skip to main content
US FlagAn official website of the United States government
dot gov icon
Official websites use .gov
A .gov website belongs to an official government organization in the United States.
https lock icon
Secure .gov websites use HTTPS
A lock ( lock ) or https:// means you've safely connected to the .gov website. Share sensitive information only on official, secure websites.


Title: Sex-specific plasticity and the nutritional geometry of insulin-signaling gene expression in Drosophila melanogaster
Abstract BackgroundSexual-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 inD. melanogasterreflects 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. ResultsThe IIS-regulated transcripts of4E-BPandInRmost 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 ofdILP5positively correlated with body size, while expression ofdILP2,3and8,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 ondILPexpression in males. ConclusionAlthough 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,dILPexpression 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
Award ID(s):
1952385
PAR ID:
10228256
Author(s) / Creator(s):
; ; ; ;
Publisher / Repository:
Springer Science + Business Media
Date Published:
Journal Name:
EvoDevo
Volume:
12
Issue:
1
ISSN:
2041-9139
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Despite widespread variation in life span across species, three clear patterns exist: sex differences in life span are ubiquitous, life span is commonly traded against reproduction, and nutrition has a major influence on these traits and how they trade‐off. One process that potentially unites these patterns is intralocus sexual conflict over the optimal intake of nutrients for life span and reproduction. If nutrient intake has sex‐specific effects on life span and reproduction but nutrient choice is genetically linked across the sexes, intralocus sexual conflict will occur and may prevent one or both sexes from feeding to their nutritional optima.Here we determine the potential for this process to operate in the decorated cricketGryllodes sigillatus. Using the Geometric Framework for Nutrition, we restrict male and female crickets to diets varying in the ratio of protein to carbohydrates and total nutrient content to quantify the effects on life span and daily reproductive effort in the sexes. We then use inbred lines to estimate the quantitative genetic basis of nutrient choice in males and females. We combine the nutrient effects and genetic estimates to predict the magnitude of evolutionary constraint for these traits in each sex. Finally, we present male and female crickets with a much broader range of diet pairs to determine how the sexes actively regulate their intake of nutrients.We show that protein and carbohydrate intake have contrasting effects on life span and reproduction in the sexes and that there are strong positive intersexual genetic correlations for the intake of these nutrients under dietary choice. This is predicted to accelerate the evolutionary response of nutrient intake in males but constrain it in females, suggesting they are losing the conflict. Supporting this view, males and females regulate nutrient intake to a common nutrient ratio that was not perfectly optimal for life span or reproduction in either sex, especially in females.Our findings show that intralocus sexual conflict over the optimal intake of nutrients is likely to be an important process generating sex differences in life span and reproduction and may help explain why females age faster and live shorter than males inG. sigillatus. A freePlain Language Summarycan be found within the Supporting Information of this article. 
    more » « less
  2. null (Ed.)
    Abstract Orangutans show a pronounced sexual dimorphism, with flanged males (i.e., males with fully grown secondary sexual characteristics) reaching twice the size of adult females. Furthermore, adult orangutans show sex-specific dispersal and activity patterns. This study investigates sex differences in adult foraging behavior and sheds light on how these differences develop in immatures. We analyzed 11 years of feeding data on ten adult female, seven flanged male, and 14 immature Bornean orangutans ( Pongo pygmaeus wurmbii ) at Tuanan in Central Kalimantan, Indonesia. We found that the diets of the adult females were significantly broader and required more processing steps before ingestion than the diets of flanged males. We also found evidence for a similar difference in overall diet repertoire sizes. For the immatures, we found that whereas females reached 100% of their mothers’ diet spectrum size by the age of weaning, males reached only around 80%. From the age of 4 years on (i.e., years before being weaned) females had significantly broader daily diets than males. We found no difference in daily or overall diet processing intensity of immature males and females but found preliminary evidence that immature males included fewer items of their mother’s diet in their own diets that were processing-intensive. Overall, our results suggest that by eating a broader variety and more complex to process food items, female orangutans go to greater lengths to achieve a balanced diet than males do. These behavioral differences are not just apparent in adult foraging behavior but also reflected in immature development from an early age on. Significance Statement In many species, males and females have different nutritional needs and are thus expected to show sex-specific foraging behavior. Sex differences in several aspects of foraging behavior have been found in various species, but it remains largely unclear when and how those develop during ontogeny, which is especially relevant for long-lived altricial species that learn foraging skills over many years. In our study, we analyzed a cross-sectional and longitudinal data set containing more than 750,000 feeding events of adult and immature Bornean orangutans ( Pongo pygmaeus wurmbii ). We found that adult females had significantly broader and more complex diets than males. We also found that these differences started to develop during infancy, suggesting that immature orangutans prepare for their sex-specific foraging niches long before those become physiologically relevant while they are still in constant association with their mothers and before being frequently exposed to other role models. 
