The chromosomal polymorphism of Drosophila subobscura: a microevolutionary weapon to monitor global change.

The Palaearctic species Drosophila subobscura recently invaded the west coast of Chile and North America. This invasion helped to corroborate the adaptive value of the rich chromosomal polymorphism of the species, as the same clinal patterns than those observed in the original Palaearctic area were reproduced in the colonized areas in a relatively short period of time. The rapid response of this polymorphism to environmental conditions makes it a good candidate to measure the effect of the global rising of temperatures on the genetic composition of populations. Indeed, the long-term variation of this polymorphism shows a general increase in the frequency of those inversions typical of low latitudes, with a corresponding decrease of those typical of populations closer to the poles. Although the mechanisms underlying these changes are not well understood, the system remains a valid tool to monitor the genetic impact of global warming on natural populations.

Introduction history of Drosophila subobscura in the New World: a microsatellite-based survey using ABC methods.

Drosophila subobscura is a Palearctic species that was first observed in South and North America in the early 1980s, and that rapidly invaded broad latitudinal ranges on both continents. To trace the source and history of this invasion, we obtained genotypic data on nine microsatellite loci from two South American, two North American and five European populations of D. subobscura. We analysed these data with traditional statistics as well as with an approximate Bayesian computation (ABC) framework. ABC methods yielded the strongest support for the scenario involving a serial introduction with founder events from Europe into South America, and then from South America into North America. Stable effective population size of the source population was very large (around one million individuals), and the propagule size was notably smaller for the introduction into South America (i.e. high bottleneck severity index with only a few effective founders) but considerably larger for the subsequent introduction into North America (i.e. low bottleneck severity index with around 100-150 effective founders). Finally, the Mediterranean region of Europe (and most likely Barcelona from the localities so far analysed) is proposed as the source of the New World flies, based on mean individual assignment statistics.

Locomotor performance of Drosophila melanogaster: interactions among developmental and adult temperatures, age, and geography.

We explored the extent to which a phenotypic trait (walking speed) of Drosophila melanogaster is influenced by population, developmental temperature, adult temperature, and age. Our goals were to estimate the importance of these factors and to test the beneficial acclimation hypothesis. We measured speed of flies from two populations (the Congo and France) that developed at different temperatures (18, 25, and 29 degrees C) and were tested at different temperatures (18, 25, and 29 degrees C) and ages (2, 7, 13 days). Not surprisingly, speed increased strongly with test temperature. Speed was generally greatest for flies reared at an intermediate developmental temperature, contrary to the beneficial acclimation hypothesis, which predicts that speed would be greatest when influenced by interactions involving population. For example, speed was greatest for flies from France that developed at a low temperature, but for flies from the Congo that developed at a high temperature. The impact of developmental temperature declined with age. Surprisingly, speed actually increased with age for flies raised and maintained at a low temperature, but decreased with age for flies raised and maintained at an intermediate or at a high temperature. Thus, walking performance is highly dynamic phenotypically, complicating potential attempts to predict responses to selection on performance.

Parental and developmental temperature effects on the thermal dependence of fitness in Drosophila melanogaster.

Cross-generational effects refer to nongenetic influences of the parental phenotype or environment on offspring phenotypes. Such effects are commonly observed, but their adaptive significance is largely unresolved. We examined cross-generational effects of parental temperature on offspring fitness (estimated via a serial-transfer assay) at different temperatures in a laboratory population of Drosophila melanogaster. Parents were reared at 18 degrees C, 25 degrees C, or 29 degrees C (Tpar) and then their offspring were reared at 18 degrees C, 25 degrees C, or 29 degrees C (Toff) to evaluate several competing hypotheses (including an adaptive one) involving interaction effects of parental and offspring temperature on offspring fitness. The results clearly show that hotter parents are better; in other words, the higher the temperature of the parents, the higher the fitness of their offspring, independent of offspring thermal environment. These data contradict the adaptive cross-generational hypothesis, which proposes that offspring fitness is maximal when the offspring thermal regime matches the parental one. Flies with hot parents have high fitness seemingly because their own offspring develop relatively quickly, not because they have higher fecundity early in life.

Rapid evolution of wing size clines in Drosophila subobscura.

