Locomotion in Response to Shifting Climate Zones: Not So Fast

Although a species’ locomotor capacity is suggestive of its ability to escape global climate change, such a suggestion is not necessarily straightforward. Species vary substantially in locomotor capacity, both ontogenetically and within/among populations, and much of this variation has a genetic basis. Accordingly, locomotor capacity can and does evolve rapidly, as selection experiments demonstrate. Importantly, even though this evolution of locomotor capacity may be rapid enough to escape changing climate, genetic correlations among traits (often due to pleiotropy) are such that successful or rapid dispersers are often limited in colonization or reproductive ability, which may be viewed as a trade-off. The nuanced assessment of this variation and evolution is reviewed for well-studied models: salmon, flying versus flightless insects, rodents undergoing experimental evolution, and metapopulations of butterflies. This work reveals how integration of physiology with population biology and functional genomics can be especially informative

Hsp70 and Larval Thermotolerance in Drosophila melanogaster: How Much is Enough and When is More Too Much?

Heat shock proteins (Hsps) and other molecular chaperones perform diverse cellular roles (e.g., inducible thermotolerance) whose functional consequences are concentration dependent. We manipulated Hsp70 concentration quantitatively in intact larvae of Drosophila melanogaster to examine its effect on survival, developmental time and tissue damage after heat shock. Larvae of an extra-copy strain, which has 22 hsp70 copies, produced Hsp70 more rapidly and to higher concentrations than larvae of a control strain, which has the wild-type 10 copies of the gene. Increasing the magnitude and duration of pretreatment increased Hsp70 concentrations, improved tolerance of more severe stress, and reduced delays in development. Pretreatment, however, did not protect against acute tissue damage. For larvae provided a brief or mild intensity pretreatment, faster expression of Hsp70 in the extra-copy strain improved survival to adult and reduced tissue damage 21 h after heat shock. Negative effects on survival ensued in extra-copy larvae pretreated most intensely, but their overexpression of Hsp70 did not increase tissue damage. Because rapid expression to yield a low Hsp70 concentration benefits larvae but overexpression harms them, natural selection may balance benefits and costs of high and low expression levels in natural populations

Reverse transcriptional profiling: non-correspondence of transcript level variation and proximal promoter polymorphism

BACKGROUND: Variation in gene expression between two Drosophila melanogaster strains, as revealed by transcriptional profiling, seldom corresponded to variation in proximal promoter sequence for 34 genes analyzed. Two sets of protein-coding genes were selected from pre-existing microarray data: (1) those whose expression varied significantly and reproducibly between strains, and (2) those whose transcript levels did not vary. Only genes whose regulation of expression was uncharacterized were chosen. At least one kB of the proximal promoters of 15–19 genes in each set was sequenced and compared between strains (Oregon R and Russian 2b). RESULTS: Of the many promoter polymorphisms, 89.6% were SNPs and 10.4% were indels, including homopolymer tracts, microsatellite repeats, and putative transposable element footprints. More than half of the SNPs were changes within a nucleotide class. Hypothetically, genes differing in expression between the two strains should have more proximal promoter polymorphisms than those whose expression is similar. The number, frequency, and type of polymorphism, however, were the same in both sets of genes. In fact, the promoters of six genes with significantly different mRNA expression were identical in sequence. CONCLUSION: For these genes, sequences external to the proximal promoter, such as enhancers or in trans, must play a greater role than the proximal promoter in transcriptomic variation between D. melanogaster strains

Natural and Genetic Engineering of the Heat-Shock Protein Hsp70 in Drosophila melanogaster: Consequences for Thermotolerance

Larvae of the fruit fly, Drosophila melanogaster, live within necrotic fruit, a challenging environment in which larvae can experience severe thermal stress. One response to thermal stress, the expression of heat-shock proteins (Hsps), has evolved distinctively in this species; the gene encoding Hsp70 has undergone extensive duplication and accounts for the bulk of Hsps that are expressed upon heat shock. Genetic engineering of hsp70 copy number is sufficient to affect thermotolerance at some (but not all) life stages. Increases in Hsp70, moreover, can protect intact larvae against thermal inactivation of the enzyme alcohol dehydrogenase and thermal inhibition of feeding. Deleterious consequences of high levels of Hsp70, however, may limit further evolutionary proliferation of hsp70 genes. These findings illustrate how the perspectives of integrative and comparative biology, if applied to even well-studied model organisms, can lead to novel findings

Natural Hyperthermia and Expression of the Heat Shock Protein Hsp70 Affect Developmental Abnormalities in Drosophila Melanogaster

We Demonstrate that Natural Heat Stress on Wild Larval Drosophila Melanogaster Results in Severe Developmental Defects in \u3e10% of Eclosing Adults, and that Increased Copy Number of the Gene Encoding the Major Inducible Heat Shock Protein of D. Melanogaster, Hsp70, is Sufficient to Reduce the Incidence of Such Abnormalities. Specifically, Non-Adult D. Melanogaster Inhabiting Necrotic Fruit Experienced Severe, Often Lethal Heat Stress in Natural Settings. Adult Flies Eclosing from Wild Larvae that Had Survived Natural Heat Stress Exhibited Severe Developmental Anomalies of Wing and Abdominal Morphology, Which Should Dramatically Affect Fitness. the Frequency of Developmental Abnormalities Varied Along Two Independent Natural Thermal Gradients, exceeding 10% in Adults Eclosing from Larvae Developing in Warm, Sunlit Fruit. When Exposed to Natural Heat Stress, D. Melanogaster Larvae with the Wild-Type Number of Hsp70 Genes (N=10) Developed Abnormal Wings Significantly More Frequently Than a Transgenic Sister Strain with 22 Copies of the Hsp70 Gene

