Plasticity of Senescence in the Antler Fly (Protopiophila litigata)
Creators: name: Angell, Christopher
Publisher: name: Université d'Ottawa / University of Ottawa
Year: 2021
Subjects: subject: Senescence
subject: Evolution
subject: Ecology
subject: FOS: Biological sciences
subject: FOS: Biological sciences
subject: Entomology
subject: Life-history
subject: Ageing

description: As most multicellular organisms age, they undergo senescence: a progressive physiological deterioration that leads to declines in survival, reproduction, and performance in late life. Although senescence was once thought to be a phenomenon peculiar to captive animals and humans, field data have demonstrated age-related performance declines in a variety of taxa. Nevertheless, the ecology and evolution of senescence is not fully understood. The bulk of our knowledge about senescence in wild populations comes from studies of long-lived vertebrates, while short-lived invertebrates are often studied in the lab. Male antler flies (Protopiophila litigata; Diptera: Piophilidae) are an emerging insect model for studying senescence in nature, as they have short lifespans and high site-fidelity, facilitating collection of longitudinal data, and they can be easily reared and manipulated in the lab. This species is an ideal model to connect our lab-invertebrate- and field-vertebrate-based insights into aging biology. The developmental environment can have an especially large impact on life-history plasticity, including plasticity in senescence. This is because a developing organism makes “decisions” affecting phenotypes such as body size, sexual investment, metabolic rate, etc., which in turn can influence longevity and senescence. In my dissertation, I investigate how the early life environment, including larval diet and parental effects, plastically alters longevity and senescence in antler flies, primarily in the field in Algonquin Provincial Park. First, I quantified the effect of experimentally manipulated larval nutrient concentration on both early-life (growth and development) and late-life traits (reproduction, survival, senescence). Rich larval diet decreased development time, and although fast developers grew large and had low initial mortality in the field (and high average lifespan), they aged rapidly and had low mating rate. Due to these contrasting effects, diet and development time did not predict lifetime mating success, suggesting trade-offs among fitness components and alternative strategies in low condition males. Only male antler flies can be tracked in the field, so nothing is known about aging in females. In my second study, I compared longevity and aging of female and male antler flies in the lab. Theory suggests that males may age faster and die sooner than females, but empirical data are highly variable. Furthermore, the sexes may respond differently to variation in nutrition, so I reared flies on different larval diets based on the design of my first chapter. The sexes did not differ in senescence or longevity in the lab, and diet had a negligible effect. Large-bodied flies of both sexes senesced slower, in contrast to previous field data, highlighting plastic differences in senescence between wild and captive populations. In my third study, I quantified parental age effects on male antler flies. Offspring quality often changes with parental age, due to accumulation of germline mutations and/or changes in nongenetic maternal or paternal effects. To investigate whether and how parental age influences performance in wild insects, I mated lab-reared young and old females and males to one another in all combinations, and tracked their male offspring’s performance in the wild. Old fathers had long-lived sons, while maternal age had no effect on offspring survival in the field. Parental age did not affect mating success. Thus, the one parental age effect I observed was in fact positive, not negative. In my final study, I looked at how natural differences in larval diet, rather than artificial lab diets, influenced survival, mating, and senescence in wild male antler flies. Antlers become depleted of resources from year to year, as multiple generations of larvae feed within them. I collected larvae that grew inside nine different shed moose antlers, and tracked them in the field as adults. Males from high quality antlers (those that were more attractive to adult flies) completed metamorphosis more quickly, but did not differ in body size, longevity or lifetime mating success. However, large flies tended to live longer and have higher mating success. In conclusion, my dissertation research expands our understanding of plasticity in life history and senescence, particularly in insects, which are enormously abundant but understudied in this area. I quantified, for the first time to my knowledge, the effects of juvenile diet and parental age on longevity, mating success, and senescence in a wild insect.