Drosophila biology in the genomic age

Over the course of the past century, flies in the family Drosophilidae have been important models for understanding genetic, developmental, cellular, ecological, and evolutionary processes. Full genome sequences from a total of 12 species promise to extend this work by facilitating comparative studies of gene expression, of molecules such as proteins, of developmental mechanisms, and of ecological adaptation. Here we review basic biological and ecological information of the species whose genomes have recently been completely sequenced in the context of current research.     

Proteomic analysis of Drosophila mojavensis male accessory glands suggests novel classes of seminal fluid proteins

Fruit-flies of the genus Drosophila are characterized by overwhelming variation in fertilization traits such as copulatory plug formation, sperm storage organ use, and nutritional ejaculatory donation. Despite extensive research on the genetic model Drosophila melanogaster, little is known about the molecular underpinnings of these interspecific differences. This study employs a proteomic approach to pin-point candidate seminal fluid proteins in Drosophila mojavensis, a cactophilic fruit-fly that exhibits divergent reproductive biology when compared to D. melanogaster. We identify several classes of candidate seminal fluid proteins not previously documented in the D. melanogaster male ejaculate, including metabolic enzymes, nutrient transport proteins, and clotting factors. Conversely, we also define 29 SFPs that are conserved despite >40 million years of Drosophila evolution. We discuss our results in terms of universal processes in insect reproduction, as well as the specialized reproductive biology of D. mojavensis.     

Density dynamics of diverse Spiroplasma strains naturally infecting different species of Drosophila

Facultative heritable bacterial endosymbionts can have dramatic effects on their hosts, ranging from mutualistic to parasitic. Within-host bacterial endosymbiont density plays a critical role in maintenance of a symbiotic relationship, as it can affect levels of vertical transmission and expression of phenotypic effects, both of which influence the infection prevalence in host populations. Species of genus Drosophila are infected with Spiroplasma, whose characterized phenotypic effects range from that of a male-killing reproductive parasite to beneficial defensive endosymbiont. For many strains of Spiroplasma infecting at least 17 species of Drosophila, however, the phenotypic effects are obscure. The infection prevalence of these Spiroplasma vary within and among Drosophila species, and little is known about the within-host density dynamics of these diverse strains. To characterize the patterns of Spiroplasma density variation among Drosophila we used quantitative PCR to assess bacterial titer at various life stages of three species of Drosophila naturally-infected with two different types of Spiroplasma. For naturally infected Drosophila species we found that non-male-killing infections had consistently lower densities than the male-killing infection. The patterns of Spiroplasma titer change during aging varied among Drosophila species infected with different Spiroplasma strains. Bacterial density varied within and among populations of Drosophila, with individuals from the population with the highest prevalence of infection having the highest density. This density variation underscores the complex interaction of Spiroplasma strain and host genetic background in determining endosymbiont density.     

Functional genomics of cactus host shifts in Drosophila mojavensis

Understanding the genetic basis of adaptation to novel environments remains one of the major challenges confronting evolutionary biologists. While newly developed genomic approaches hold considerable promise for addressing this overall question, the relevant tools have not often been available in the most ecologically interesting organisms. Our study organism, Drosophila mojavensis, is a cactophilic Sonoran Desert endemic utilizing four different cactus hosts across its geographical range. Its well-known ecology makes it an attractive system in which to study the evolution of gene expression during adaptation. As a cactophile, D. mojavensis oviposits in the necrotic tissues of cacti, therefore exposing larvae and even adults to the varied and toxic compounds of rotting cacti. We have developed a cDNA microarray of D. mojavensis to examine gene expression associated with cactus host use. Using a population from the Baja California population we examined gene expression differences of third instar larvae when reared in two chemically distinct cactus hosts, agria (Stenocereus gummosus, native host) vs. organpipe (Stenocereus thurberi, alternative host). We have observed differential gene expression associated with cactus host use in genes involved in metabolism and detoxification.     

Diversity-enhancing selection acts on a female reproductive protease family in four subspecies of Drosophila mojavensis

Protein components of the Drosophila male ejaculate are critical modulators of reproductive success, several of which are known to evolve rapidly. Recent evidence of adaptive evolution in female reproductive tract proteins suggests this pattern may reflect sexual selection at the molecular level. Here we explore the evolutionary dynamics of a five-paralog gene family of female reproductive proteases within geographically isolated subspecies of Drosophila mojavensis. Remarkably, four of five paralogs show exceptionally low differentiation between subspecies and unusually structured haplotypes that suggest the retention of old polymorphisms. These gene genealogies are accompanied by deviations from neutrality consistent with diversifying selection. While diversifying selection has been observed among the reproductive molecules of mammals and marine invertebrates, our study provides the first evidence of this selective regime in any Drosophila reproductive protein, male or female.