Experimental Manipulation of the Cost of Thermal Acclimation in Drosophila melanogaster

Acclimation to environmental change can impose costs on organisms. One potential cost is the energy and nutrients consumed by a physiological response, e.g. the resources required for expression of heat-shock proteins (Hsps). We examined the significance of this cost by genetic manipulation. We isolated four isofemale lines from a Drosophila melanogaster population previously transformed with a hsp70-kcZ fusion. Lines were similar in Hsp70 expression but differed in P-galactosidase expression upon heat shock, and replicates of each line were reared on a high quantity and low quantity medium. Multiple heat shock reduced survival in all lines, but did not increase developmental time. Variation in expression of β-galactosidase among lines, which differed more than 4-fold in response to heat treatment, was unrelated to the decreased survival. Thus the predicted effects of β-galactosidase expression on components of fitness were not evident. The superimposition of costs upon those normal for acclimation had no effect on mortality or developmental time, even when resources were especially limiting

Heat-Shock Promoters: Targets for Evolution by <i>P</i> Transposable Elements in <i>Drosophila</i>

Transposable elements are potent agents of genomic change during evolution, but require access to chromatin for insertion—and not all genes provide equivalent access. To test whether the regulatory features of heat-shock genes render their proximal promoters especially susceptible to the insertion of transposable elements in nature, we conducted an unbiased screen of the proximal promoters of 18 heat-shock genes in 48 natural populations of Drosophila. More than 200 distinctive transposable elements had inserted into these promoters; greater than 96% are P elements. By contrast, few or no P element insertions segregate in natural populations in a “negative control” set of proximal promoters lacking the distinctive regulatory features of heat-shock genes. P element transpositions into these same genes during laboratory mutagenesis recapitulate these findings. The natural P element insertions cluster in specific sites in the promoters, with up to eight populations exhibiting P element insertions at the same position; laboratory insertions are into similar sites. By contrast, a “positive control” set of promoters resembling heat-shock promoters in regulatory features harbors few P element insertions in nature, but many insertions after experimental transposition in the laboratory. We conclude that the distinctive regulatory features that typify heat-shock genes (in Drosophila) are especially prone to mutagenesis via P elements in nature. Thus in nature, P elements create significant and distinctive variation in heat-shock genes, upon which evolutionary processes may act.</p

Heritability of Expression of the 70kd Heat-shock Protein in Drosophila melanogaster and its Relevance to the Evolution of Thermotolerance

The principle inducible heat-shock protein of Drosophila melanogasrer, Hsp70, contributes to thermotolerance throughout the entire life cycle of the species but may also reduce fitness in some life stages. In principle, selection might maximize the benefits of Hsp70 expression relative to its costs by adjusting the magnitude of Hsp70 expression for each life-cycle stage independently. Therefore we examined whether the magnitude of Hsp70 ex pre sion varied during the life cycle and the relationship of this variation to several life-history traits. For 28 isofemale lines derived from a single natural population, estimates of heritable variation in Hsp70 expression ranged between 0.25 and 0.49, and the association among variation in first- and third-instar larvae and in adults correlated highly. Thus, Hsp70 expression is genetically coupled at these developmental stages. A line engineered with extra copies of the hsp70 gene produced more Hsp70 and survived heat shock much better than did a control strain . Among natural lines, Hsp70 expression was only weakly related to tolerance of heat shock and to larva-to-adult survival and developmental time at permissive temperatures. Additionally, lines with high adult survival developed slowly as larvae, which is a possible trade-off. These and other findings suggest that trade-offs may maintain quantitative variation both in heat shock protein expression and in life-history traits that associate with thermotolerance

Heat-Shock Promoters: Targets for Evolution by P Transposable Elements in Drosophila

Transposable elements are potent agents of genomic change during evolution, but require access to chromatin for insertion—and not all genes provide equivalent access. To test whether the regulatory features of heat-shock genes render their proximal promoters especially susceptible to the insertion of transposable elements in nature, we conducted an unbiased screen of the proximal promoters of 18 heat-shock genes in 48 natural populations of Drosophila. More than 200 distinctive transposable elements had inserted into these promoters; greater than 96% are P elements. By contrast, few or no P element insertions segregate in natural populations in a “negative control” set of proximal promoters lacking the distinctive regulatory features of heat-shock genes. P element transpositions into these same genes during laboratory mutagenesis recapitulate these findings. The natural P element insertions cluster in specific sites in the promoters, with up to eight populations exhibiting P element insertions at the same position; laboratory insertions are into similar sites. By contrast, a “positive control” set of promoters resembling heat-shock promoters in regulatory features harbors few P element insertions in nature, but many insertions after experimental transposition in the laboratory. We conclude that the distinctive regulatory features that typify heat-shock genes (in Drosophila) are especially prone to mutagenesis via P elements in nature. Thus in nature, P elements create significant and distinctive variation in heat-shock genes, upon which evolutionary processes may act

Locomotion in Response to Shifting Climate Zones: Not So Fast

Although a species’ locomotor capacity is suggestive of its ability to escape global climate change, such a suggestion is not necessarily straightforward. Species vary substantially in locomotor capacity, both ontogenetically and within/among populations, and much of this variation has a genetic basis. Accordingly, locomotor capacity can and does evolve rapidly, as selection experiments demonstrate. Importantly, even though this evolution of locomotor capacity may be rapid enough to escape changing climate, genetic correlations among traits (often due to pleiotropy) are such that successful or rapid dispersers are often limited in colonization or reproductive ability, which may be viewed as a trade-off. The nuanced assessment of this variation and evolution is reviewed for well-studied models: salmon, flying versus flightless insects, rodents undergoing experimental evolution, and metapopulations of butterflies. This work reveals how integration of physiology with population biology and functional genomics can be especially informative