Indirect thermal selection in Drosophila melanogaster and adaptive consequences

Summary Short-term indirect selection in Drosophila melanogaster for heat-sensitivity and heat resistance resulted in two strains, one heat sensitive and another heat resistant, and correlated responses were found for the rate of heat shock protein synthesis, behavioral patterns (asymmetrical sexual isolation) and fitness components (fecundity, fertility, viability, developmental time), as well as for several enzyme activities (MDH, G-6-PDH, ADH, ACHE). These responses associated with temperature selection may reflect the effects of differential inbreeding depression caused by homozygosity of temperature sensitive mutations with different pleiotropic effects. Selection even of a very short duration can induce significant adaptive and evolutionary changes.     

Developmental consequences of mutations in the 84B alpha-tubulin gene of Drosophila melanogaster

Developmental effects of six mutations in the gene encoding the majority of alpha-tubulin in all tissues at all stages of Drosophila melanogaster development have been examined. All six alleles produce at least partially stable alpha 84B protein. In genetic assays, two of these alleles approximate the null condition. The other four alleles appear to form a graded series of hypomorphs. The two most severe alleles produce a semidominant maternal-effect polyphasic lethality, plus a predominantly larval recessive zygotic lethality. Clonal analysis of one of these alleles suggests it is a cell lethal. Worsening of the lethal phenotype (negative complementation) occurs in most interallelic heterozygotes involving these two mutations. As hemizygotes, the other four alleles are predominantly larval/pupal lethals. Partial complementation is achieved by most interallelic heterozygotes involving these four alleles. Phenotypic defects associated with the six tubulin mutation include disrupted embryos, pseudopupae, pharate adults with defects in various cuticular pattern elements, pharate adults with retarded head development, adults with leg tremors and extremely short life spans, and viable but sterile adults with bristle defects.     

Behavioral mutants of Drosophila melanogaster. IV. Analysis of developmentally temperature-sensitive mutations affecting flight

Mutations in 13 genes with temperature-sensitive (ts), flightless phenotypes have been examined. All hop and fly well when raised at the permissive temperature, but fly poorly, or not at all, when raised at the restrictive temperature. The mutations were divided into three groups on the basis of their temperature-sensitive periods (TSPs) for flightlessness. The TSPs for mutations at five loci, fli-C¹, D¹, E¹, I¹, and shak A¹, in the first group are confined to 24 to 48 hr interval during early pupal development. Mutations in the second group, including eag¹⁰¹, fli B¹, and fu^ts1 have continuous TSPs 3 to 4 days in length, extending from late larval through the early pupal stages. The flight TSPs for mutations in the third class, including fli J¹, fli K², flrd H³, and flrd N¹, are almost continuous, and span most of the larval and pupal periods. Many of the mutations have pleiotropic phenotypes, including semilethality and lethality, and wing posture and cuticle abnormalities, with discernible TSPs. One of the more intriguing pleiotropic phenotypes is the ts optomotor response exhibited by fli J², the TSP for which extends from late larval through late pupal stages.     

The nature of reverse mutations in Drosophila melanogaster

A selection system for the screening of reversions has been constructed and used to test reversions of lethals located in the proximal region of the X chromosome of Drosophila and of Kpn mutations.Spontaneous and induced reversions have been screened, X-rays and ethyl methanesulphonate (EMS) being the mutagens used in the induction experiments.No genuine back-mutation was found in 6·10⁵ gametes scored. Sterile reversions of all four lethals tested were obtained. Their frequency suggested that at least in three of the lethals the sterile reversions represented “escapers” of the lethal effect rather than true revertants.Three fertile reversions of l^x4 were found and analyzed. All three were autosomal suppressors, located on the second chromosome, allelic to each other, dominant in males and recessive in females.One fertile reversion of l^3DES was found to be an X-linked suppressor. It is suggested that this suppressor is a Y-suppressed lethal, showing a V-type position effect, resulting from an aberration included in the proximal heterochromatin of the X chromosome.Reversions of Kpn were obtained at a similar rate to that found in previous reports²².The absence of true back-mutants in our experiments, in contrast to findings in previous reports, is discussed. From the existing literature on spontaneous and induced back-mutations in Drosophila melanogaster it appears that for several mutations the rates of forward and back-mutation are of the same order of magnitude. It is suggested that reported cases of back-mutations represent mainly inter- and intrachromosomal recombination in duplicated regions rather than mutational events and that the frequency of true back-mutation in Drosophila is usually of an order of magnitude, similar to that known for microorganisms and fungi.     

