Therese A. Markow

EVOLUTION OF MULTIPLE KINDS OF FEMALE SPERM-STORAGE ORGANS IN DROSOPHILA

Females of all species belonging to the family Drosophilidae have two kinds of sperm‐storage organs: paired spherical spermathecae and a single elongate tubular seminal receptacle. We examined 113 species belonging to the genus Drosophila and closely allied genera and describe variation in female sperm‐storage organ use and morphology. The macroevolutionary pattern of organ dysfunction and morphological divergence suggests that ancestrally both kinds of organs stored sperm. Loss of use of the spermathecae has evolved at least 13 times; evolutionary regain of spermathecal function has rarely if ever occurred. Loss of use of the seminal receptacle has likely occurred only once; in this case, all descendant species possess unusually elaborate spermathecae. Data further indicate that the seminal receptacle is the primary sperm‐storage organ in Drosophila. This organ exhibits a pattern of strong correlated evolution with the length of sperm. The evolution of multiple kinds of female sperm‐storage organs and the rapidly divergent and correlated evolution of sperm and female reproductive tract morphology are discussed.

Male Gametic Strategies: Sperm Size, Testes Size, and the Allocation of Ejaculate Among Successive Mates by the Sperm-Limited Fly Drosophila pachea and Its Relatives

The gametic strategy of males comprises the amount of energy invested per sperm, the total amount invested in sperm production, and the pattern of sperm allocation among successive reproductive bouts. All of these variables were measured for each of the four species constituting the nannoptera species group of the Drosophilidae. Extreme interspecific variation was identified for all variables and enigmatic male reproductive strategies, including submaximal insemination of females, partitioning of ejaculate among successive mates, and production of few large sperm, were observed. Variation among species in female remating behavior was found to occur concomitantly with male remating behavior, probably because of female fertility demands. Relationships among testes size, sperm size, sperm numbers, and mating systems in these fruit flies are examined. These relationships are not consistent with patterns identified in studies of vertebrate taxa and suggest fundamental differences between vertebrates and invertebrates with respect to these traits. Hypotheses to explain the maintenance of male ejaculate delivery patterns that are consistent with sperm competition and bet-hedging theory are examined, as are potential selection pressures responsible for sperm-size evolution.

Drosophila Males Contribute to Oogenesis in a Multiple Mating Species

Two species of Drosophila that differ in their ecology and mating systems have been compared with respect to male contribution to the somatic tissues and developing oocytes of females. In the species Drosophila mojavensis females remate daily, exhibit a copulatory plug, and have been shown to obtain a contribution from the male ejaculate. In contrast, Drosophila melanogaster males do not contribute to females. Female Drosophila melanogaster do not remate as frequently as Drosophila mojavensis females nor is a copulatory plug formed.

Polytene Chromosomal Maps of 11 Drosophila Species: The Order of Genomic Scaffolds Inferred From Genetic and Physical Maps

The sequencing of the 12 genomes of members of the genus Drosophila was taken as an opportunity to reevaluate the genetic and physical maps for 11 of the species, in part to aid in the mapping of assembled scaffolds. Here, we present an overview of the importance of cytogenetic maps to Drosophila biology and to the concepts of chromosomal evolution. Physical and genetic markers were used to anchor the genome assembly scaffolds to the polytene chromosomal maps for each species. In addition, a computational approach was used to anchor smaller scaffolds on the basis of the analysis of syntenic blocks. We present the chromosomal map data from each of the 11 sequenced non-Drosophila melanogaster species as a series of sections. Each section reviews the history of the polytene chromosome maps for each species, presents the new polytene chromosome maps, and anchors the genomic scaffolds to the cytological maps using genetic and physical markers. The mapping data agree with Mullers idea that the majority of Drosophila genes are syntenic. Despite the conservation of genes within homologous chromosome arms across species, the karyotypes of these species have changed through the fusion of chromosomal arms followed by subsequent rearrangement events.

Effects of starvation and desiccation on energy metabolism in desert and mesic Drosophila

Energy availability can limit the ability of organisms to survive under stressful conditions. In Drosophila, laboratory experiments have revealed that energy storage patterns differ between populations selected for desiccation and starvation. This suggests that flies may use different sources of energy when exposed to these stresses, but the actual substrates used have not been examined. We measured lipid, carbohydrate, and protein content in 16 Drosophila species from arid and mesic habitats. In five species, we measured the rate at which each substrate was metabolized under starvation or desiccation stress. Rates of lipid and protein metabolism were similar during starvation and desiccation, but carbohydrate metabolism was several-fold higher during desiccation. Thus, total energy consumption was lower in starved flies than desiccated ones. Cactophilic Drosophila did not have greater initial amounts of reserves than mesic species, but may have lower metabolic rates that contribute to stress resistance.

