Density-by-diet interactions during larval development shape adult life-history trait expression and fitness in a polyphagous fly

Habitat quality early in life determines individual fitness, with possible long-term evolutionary effects on groups and populations. In holometabolous insects, larval ecology plays a major role in determining the expression of traits in adulthood, but how ecological conditions during larval stage interact to shape adult life-history and fitness, particularly in non-model organisms, remains subject to scrutiny. Consequently, our knowledge of the interactive effects of ecological factors on insect development is limited. Here, using the polyphagous fly Bactrocera tryoni, we conducted a fully-factorial design where we manipulated larval density and larval diet (protein-rich, standard, and sugar-rich) to gain insights into how these ecological factors interact to modulate adult fitness. As expected, a protein-rich diet resulted in faster larval development, heavier and leaner adults that were more fecund compared with standard and sugar-rich diets, irrespective of larval density. Females from the protein-rich larval diet had overall higher reproductive rate (i.e., eggs per day) than females from other diets, and reproductive rate decreased linearly with density for females from the protein-rich but non-linearly for females from the standard and sugar-rich diets over time. Surprisingly, adult lipid reserve increased with larval density for adults from the sugar-rich diet (as opposed to decreasing, as in other diets), possibly due to a stress-response to an extremely adverse condition during development (i.e., high intraspecific competition and poor nutrition). Together, our results provide insights into how ecological factors early in life interact and shape the fate of individuals through life-stages in holometabolous insects.

生命早期的生境质量决定个体适合度（fitness），且可能对类群与种群产生深远的进化效应。在全变态昆虫（holometabolous insects）中，幼虫生态学对成虫性状的表达起着关键调控作用，但幼虫期的多种生态条件如何交互作用以塑造成虫生活史与适合度，尤其是在非模式生物中，这一问题仍有待学界深入探究。因此，学界对生态因子交互作用如何影响昆虫发育的认知仍较为有限。本研究以多食性蝇类昆士兰果实蝇（Bactrocera tryoni）为实验对象，采用全因子实验设计，通过操控幼虫密度与幼虫日粮类型（高蛋白型、标准型、高糖型），探究这两类生态因子的交互作用如何调控成虫适合度。正如预期，无论幼虫密度如何，高蛋白日粮组的幼虫发育速度更快，羽化后的成虫体重更高且体脂更低，繁殖力也较标准日粮组与高糖日粮组更强。幼虫期取食高蛋白日粮的雌成虫整体繁殖速率（即日产卵量）显著高于其他日粮组的雌成虫；且随时间推移，高蛋白日粮组雌成虫的繁殖速率随幼虫密度升高呈线性下降，而标准日粮组与高糖日粮组雌成虫的繁殖速率则呈非线性下降。令人意外的是，高糖日粮组成虫的体内脂质储备随幼虫密度升高而增加（与其他日粮组的下降趋势相反），这可能是昆虫在发育过程中应对极端不利条件（即高种内竞争与营养匮乏）的应激响应所致。综上，本研究结果揭示了全变态昆虫生命早期的生态因子如何通过各发育阶段的交互作用，进而塑造个体的生活史轨迹。