The recent demographic and adaptive history of Drosophila melanogaster

Population genetic analyses of the past two decades confirmed an earlier hypothesis by L Tsacas and D Lachaise that the cosmopolitan species Drosophila melanogaster has an Afrotropical origin, and that it colonized the rest of the world only very recently. Maximum likelihood analyses based on multilocus data suggest that the putative ancestral African population expanded its size about 60,000 years ago (ya). These demographic changes were accompanied by the fixation of numerous beneficial mutations, as revealed by signatures of positive directional selection in the genome (selective sweeps). The estimated rate of adaptive substitution on the X chromosome is in the order of 10(-11) per nucleotide site per generation. Comparable (but not significantly higher) substitution rates are found in derived populations that colonized new habitats outside Africa, such as in a European population that branched off from the African lineage about 16,000 ya.     

Life-history consequences of egg size in Drosophila melanogaster

We used a novel approach to study the effects of egg size on offspring fitness components in Drosophila melanogaster. Populations that differed genetically in egg size were crossed, and the female offspring from these reciprocal crosses were examined for life-history traits. These flies expressed effects of egg size, because they developed from eggs of different sizes as a result of maternal genetic effects, but displayed an equivalent range of nuclear genetic variation. The crosses used four independent pairs of outbred populations that differed in the pattern of covariation between egg size and life-history traits, so that the maternal genetic effects of egg size on offspring characters could be contrasted to the associations present among the parental populations. Egg size showed positive maternal genetic effects on embryonic viability and development rate, hatchling weight and feeding rate, and egg-larva and egg-adult development rate but no consistent effects on larval competitive ability, adult weight, or egg size in the offspring. Our method revealed a pattern of causality that could not be deduced from interpopulation comparisons and therefore provides a good way of disentangling the causes and consequences of variation in egg size while controlling for zygotic genetic effects.     

The adaptive significance of chromosomal inversion polymorphisms in Drosophila melanogaster

Chromosomal inversions, structural mutations that reverse a segment of a chromosome, cause suppression of recombination in the heterozygous state. Several studies have shown that inversion polymorphisms can form clines or fluctuate predictably in frequency over seasonal time spans. These observations prompted the hypothesis that chromosomal rearrangements might be subject to spatially and/or temporally varying selection. Here, we review what has been learned about the adaptive significance of inversion polymorphisms in the vinegar fly Drosophila melanogaster, the species in which they were first discovered by Sturtevant in 1917. A large body of work provides compelling evidence that several inversions in this system are adaptive; however, the precise selective mechanisms that maintain them polymorphic in natural populations remain poorly understood. Recent advances in population genomics, modelling and functional genetics promise to greatly improve our understanding of this long‐standing and fundamental problem in the near future.     

The genetic basis of adaptive pigmentation variation in Drosophila melanogaster

In a broad survey of Drosophila melanogaster population samples, levels of abdominal pigmentation were found to be highly variable and geographically differentiated. A strong positive correlation was found between dark pigmentation and high altitude, suggesting adaptation to specific environments. DNA sequence polymorphism at the candidate gene ebony revealed a clear association with the pigmentation of homozygous third chromosome lines. The darkest lines sequenced had nearly identical haplotypes spanning 14.5 kb upstream of the protein-coding exons of ebony. Thus, natural selection may have elevated the frequency of an allele that confers dark abdominal pigmentation by influencing the regulation of ebony.     

