Dietary choice for a balanced nutrient intake increases the mean and reduces the variance in the reproductive performance of male and female cockroaches

Abstract

Sexual selection may cause dietary requirements for reproduction to diverge across the sexes and promote the evolution of different foraging strategies in males and females. However, our understanding of how the sexes regulate their nutrition and the effects that this has on sex-specific fitness is limited. We quantified how protein (P) and carbohydrate (C) intakes affect reproductive traits in male (pheromone expression) and female (clutch size and gestation time) cockroaches (Nauphoeta cinerea). We then determined how the sexes regulate their intake of nutrients when restricted to a single diet and when given dietary choice and how this affected expression of these important reproductive traits. Pheromone levels that improve male attractiveness, female clutch size and gestation time all peaked at a high daily intake of P:C in a 1:8 ratio. This is surprising because female insects typically require more P than males to maximize reproduction. The relatively low P requirement of females may reflect the action of cockroach endosymbionts that help recycle stored nitrogen for protein synthesis. When constrained to a single diet, both sexes prioritized regulating their daily intake of P over C, although this prioritization was stronger in females than males. When given the choice between diets, both sexes actively regulated their intake of nutrients at a 1:4.8 P:C ratio. The P:C ratio did not overlap exactly with the intake of nutrients that optimized reproductive trait expression. Despite this, cockroaches of both sexes that were given dietary choice generally improved the mean and reduced the variance in all reproductive traits we measured relative to animals fed a single diet from the diet choice pair. This pattern was not as strong when compared to the single best diet in our geometric array, suggesting that the relationship between nutrient balancing and reproduction is complex in this species.

Keywords: Geometric framework of nutrition; optimal foraging; pheromones; sexual selection.

Figure 1

Nutritional landscapes illustrating the effects of daily protein (P) and carbohydrate (C) intake on the expression of the three male sex pheromones, (A) 3H2B, (B) 2MT, and (C) 4E2M, and (D) clutch size and (E) gestation time in females. High values of these reproductive traits are given in red and low values in blue. Black dots represent the intake of these nutrients by individual cockroaches. The blue crosses (yellow in the case of gestation time) on each landscape represent the mean (±SE) intake of nutrients in each of the diet pairs, with the number corresponding to the specific diet pair. The white crosses on each landscape represent the regulated intake point (±SE), calculated as the mean daily intake of P and C across diet pairs.

Figure 2

The mean (±SE) daily protein (P) and carbohydrate (C) intake for the male (open circles) and female (closed circles) cockroaches fed ad libitum amounts of diets along the six nutritional rails (dashed lines). The solid lines connecting the mean nutrient intake across rails for each sex create an intake array, the slope of which indicates the degree to which individuals prioritize their intake of nutrients when constrained to a single, nutritionally imbalanced diet.

Figure 3

The mean (±SE) daily protein (P) and carbohydrate (C) intake for male (open symbols) and female (closed symbols) N. cinerea on each of the four diet pairs (indicated by numbers). The regulated intake point is also provided for males (open red square) and females (closed red square). The black dashed lines represent the nutritional rails that the alternate diets in each diet pair originate from and cockroaches can, in theory, regulate their intake of nutrients to any location within these rails. The total region in nutrient space that males (red, dashed) and females (red, solid) occupy through active dietary choice is also provided.

Figure 4

Mean (±SE) expression of the three male sex pheromones [(A) 3H2B, (C) 2MT, and (E) 4E2M], as well as female (G) clutch size and (I) gestation time in N. cinerea fed one the four alternate diet pairs. Diet pairs with different letters (above the bars) differ significantly in post hoc analysis. The mean (±SE) difference in (B) 3H2B, (D) 2MT, (F) 4E2M, (H) clutch size, and (J) gestation time when individuals are able to actively choose between diets and when they consume each diet in the pair exclusively (i.e., without choice), where the white bars represent the high protein diet in the pair (either diet 2 or 4, Table S1) and the gray bars represent the high carbohydrate diets in the pair (either diet 22 or 24, Table S1). Significance of these differences from a mean of zero (as determined by a one‐sample t‐test) is provided by asterisks, where *P < 0.05, **P < 0.01, and ***P < 0.0001. Percentage increases or decreases from the mean when consuming only a single diet in the pair is added above each bar.