Life-History Evolution and the Genetics of Fitness Components in Drosophila melanogaster

Abstract

Life-history traits or "fitness components"-such as age and size at maturity, fecundity and fertility, age-specific rates of survival, and life span-are the major phenotypic determinants of Darwinian fitness. Analyzing the evolution and genetics of these phenotypic targets of selection is central to our understanding of adaptation. Due to its simple and rapid life cycle, cosmopolitan distribution, ease of maintenance in the laboratory, well-understood evolutionary genetics, and its versatile genetic toolbox, the "vinegar fly" Drosophila melanogaster is one of the most powerful, experimentally tractable model systems for studying "life-history evolution." Here, I review what has been learned about the evolution and genetics of life-history variation in D. melanogaster by drawing on numerous sources spanning population and quantitative genetics, genomics, experimental evolution, evolutionary ecology, and physiology. This body of work has contributed greatly to our knowledge of several fundamental problems in evolutionary biology, including the amount and maintenance of genetic variation, the evolution of body size, clines and climate adaptation, the evolution of senescence, phenotypic plasticity, the nature of life-history trade-offs, and so forth. While major progress has been made, important facets of these and other questions remain open, and the D. melanogaster system will undoubtedly continue to deliver key insights into central issues of life-history evolution and the genetics of adaptation.

Keywords: FlyBook; adaptation; fitness; fitness components; life-history evolution; plasticity; selection; trade-offs; variation.

Figure 1

The vinegar fly (D. melanogaster), here depicted sitting on a ripe banana in a kitchen, is a human commensal (Lachaise et al. 1988; Keller 2007; Markow 2015; Mansourian et al. 2018) and represents the probably most intensely studied model organism, having first been bred in the laboratory in the early 1900s (Kohler 1994; Mohr 2018). As reviewed here, this holometabolous insect has been widely used in studies of life-history evolution, genetics of fitness components, correlated responses to selection and trade-offs, and the evolution of aging. Figure credit: Chloé Schmidt (University of Manitoba).

Figure 2

The preadult life cycle of D. melanogaster. At 25° the developmental cycle, from the fertilized egg to the adult fly (imago), proceeds through three larval instar stages and one pupal stage, and takes ∼10 days. For a depiction of the adult part of the life cycle see Figure 3. See main text for further details. Figure credit: Chloé Schmidt (University of Manitoba).

Figure 3

The adult life history of D. melanogaster. The figure gives (very approximate) timelines for the major life-history events and stages, including reproductive maturation, reproductive activity, and the overall life span of female and male flies. The durations of the different events and phases are mainly based on values obtained under optimal, protected laboratory conditions; however, estimates can vary widely among studies (i.e., depending on laboratory conditions, populations and strains assayed, etc.) and might therefore not be representative of the situation in the wild. See main text for further details; see Figure 2 for a depiction of the preadult life cycle. Figure credit: Chloé Schmidt (University of Manitoba).

Figure 4

Latitudinal life-history clines in D. melanogaster. On multiple continents and subcontinents, spanning temperate to subtropical/tropical regions, fly populations exhibit major differences in fitness components across latitudes. For example, in the northern hemisphere there exists a well-established latitudinal cline for body size along the North American east coast, with flies being larger in temperate populations (e.g., Maine) but smaller in subtropical/tropical areas (e.g., Florida). This pattern is matched, in an upside-down manner, in the southern hemisphere, for example along the Australian east coast. Such parallel clines exist for several fitness-related traits and imply that these clines are (at least partly) shaped by spatially varying selection. For example, high-latitude flies are typically not only larger but also less fecund, more stress-resistant, and longer-lived than flies from subtropical/tropical locales. See main text for further details; also see Figure 6. Figure credit: Chloé Schmidt (University of Manitoba).

Figure 5

Adult reproductive dormancy in D. melanogaster. In response to cool temperatures and short day lengths, some populations of vinegar flies can undergo a plastic, reversible state of adult reproductive dormancy (often referred to as reproductive diapause). This syndrome is associated with ovarian arrest in females (causing small, nonvitellogenic ovaries, as illustrated in the figure) or arrested spermatogenesis in males, increased levels of stress resistance, and greatly improved adult survival. See main text for further details. Figure credit: Chloé Schmidt (University of Manitoba).

Figure 6

An example of a naturally segregating life-history polymorphism in D. melanogaster. (A) A polytene third chromosome of a fly heterozygous for the In(3R)Payne inversion polymorphism, i.e., the fly carries one normal noninverted third chromosome (standard arrangement) and one homologous chromosome with the inverted arrangement. In the region spanned by the inversion, the inverted and standard arrangements have paired by forming a loop structure (inversion loop). (B) Around the world, the In(3R)Payne inversion polymorphism is typically at intermediate frequency in warm climates but decreases in frequency toward temperate regions. Experiments show that the inversion confers small body size, decreased stress resistance, and shorter life span, while flies carrying the standard arrangement are characterized by the opposite phenotypes. This balanced polymorphism makes a major contribution to the well-known clines for these fitness components. Because the inversion affects several quantitative fitness-related traits that are likely to be affected by multiple loci inside the inversion, this polymorphism has been hypothesized to represent a life-history “supergene.” Also see Figure 4. Figure credit: Chloé Schmidt (University of Manitoba).