Genetic,cytological, and ultrastructural characterization of a temperature-sensitive lethal in Drosophila melanogaster

Genetic analysis of a strain of Drosophila melanogaster revealed that a recessive mutation [l(1)ER^ts] causing temperature-sensitive embryonic lethality is located in the distal region of the X chromosome approximately at map position 18. At 22–25°C mutant embryos exhibit normal viability, and all eggs arrest prior to gastrulation if they are reared at 29°C. The mutant is biphasic, exhibiting a maternal effect which is expressed throughout the first 8 hr of development as well as a second temperature-sensitive period (TSP) during the first 3 days of larval life. Larvae exposed to the restrictive temperature (RT) during the second TSP must also spend the remainder of larval and pupal life and the time of normal eclosion at RT to die as fully developed pupae which fail to eclose. Light and electron microscopy of arrested embryos reveal disturbances in the distribution of nuclei, cytoplasm, and yolk and abnormal configurations of rough endoplasmic reticulum. The cause of pupal death during the second lethal period is unknown.     

Genetic instability in Drosophila melanogaster. Evidence for insertion mutations

Summary An X chromosome in Drosophila melanogaster is described which is mutationally unstable. Mutational events were identified through phenotypic changes associated with a tandem duplication of the X chromosome in which the white locus is present in duplicate. The left segment of the tandem duplication was marked with the mutant w ^sp, the right segment with mutant w ^17G. Some of the phenotypic changes were identified as deletions involving the w ^17G marked segment of the duplication. Other phenotypic changes involved the left segment in which phenotypically w ^sp mutated to w. Experimental evidence is presented which attributes these latter mutations to insertions of foreign DNA into the w locus equivalent to the insertion mutations of E. coli.     

Genomic analysis of adaptive differentiation in Drosophila melanogaster

Drosophila melanogaster shows clinal variation along latitudinal transects on multiple continents for several phenotypes, allozyme variants, sequence variants, and chromosome inversions. Previous investigation suggests that many such clines are due to spatially varying selection rather than demographic history, but the genomic extent of such selection is unknown. To map differentiation throughout the genome, we hybridized DNA from temperate and subtropical populations to Affymetrix tiling arrays. The dense genomic sampling of variants and low level of linkage disequilibrium in D. melanogaster enabled identification of many small, differentiated regions. Many regions are differentiated in parallel in the United States and Australia, strongly supporting the idea that they are influenced by spatially varying selection. Genomic differentiation is distributed nonrandomly with respect to gene function, even in regions differentiated on only one continent, providing further evidence for the role of selection. These data provide candidate genes for phenotypes known to vary clinally and implicate interesting new processes in genotype-by-environment interactions, including chorion proteins, proteins regulating meiotic recombination and segregation, gustatory and olfactory receptors, and proteins affecting synaptic function and behavior. This portrait of differentiation provides a genomic perspective on adaptation and the maintenance of variation through spatially varying selection.     

Characterisation of male meiotic-sterile mutations in Drosophila melanogaster

Male meiotic sterile mutations were selected among X-linked male—steriles by detection of micronuclei in early spermatids. Despite severe defects in the 1st or 2nd meiotic spindles in all mutants, no effect on mitosis was observed. Various features of spindle structure, chromosome segregation, and centriole movements were compared in seven meiotic steriles and in XO males. Chromosome behaviour and centriole movement were always affected concomitantly, and were both shown to be genetically independent of centre formation in the meiotic spindles. Precocious and delayed centromere separation was observed in the various mutants in both divisions, and similarly attributed to basic spindle lesions rather than chromosome defects. Attachment of the centriole body to the membrane of the spermatid nucleus was normal only in mutants where second division nuclei were formed. The role of the centriole body was shown to be independent of membrane attachment.—The phenomena observed in this study were discussed mainly with regard to genetic interdependence of morphogenetic processes during male meiosis. A common base for the pleiotropic defects of meiotic steriles and XO males is suggested, and the genetic control of meiosis is re-evaluated in the light of comparison with fertile meiotic mutants.     