    more » « less
  3. In holometabolous insects, larval nutrition affects adult body size, a life history trait with a profound influence on performance and fitness. Individual nutritional components of larval diets are often complex and may interact with one another, necessitating the use of a geometric framework for elucidating nutritional effects. In the honey bee, Apis mellifera, nurse bees provision food to developing larvae, directly moderating growth rates and caste development. However, the eusocial nature of honey bees makes nutritional studies challenging, because diet components cannot be systematically manipulated in the hive. Using in vitro rearing, we investigated the roles and interactions between carbohydrate and protein content on larval survival, growth, and development in A. mellifera. We applied a geometric framework to determine how these two nutritional components interact across nine artificial diets. Honey bees successfully completed larval development under a wide range of protein and carbohydrate contents, with the medium protein (∼5%) diet having the highest survival. Protein and carbohydrate both had significant and non-linear effects on growth rate, with the highest growth rates observed on a medium-protein, low-carbohydrate diet. Diet composition did not have a statistically significant effect on development time. These results confirm previous findings that protein and carbohydrate content affect the growth of A. mellifera larvae. However, this study identified an interaction between carbohydrate and protein content that indicates a low-protein, high-carb diet has a negative effect on larval growth and survival. These results imply that worker recruitment in the hive would decline under low protein conditions, even when nectar abundance or honey stores are sufficient. 
    more » « less
  4. ABSTRACT Male alternative reproductive tactics are taxonomically widespread, with many species showing males with distinctly different phenotypic characters such as body size or weaponry. Several mechanisms can drive the expression of these male morphs, including genetic polymorphism or environmental interactions during development. In insects, multiple male morphs are common in several orders, including Coleoptera, Odonata, and Hymenoptera, but are rare in Orthoptera. This study establishes the presence of two male phenotypic morphs in the bush cricketSatizabalus jorgevargasi, a species in which the males display mandibular weaponry, and tests the effects of diet on the expression of male dimorphic characters. Male nymphs were raised under standard conditions until adulthood, whereupon morphological measurements were taken. Males raised under standard conditions showed two male phenotypes on the basis of head size and body colouration—a major morph with larger heads and more colouration, and a smaller and duller minor morph. A second group of male nymphs were housed individually and fed either a high‐protein diet or a high‐carbohydrate diet. Body weight and pronotum length were measured on a weekly basis as the nymphs developed, and once the males had matured, morphological and bioacoustic characters were measured. Diet had a significant impact on these male dimorphic characters, with protein‐fed males having significantly larger heads and mandibles. Additionally, males reared on the high‐protein diet had significantly more regions with colour when compared to carbohydrate‐fed males. Our data parallel that seen in other invertebrate groups, where higher levels of protein during maturation are key to the production of larger male morphs. 
    more » « less
  5. Our lab previously established that repeated exposure to a bitter diet can increase salivary protein (SP) expression, which corresponds to an increase in acceptance of the bitter stimulus. However, this work was exclusively in male rodents, here we examine sex differences. We found that there are no differences in SP expression (experiment 1) or quinine diet acceptance (experiment 2) across stage of estrous cycle. Yet, males and females differ in feeding behaviors, SP expression, and responses to a quinine diet (experiment 3). On a quinine diet, males accepted the diet much faster than females. Males displayed a compensatory increase in meal number as meal size and rate of feeding decreased with initial exposure to a quinine diet, whereas females decreased meal size and rate of feeding with no compensation in meal number. There were sex differences in SP expression at day 14 of quinine exposure but these were gone by day 24. Both sexes increased acceptance of quinine in a brief access taste test after the feeding trial concluded. These data suggest that males and females have different patterns of bitter diet acceptance, but extended exposure to quinine diet still results in altered bitter taste responding and changes in SP profiles in females. 
    more » « less