Physiological demands and nutrient intake modulate a trade-off between dispersal and reproduction based on age and sex of field crickets

Abstract

Animals adjust resource acquisition throughout life to meet changing physiological demands of growth, reproduction, activity and somatic maintenance. Wing-polymorphic crickets invest in either dispersal or reproduction during early adulthood, providing a system in which to determine how variation in physiological demands, determined by sex and life history strategy, impact nutritional targets, plus the consequences of nutritionally imbalanced diets across life stages. We hypothesized that high demands of biosynthesis (especially oogenesis in females) drive elevated resource acquisition requirements and confer vulnerability to imbalanced diets. Nutrient targets and allocation into key tissues associated with life history investments were determined for juvenile and adult male and female field crickets (Gryllus lineaticeps) when given a choice between two calorically equivalent but nutritionally imbalanced (protein- or carbohydrate-biased) artificial diets, or when restricted to one imbalanced diet. Flight muscle synthesis drove elevated general caloric requirements for juveniles investing in dispersal, but flight muscle quality was robust to imbalanced diets. Testes synthesis was not costly, and life history investments by males were insensitive to diet composition. In contrast, costs of ovarian synthesis drove elevated caloric and protein requirements for adult females. When constrained to a carbohydrate-biased diet, ovary synthesis was reduced in reproductive morph females, eliminating their advantage in early life fecundity over the dispersal morph. Our findings demonstrate that nutrient acquisition modulates dispersal–reproduction trade-offs in an age- and sex-specific manner. Declines in food quality will thus disproportionately affect specific cohorts, potentially driving demographic shifts and altering patterns of life history evolution.

Flight capacity drives circadian patterns of metabolic rate and alters resource dynamics

“…Although my study used a protein‐biased diet and did not monitor the allocation of specific macronutrients, its results mirror those from a recent study in G. lineaticeps that focused on macronutrient acquisition and allocation. Despite burning more calories, flight‐capable G. lineaticeps in this study ate 45% less food than flight‐incapable crickets in agreement with Treidel et al, 2021, and they were less efficient at converting ingested food into body or ovary mass (Figures 2b and 3). Therefore, conventional studies using gravimetric data can complement experiments examining the role of macronutrient composition of food in feeding behavior and allocation.…”

“…Thus, flight capacity diverts resources from body stores and reproductive tissue while also increasing energy use, which appears to leave LW(f) crickets in a very precarious energetic state. However, recent work in G. lineaticeps indicates that LW(f) crickets eat more food before adulthood relative to flight‐incapable crickets (Treidel et al, 2021). This temporal pattern of feeding may facilitate flight capacity by (1) fueling an increase in body size and features of flight morphology, including wing length and flight muscle mass, before adulthood, because such traits are fixed in size during adulthood, and (2) reducing flight load (body mass) during the dispersal phase of adulthood.…”

“…Flight‐capable crickets invest in lipogenesis to produce lipid flight fuel and allocate more to somatic stores, whereas flight‐incapable crickets conserve protein and allocate more to ovaries (reviewed in Zera, 2005). These allocation strategies are achieved through differential feeding strategies—flight‐incapable females preferentially feed on a more protein‐biased diet relative to flight‐capable females (Clark et al, 2013; Treidel et al, 2021). Feeding in house ( Acheta ) crickets largely occurs at night (Woodring & Clifford, 1986), but it is not known if flight capacity in Gryllus influences circadian patterns of resource acquisition similar to the flight‐dependent rhythmicity of energy use (Figure 1).…”

“…Throughout ontogeny, crickets were reared in standard conditions: 28 ± 1°C and 14:10 light:dark cycle with ad libitum access to water (water‐filled shell vials plugged with cotton) and shelter (cardboard egg cartons). Crickets were also supplied with ad libitum access to high‐protein (33% crude protein) commercial dry cat food pellets, because SW and LW G. lineaticeps fed a high‐protein diet exhibit the same investment into flight muscle and ovary mass as SW and LW crickets fed a diet of their choice (i.e., when offered several diets ranging in protein‐to‐carbohydrate ratios; Treidel et al, 2021). Newly molted female adults (<1 day after final ecdysis; Day 1) were weighed and individually housed in standard conditions (see above) in small translucent deli cups (473 ml) containing shelter (overturned 30 ml opaque containers with access holes) and preweighed food (pellets of dry cat food).…”

“…For example, LW(f) Gryllus are less efficient at converting digested food into body mass, potentially indicating a metabolic cost of flight capacity (Mole & Zera, 1993, 1994). Yet, LW crickets may offset greater energy use by exhibiting higher rates of food consumption, which has been shown in Gryllus firmus (Mole & Zera, 1994; but see Clark et al, 2016) and Gryllus lineaticeps (Treidel et al, 2021), but not in Gryllus rubens or Gryllus assimilis (Mole & Zera, 1993; Zera et al, 1998). Less studied is whether SW crickets exhibit greater reproductive investment because they more efficiently allocate ingested resources to ovary mass, or because they simply ingest more food thereby facilitating increased allocation to reproductive tissue.…”