Dominance of mutations affecting viability in Drosophila melanogaster

There have been several attempts to estimate the average dominance (ratio of heterozygous to homozygous effects) of spontaneous deleterious mutations in Drosophila melanogaster, but these have given inconsistent results. We investigated whether transposable element (TE) insertions have higher average dominance for egg-to-adult viability than do point mutations, a possibility suggested by the types of fitness-depressing effects that TEs are believed to have. If so, then variation in dominance estimates among strains and crosses would be expected as a consequence of variation in TE activity. As a first test, we estimated the average dominance of all mutations and of copia insertions in a set of lines that had accumulated spontaneous mutations for 33 generations. A traditional regression method gave a dominance estimate for all mutations of 0.17, whereas average dominance of copia insertions was 0.51; the difference between these two estimates approached significance (P = 0.08). As a second test, we reanalyzed Ohnishi 1974 data on dominance of spontaneous and EMS-induced mutations. Because a considerable fraction of spontaneous mutations are caused by TE insertions, whereas EMS induces mainly point mutations, we predicted that average dominance would decline with increasing EMS concentration. This pattern was observed, but again fell short of formal significance (P = 0.07). Taken together, however, the two results give modest support for the hypothesis that TE insertions have greater average dominance in their viability effects than do point mutations, possibly as a result of deleterious effects of expression of TE-encoded genes.     

Age-specific properties of spontaneous mutations affecting mortality in Drosophila melanogaster.

An analysis of the effects of spontaneous mutations affecting age-specific mortality was conducted using 29 lines of Drosophila melanogaster that had accumulated spontaneous mutations for 19 generations. Divergence among the lines was used to estimate the mutational variance for weekly mortality rates and the covariance between weekly mortality rates at different ages. Significant mutational variance was observed in both males and females early in life (up to approximately 30 days of age). Mutational variance was not significantly different from zero for mortality rates at older ages. Mutational correlations between ages separated by 1 or 2 wk were generally positive, but they declined monotonically with increasing separation such that mutational effects on early-age mortality were uncorrelated with effects at later ages. Analyses of individual lines revealed several instances of mutation-induced changes in mortality over a limited range of ages. Significant age-specific effects of mutations were identified in early and middle ages, but surprisingly, mortality rates at older ages were essentially unaffected by the accumulation procedure. Our results provide strong evidence for the existence of a class of polygenic mutations that affect mortality rates on an age-specific basis. The patterns of mutational effects measured here relate directly to recently published estimates of standing genetic variance for mortality in Drosophila, and they support mutation accumulation as a viable mechanism for the evolution of senescence.     

Evolutionary consequences of altered atmospheric oxygen in Drosophila melanogaster

Twelve replicate populations of Drosophila melanogaster, all derived from a common ancestor, were independently evolved for 34+ generations in one of three treatment environments of varying PO(2): hypoxia (5.0-10.1 kPa), normoxia (21.3 kPa), and hyperoxia (40.5 kPa). Several traits related to whole animal performance and metabolism were assayed at various stages via "common garden" and reciprocal transplant assays to directly compare evolved and acclimatory differences among treatments. Results clearly demonstrate the evolution of a greater tolerance to acute hypoxia in the hypoxia-evolved populations, consistent with adaptation to this environment. Greater hypoxia tolerance was associated with an increase in citrate synthase activity in fly homogenate when compared to normoxic (control) populations, suggesting an increase in mitochondrial volume density in these populations. In contrast, no direct evidence of increased performance of the hyperoxia-evolved populations was detected, although a significant decrease in the tolerance of these populations to acute hypoxia suggests a cost to adaptation to hyperoxia. Hyperoxia-evolved populations had lower productivity overall (i.e., across treatment environments) and there was no evidence that hypoxia or hyperoxia-evolved populations had greatest productivity or longevity in their respective treatment environments, suggesting that these assays failed to capture the components of fitness relevant to adaptation.