Development time mediates the effect of larval diet on ageing and mating success of male antler flies in the wild

Abstract

High-quality developmental environments often improve individual performance into adulthood, but allocating toward early life traits, such as growth, development rate and reproduction, may lead to trade-offs with late-life performance. It is, therefore, uncertain how a rich developmental environment will affect the ageing process (senescence), particularly in wild insects. To investigate the effects of early life environmental quality on insect life-history traits, including senescence, we reared larval antler flies ( Protopiophila litigata ) on four diets of varying nutrient concentration, then recorded survival and mating success of adult males released in the wild. Declining diet quality was associated with slower development, but had no effect on other life-history traits once development time was accounted for. Fast-developing males were larger and lived longer, but experienced more rapid senescence in survival and lower average mating rate compared to slow developers. Ultimately, larval diet, development time and body size did not predict lifetime mating success. Thus, a rich environment led to a mixture of apparent benefits and costs, mediated by development time. Our results indicate that ‘silver spoon' effects can be complex and that development time mediates the response of adult life-history traits to early life environmental quality.

Larval nutrition impacts survival to adulthood, body size and the allometric scaling of metabolic rate in adult honeybees

“…Bees reared on the high carbohydrate diet, the best for survival, also took significantly longer to emerge as adults compared with bees in all other diet groups. This contrasts with previous studies in insects which have typically observed slower development on lower quality diets (Angell et al, 2020;Johnson et al, 1992).…”

Larval nutrition impacts survival to adulthood, body size, and the allometric scaling of metabolic rate in adult honeybees

“…Bees reared on the high carbohydrate diet, the best for survival, also took significantly longer to emerge as adults compared to bees in all other diet groups. This contrasts with previous studies in insects which have typically observed slower development on lower quality diets (Johnson, Wofford and Whitehand, 1992; Angell et al ., 2020). For example, Rodrigues et al .…”

“Born with a silver spoon in the mouth has bad sides too”: Experimentally increasing growth rate enhances individual quality but accelerates reproductive senescence in females of the mealworm beetle, Tenebrio molitor

“…Indeed, considering the fact that females reared at 85% RH during their larval stages were also those that lived the longest, were the largest, and laid more eggs (see below), they may benefit from a "silver spoon" effect, where individuals born in good conditions have fitness advantages later in life (Grafen, 1988;Lindström, 1999;Monaghan, 2008). Such an effect has already been observed-not consistent with all life-history traits, howeverin an experimental study manipulating larval diet in an insect (Angell et al, 2020). Alternatively, high environmental relative humidity may represent cues for a harsher environment, The reproductive senescence was estimated as the ratio of the difference between the two reproductive episodes (early and late) over the total of eggs laid during both reproductive episodes.…”

“…However, the incomplete knowledge of the environmental conditions experienced early in life by the two ecotypes and the fact that snakes are growing continuously may have prevented the evidence of such a trade-off. In another study, the growth rate of males of the antler fly, Protopiophila litigata, was altered by the experimental manipulation of the larval diet, generating variation in development time, which was positively correlated with lifetime mating rate but not with reproductive senescence (Angell et al, 2020). As a result, more research is needed into the early-late trade-off between growth rate and early reproductive success, as well as their respective impacts on late-life reproductive success and senescence.…”

“…Nevertheless, this approach may have several drawbacks when confronted with the phenomenon 10.3389/fevo.2022.915054 of compensatory growth after periods of starvation (e.g., Metcalfe and Monaghan, 2003;Kecko et al, 2017;Ziegelbecker and Sefc, 2021), or when aging does not depend on early diet (Zajitschek et al, 2009), leading to contradictory or inconclusive results. Moreover, increasing growth rate by setting highly favorable conditions may generate individuals with a higher fitness, called the "silver spoon" effect (Grafen, 1988;Lindström, 1999;Monaghan, 2008), which may prevent detection of senescence (Angell et al, 2020). There is therefore a need to explore further the early-late trade-off between growth rate and reproductive senescence using experimental approaches a priori avoiding resource alteration during growth to manipulate growth rate.…”