An official website of the United States government
Abstract Background Sexual-size dimorphism (SSD) is replete among animals, but while the selective pressures that drive the evolution of SSD have been well studied, the developmental mechanisms upon which these pressures act are poorly understood. Ours and others’ research has shown that SSD in D. melanogaster reflects elevated levels of nutritional plasticity in females versus males, such that SSD increases with dietary intake and body size, a phenomenon called sex-specific plasticity (SSP). Additional data indicate that while body size in both sexes responds to variation in protein level, only female body size is sensitive to variation in carbohydrate level. Here, we explore whether these difference in sensitivity at the morphological level are reflected by differences in how the insulin/IGF-signaling (IIS) and TOR-signaling pathways respond to changes in carbohydrates and proteins in females versus males, using a nutritional geometry approach. Results The IIS-regulated transcripts of 4E-BP and InR most strongly correlated with body size in females and males, respectively, but neither responded to carbohydrate level and so could not explain the sex-specific response to body size to dietary carbohydrate. Transcripts regulated by TOR-signaling did, however, respond to dietary carbohydrate in a sex-specific manner. In females, expression of dILP5 positively correlated with body size, while expression of dILP2,3 and 8, was elevated on diets with a low concentration of both carbohydrate and protein. In contrast, we detected lower levels of dILP2 and 5 protein in the brains of females fed on low concentration diets. We could not detect any effect of diet on dILP expression in males. Conclusion Although females and males show sex-specific transcriptional responses to changes in protein and carbohydrate, the patterns of expression do not support a simple model of the regulation of body-size SSP by either insulin- or TOR-signaling. The data also indicate a complex relationship between carbohydrate and protein level, dILP expression and dILP peptide levels in the brain. In general, diet quality and sex both affect the transcriptional response to changes in diet quantity, and so should be considered in future studies that explore the effect of nutrition on body size.
more »
« less
Sexual Size Dimorphism Correlates With the Number of Androgen Response Elements in Mammals, But Only in Small-Bodied Species
Abstract Sexual size dimorphism is common throughout the animal kingdom, but its evolution and development remain difficult to explain given most of the genome is shared between males and females. Sex-biased regulation of genes via sex hormone signaling offers an intuitive mechanism by which males and females could develop different body sizes. One prediction of this hypothesis is that the magnitude of sexual size dimorphism scales with the number of androgen response elements or estrogen response elements, the DNA motifs to which sex hormone receptors bind. Here, we test this hypothesis using 268 mammalian species with full genome assemblies and annotations. We find that in the two smallest-bodied lineages (Chiroptera and Rodentia), sexual size dimorphism increases (male-larger) as the number of androgen response elements in a genome increases. In fact, myomorph rodents—which are especially small-bodied with high sexual size dimorphism—show an explosion of androgen receptor elements in their genomes. In contrast, the three large-bodied lineages (orders Carnivora, Cetartiodactyla, and Primates) do not show this relationship, instead following Rensch's Rule, or the observation that sexual size dimorphism increases with overall body size. One hypothesis to unify these observations is that small-bodied organisms like bats and rodents tend to reach peak reproductive fitness quickly and are more reliant on hormonal signaling to achieve sexual size dimorphism over relatively short time periods. Our study uncovers a previously unappreciated relationship between sexual size dimorphism, body size, and hormone signaling that likely varies in ways related to life history.
more »
« less
- Award ID(s):
- 2027373
- PAR ID:
- 10655420
- Editor(s):
- Cortez, Diego
- Publisher / Repository:
- PLoS Genetics
- Date Published:
- Journal Name:
- Genome Biology and Evolution
- Volume:
- 17
- Issue:
- 4
- ISSN:
- 1759-6653
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
Bronikowski, Anne (Ed.)Abstract Phenotypic sexual dimorphism often involves the hormonal regulation of sex-biased expression for underlying genes. However, it is generally unknown whether the evolution of hormonally mediated sexual dimorphism occurs through upstream changes in tissue sensitivity to hormone signals, downstream changes in responsiveness of target genes, or both. Here, we use comparative transcriptomics to explore these possibilities in 2 species of Sceloporus lizards exhibiting different patterns of sexual dichromatism. Sexually dimorphic S. undulatus develops blue and black ventral coloration in response to testosterone, while sexually monomorphic S. virgatus does not, despite exhibiting similar sex differences in circulating testosterone levels. We administered testosterone implants to juveniles of each species and used RNAseq to quantify gene expression in ventral skin. Transcriptome-wide responses to testosterone were stronger in S. undulatus than in S. virgatus, suggesting species differences in tissue sensitivity to this hormone signal. Species differences in the expression of genes for androgen metabolism and sex hormone-binding globulin were consistent with this idea, but expression of the androgen receptor gene was higher in S. virgatus, complicating this interpretation. Downstream of androgen signaling, we found clear species differences in hormonal responsiveness of genes related to melanin synthesis, which were upregulated by testosterone in S. undulatus, but not in S. virgatus. Collectively, our results indicate that hormonal regulation of melanin synthesis pathways contributes to the development of sexual dimorphism in S. undulatus, and that changes in the hormonal responsiveness of these genes in S. virgatus contribute to the evolutionary loss of ventral coloration.more » « less
-
