in an avian song control nucleus

In zebra finches only males sing, and several song control nuclei contain more neurons in adult males than in females. In the robust nucleus of the archistriatum (RA), this sex difference in neuron number arises because neuron survival is greater in young males than in females. The events initiating this sex difference in neuron survival are not known, but in earlier studies we observed that during sexual differentiation the proliferation and/or survival of RA cells exhibiting glial morphology is greater in males than in females. Because glia and glia-derived molecules are known to exert trophic effects on developing neurons, we wanted to determine when the sex difference in RA glia develops relative to the sexually dimorphic growth and survival of RA neurons. Male and female zebra finches were injected twice daily with ³[H]thymidine for 2 days beginning either on day 15 or 27. Two days later (day 18 or 30) sections through the RA were processed for autoradiography. Virtually all of the ³[H]thymidine labeled cells within the RA exhibited morphological features characteristic of glia and were not immunoreactive for the neuron-specific antigen, Hu. The number of these ³[H]thymidine labeled cells was measured, as were the number and soma size of RA neurons. Sex differences in RA neuron number and soma size were not evident at day 18, but emerged by day 30. However, at both ages the density of ³[H]thymidine labeled RA cells and their total number/RA neuron were significantly greater in males than in females. No such sexual dimorphism in the density of ³[H]thymidine labeled cells was evident in the archistriatum lateral to the RA, or within the RA of adult birds. These data indicate that sexually dimorphic gliogenesis is an early event in the sexual differentiation of the RA, preceding sex differences in RA neuron growth and survival. The possibility that glia (or glia-derived substances) may contribute to the neurotrophic effects of masculinization within the RA is discussed. © 1996 John Wiley & Sons, Inc.