Heritable endosymbionts of Drosophila.

Although heritable microorganisms are increasingly recognized as widespread in insects, no systematic screens for such symbionts have been conducted in Drosophila species (the primary insect genetic models for studies of evolution, development, and innate immunity). Previous efforts screened relatively few Drosophila lineages, mainly for Wolbachia. We conducted an extensive survey of potentially heritable endosymbionts from any bacterial lineage via PCR screens of mature ovaries in 181 recently collected fly strains representing 35 species from 11 species groups. Due to our fly sampling methods, however, we are likely to have missed fly strains infected with sex ratio-distorting endosymbionts. Only Wolbachia and Spiroplasma, both widespread in insects, were confirmed as symbionts. These findings indicate that in contrast to some other insect groups, other heritable symbionts are uncommon in Drosophila species, possibly reflecting a robust innate immune response that eliminates many bacteria. A more extensive survey targeted these two symbiont types through diagnostic PCR in 1225 strains representing 225 species from 32 species groups. Of these, 19 species were infected by Wolbachia while only 3 species had Spiroplasma. Several new strains of Wolbachia and Spiroplasma were discovered, including ones divergent from any reported to date. The phylogenetic distribution of Wolbachia and Spiroplasma in Drosophila is discussed.

Ejaculate-female coevolution in Drosophila mojavensis

Interspecific studies indicate that sperm morphology and other ejaculatory traits diverge more rapidly than other types of character in Drosophila and other taxa. This pattern has largely been attributed to postcopulatory sexual selection involving interaction between the sexes. Such divergence has been suggested to lead rapidly to reproductive isolation among populations and thus to be an ‘engine of speciation.’ Here, we test two critical predictions of this hypothesis: (i) there is significant variation in reproductive traits among incipient species; and (ii) divergence in interacting sex–specific traits exhibits a coevolutionary pattern among populations within a species, by examining geographical variation in Drosophila mojavensis, a species in the early stages of speciation. Significant among–population variation was identified in sperm length and female sperm–storage organ length, and a strong pattern of correlated evolution between these interacting traits was observed. In addition, crosses among populations revealed coevolution of male and female contributions to egg size. Support for these two important predictions confirms that coevolving internal characters that mediate successful reproduction may play an important part in speciation. The next step is to determine exactly what that role is.

Fluctuating Dermatoglyphic Asymmetry and the Genetics of Liability to Schizophrenia

Schizophrenic subjects were compared to normal and psychiatric control subjects for degree of fluctuating asymmetry in two dermatoglyphic traits, a-b ridge count and fingertip pattern. The schizophrenic group exhibited significantly greater fluctuating asymmetry than either control group. Furthermore, indicators of disease severity such as early onset and declining course of illness correlated with degree of asymmetry. Both of these observations are expected if a disorder has a polygenic basis, since fluctuating asymmetry is a marker of polygenic inheritance.

Male size, developmental stability, and mating success in natural populations of three Drosophila species

Morphological correlates of male mating success were assessed in natural populations of three Drosophila species. Mating males in D. simulans were larger than single males but were characterized by reduced developmental stability as indicated by fluctuating asymmetry. Mating male D. pseudoobscura were no larger than single males but exhibited significantly greater developmental stability. In D. mojavensis, however, mating males were larger and they showed a similar level of fluctuating asymmetry to that observed in single males. The differences observed between species are discussed in the context of their mating systems and reproductive ecology.

Analysis of Drosophila Species Genome Size and Satellite DNA Content Reveals Significant Differences Among Strains as Well as Between Species

The size of eukaryotic genomes can vary by several orders of magnitude, yet genome size does not correlate with the number of genes nor with the size or complexity of the organism. Although “whole”-genome sequences, such as those now available for 12 Drosophila species, provide information about euchromatic DNA content, they cannot give an accurate estimate of genome sizes that include heterochromatin or repetitive DNA content. Moreover, genome sequences typically represent only one strain or isolate of a single species that does not reflect intraspecies variation. To more accurately estimate whole-genome DNA content and compare these estimates to newly assembled genomes, we used flow cytometry to measure the 2C genome values, relative to Drosophila melanogaster. We estimated genome sizes for the 12 sequenced Drosophila species as well as 91 different strains of 38 species of Drosophilidae. Significant differences in intra- and interspecific 2C genome values exist within the Drosophilidae. Furthermore, by measuring polyploid 16C ovarian follicle cell underreplication we estimated the amount of satellite DNA in each of these species. We found a strong correlation between genome size and amount of satellite underreplication. Addition and loss of heterochromatin satellite repeat elements appear to have made major contributions to the large differences in genome size observed in the Drosophilidae.