Abstract Background In most arthropods, adult females are larger than males, and male competition is a race to quickly locate and mate with scattered females (scramble competition polygyny). Variation in body size among males may confer advantages that depend on context. Smaller males may be favored due to more efficient locomotion leading to higher mobility during mate searching. Alternatively, larger males may benefit from increased speed and higher survivorship. While the relationship between male body size and mobility has been investigated in several systems, how different aspects of male body morphology specifically affect their locomotor performance in different contexts is often unclear. Results Using a combination of empirical measures of flight performance and modelling of body aerodynamics, we show that large body size impairs flight performance in male leaf insects ( Phyllium philippinicum ), a species where relatively small and skinny males fly through the canopy in search of large sedentary females. Smaller males were more agile in the air and ascended more rapidly during flight. Our models further predicted that variation in body shape would affect body lift and drag but suggested that flight costs may not explain the evolution of strong sexual dimorphism in body shape in this species. Finally, empirical measurements of substrate adhesion and subsequent modelling of landing impact forces suggested that smaller males had a lower risk of detaching from the substrates on which they walk and land. Conclusions By showing that male body size impairs their flight and substrate adhesion performance, we provide support to the hypothesis that smaller scrambling males benefit from an increased locomotor performance and shed light on the evolution of sexual dimorphism in scramble competition mating systems.more » « less
-
Abstract Climatic and soil features influence resources and mate availability for plants. Because of different resource/mating demands of the male and female reproductive pathways, environmental variation can drive geographic patterns of sex‐specific factors in sexually polymorphic species. Yet, the relationship between environment and sex, sexual dimorphism or sex chromosomes at the range‐wide scale is underexamined.Using ~7000 herbarium and iNaturalist specimens we generate a landscape‐scale understanding of how sex ratio and sexual dimorphism vary with geographic, climatic and soil gradients in the sexually polymorphic wild strawberry (Fragaria virginiana) and test whether these conform to predictions from theory. Then, for ~300 specimens we use genotyping of the sex‐determining region (SDR haplotypes) to reveal geographic and phenotypic patterns in sex chromosome types.Across North America, the sex ratio was hermaphrodite/male‐biased and was associated more with soil attributes than climate. Sex ratio‐environment associations matched predictions for subdioecy in the West but for gynodioecy in the East. Climatic factors correlated with sexual dimorphism in traits related to carbon acquisition (leaf size and runnering while flowering) but not mate access (petal size, flowering time). Variation in sexual dimorphism was due to one sex being more responsive to the environmental variation than the other. Specifically, leaf length in females was more responsive to variation in precipitation than in hermaphrodite/males, but the probability of runnering while flowering in hermaphrodite/males was more responsive to variation in temperature than in females. The ancestral sex chromosome type was most common overall. But the frequency of the more derived sex chromosomes varied with environmental factors that differed between East–West regions.Synthesis. A landscape‐level perspective revealed that variation in soil and climate factors can explain geospatial variation in sex ratio and sexual dimorphism in a wild strawberry. Variation in sex ratio was associated more with soil resources than climate, while variation in sexual dimorphism was the result of sex‐differential responses to climate for vegetative traits but a similar response to abiotic factors in mate access traits. Finally, sex chromosome types were associated with soil moisture and precipitation in ways that could contribute to the evolution of sex determination.more » « less
-
Sex differences in gene expression tend to increase with age across a variety of species, often coincident with the development of sexual dimorphism and maturational changes in hormone levels. However, because most transcriptome-wide characterizations of sexual divergence are framed as comparisons of sex-biased gene expression across ages, it can be difficult to determine the extent to which age-biased gene expression within each sex contributes to the emergence of sex-biased gene expression. Using RNAseq in the liver of the sexually dimorphic brown anole lizard ( Anolis sagrei ), we found that a pronounced increase in sex-biased gene expression with age was associated with a much greater degree of age-biased gene expression in males than in females. This pattern suggests that developmental changes in males, such as maturational increases in circulating testosterone, contribute disproportionately to the ontogenetic emergence of sex-biased gene expression. To test this hypothesis, we used four different experimental contrasts to independently characterize sets of genes whose expression differed as a function of castration and/or treatment with exogenous testosterone. We found that genes that were significantly male-biased in expression or upregulated as males matured tended to be upregulated by testosterone, whereas genes that were female-biased or downregulated as males matured tended to be downregulated by testosterone. Moreover, the first two principal components describing multivariate gene expression indicated that exogenous testosterone reversed many of the feminizing effects of castration on the liver transcriptome of maturing males. Collectively, our results suggest that developmental changes that occur in males contribute disproportionately to the emergence of sex-biased gene expression in the Anolis liver, and that many of these changes are orchestrated by androgens such as testosterone.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript
- Journal Article:
- https://doi.org/10.1093/gbe/evaf068
