Molecular basis of life-history evolution: a tale of two insects

The field of life-history evolution is aimed at understanding the diversity of fertility and longevity patterns observed in nature. These patterns are influenced by the interplay of traits that directly affect the fitness of individuals, including age at first reproduction, growth rate, age-specific fecundity, and age-specific survival. Variation in life-history strategies occurs because of phylogenetic constraints on organisms, influence of extrinsic factors on mortality (i.e. predation), and tradeoffs in energy allocation between competing physiological processes. Differences in life-history strategies have been well documented at the phenotypic level but their causal genetic mechanisms remain largely unknown. At the genetic level, tradeoffs between lifespan and reproduction have been hypothesized to arise because the force of natural selection decreases with advancing age and favors pleiotropic alleles that have beneficial effects on reproduction early in life even at the cost of survival later in life. Experimental evolution studies in Drosophila have highlighted the existence of tradeoffs between lifespan and reproduction that seem to be consistent with the concept of antagonistic pleiotropy. Selection for increased age at first reproduction, as well as selection for lifespan led to increases in lifespan and reduced early life fecundity in these flies. The underlying physiological cause of tradeoffs has been difficult to study because of the diversity of processes that influence life-history traits. Given that increases in lifespan have widespread influence on reproductive output, molecular geneticists interested in aging have documented survival costs of reproduction in long-lived individuals. Mutations in signaling pathways that couple environmental signals to key physiological processes affect growth, reproduction and lifespan. These studies have provided molecular mechanisms that are excellent candidates for regulating life history traits. However, whether natural variation in any of these genes is important in life history evolution remains an open question. My dissertation research focused on understanding differences in life histories in one eusocial and one non-social insect. Eusocial insects are good candidates to study mechanisms of tradeoffs between fecundity and survival. Eusocial insect queens enjoy a long lifespan that does not come at the cost of reduced fecundity, whereas workers are usually short lived and non-reproductive. Both queens and workers can potentially develop from larvae with identical genotypes but yet show strikingly different phenotypes as adults. My work on honey bee aging established the importance of intrinsic physiological factors in regulating differences in lifespan between queen and worker bees, and provided a potential mechanism for such differences. For the second part of my dissertation, I generated fruit fly strains with divergent life-histories to study the molecular underpinnings of life-history evolution. These studies were designed to investigate how phenotypic tradeoffs are regulated at the molecular level. I used a candidate gene approach to evaluate the role of insulin signaling in differential survival and reproduction. Results from this study do not support the involvement of genes in this pathway in life history divergence. A genome-wide screen was also employed to evaluate if other genes were involved in regulating the tradeoff between reproduction and lifespan in my fly strains. Genes involved in nutrient reservoir activity, stress response, and detoxification were differentially expressed between strains. This suggests that life history divergence in my fly lines was possible through differential energy allocation to competing processes (i.e. somatic maintenance vs. reproduction). Understanding variation among organisms in patterns of longevity and reproduction is a key goal of evolutionary biology. Research on the molecular mechanisms that regulate the evolution of life history traits will allow us to link the genetic architecture of these traits to the ecological factors that shape them and this will ultimately help us understand how organisms adapt to their environment. The study of the mechanistic basis of tradeoffs between lifespan and reproduction is also fundamental given the relationship between aging and other life-history traits

lifeMatedLong

Lifespan data for mated females and males. Population Treatment is indicated by variable 'Line' (S or C), 'dead' is number dead at that census, censor is censoring variable, day is the age of flies at that census. Population replicate is indicated by variable 'set' (1,2,3)

Fecundity

Fecundity data. Line column gives Treatment (Selection, S, or Control, C) populations. Set is the population replicate (1,2,3). Column 'offspring' gives total number of offspring produced at a given age in a given vial. Column 'alivefem' is the number of females that contributed offspring to the vial. Column 'fec' is the total number of offspring divided by the number of alive females

life50Long

Lifespan data for virgin males and females. Selection and Control populations are indicated in column 'Line' (S, C). Population replicate is indicated by column 'replicate' (1,2,3). The x,y columns were used only for plotting

Evolution and mechanisms of long life and high fertility in queen honey bees

Honey bees (Apis mellifera) are eusocial insects that exhibit striking caste-specific differences in longevity. Queen honey bees live on average 1–2 years whereas workers live on average 15–38 days in the summer and 150–200 days in the winter. Previous studies of senescence in the honey bee have focused on establishing the importance of extrinsic mortality factors (predation, weather) and behavior (nursing and foraging) in worker bee longevity. However, few studies have tried to elucidate the mechanisms that allow queen honey bees to achieve their long lifespan without sacrificing fecundity. Here, we review both types of studies and emphasize the importance of understanding both proximate and ultimate causes of the unusual life history of honey bee queens