Parallel latitudinal clines across species and continents provide dramatic evidence of the efficacy of natural selection, however little is known about the dynamics involved in cline formation. For example, several drosophilids and other ectotherms increase in body and wing size at higher latitudes. Here we compare evolution in an ancestral European and a recently introduced (North America) cline in wing size and shape in Drosophila subobscura. We show that clinal variation in wing size, spanning more than 15 degrees of latitude, has evolved in less than two decades. In females from Europe and North America, the clines are statistically indistinguishable however the cline for North American males is significantly shallower than that for European males. We document that while overall patterns of wing size are similar on two continents, the European cline is obtained largely through changing the proximal portion of the wing, whereas the North American cline is largely in the distal portion. We use data from sites collected in 1986/1988 (Pegueroles et al. 1995) and our 1997 collections to compare synchronic (divergence between contemporary populations that share a common ancestor) and allochronic (changes over time within a population) estimates of the rates of evolution. We find that, for these populations, allochronically estimated evolutionary rates within a single population are over 0.02 haldanes (2800 darwins), a value similar in magnitude to the synchronic estimates from the extremes of the cline. This paper represents an expanded analysis of data partially presented in Huey et al. (2000).

Rapid evolution of a geographic cline in size in an introduced fly.

The introduction and rapid spread of Drosophila subobscura in the New World two decades ago provide an opportunity to determine the predictability and rate of evolution of a geographic cline. In ancestral Old World populations, wing length increases clinally with latitude. In North American populations, no wing length cline was detected one decade after the introduction. After two decades, however, a cline has evolved and largely converged on the ancestral cline. The rate of morphological evolution on a continental scale is very fast, relative even to rates measured within local populations. Nevertheless, different wing sections dominate the New versus Old World clines. Thus, the evolution of geographic variation in wing length has been predictable, but the means by which the cline is achieved is contingent.

The direct response of Drosophila melanogaster to selection on knockdown temperature.

We selected on knockdown temperature, the upper temperature at which insects lose the ability to cling to an inclined surface, in replicate populations of Drosophila melanogaster for 32 generations (46 generations of rearing). Knockdown temperature (Tkd) was initially bimodally distributed in both control and selected lines, and a similar pattern was found in several populations surveyed from two other continents. Within 20 generations of selection, the Up-selected lines (top 25% each generation) had lost the lower mode and the Low-selected lines (selected to fall out at approximately 37 degrees C) had largely lost the upper mode. The realized heritability of Tkd computed over the first 10 selection episodes was approximately 0.12 in the Up-selected and approximately 0.19 in the Low-selected lines. Realized heritability rose dramatically in the Low-selected lines over the first 20 generations of selection. The two modes, plus this rise in heritability, suggest that knockdown temperature is the product of one or two genes of large effect. The global polymorphism for knockdown temperature, coupled with the ease of selective removal of either mode, suggests that genetic variation for knockdown temperature may be maintained by natural selection.

Thermal sensitivity of Drosophila melanogaster: evolutionary responses of adults and eggs to laboratory natural selection at different temperatures.

We compared aspects of the thermal sensitivity of replicated lines of Drosophila melanogaster that had been evolving by laboratory natural selection at three selection temperatures: 16.5 degrees C (10+ yr), 25 degrees C (9+ yr), or 29 degrees C (4+ yr). The 16.5 degrees C and 25 degrees C lines are known to have diverged in fitness at 16.5 degrees C versus 25 degrees C and also in heat tolerance. We designed new experiments to explore further possible shifts in thermal sensitivity of these lines. The optimal temperature for walking speed of adults was positively related to selection temperature, but differences among lines in thermal sensitivity of walking speed were small. Performance breath was inversely related to selection temperature. Tolerance of adults to an acute heat shock was also positively related to selection temperature, but tolerance to a cold shock was not. Thus, fitness at moderately high temperatures is genetically coupled with tolerance of extreme high (but not of low) temperature. Knock-down temperature and walking speed at high temperature, however, were independent of selection temperature. In contrast to adults, eggs from different lines had similar heat and cold tolerance. Thus, long-term natural selection has led to divergence in thermal sensitivity of some (but not of all) traits and may have had more of an impact on adults than on eggs. Attempts to predict evolutionary states in nature are, however, complicated because of the observed genetic correlations and the simple selection scheme.

Within- and between-generation effects of temperature on early fecundity of Drosophila melanogaster.

We used a repeated-measures, four-factor experimental design to determine how the fecundity of Drosophila melanogaster during the first 5 days of adult life was influenced by paternal, maternal, developmental and laying temperature, with two different temperature levels (18 degrees C vs. 25 degrees C) per factor. Laying temperature had by far the largest effect on fecundity and accounted for 79 per cent of the variance in overall fecundity: flies laying at 25 degrees C began laying eggs about a day earlier and had much higher daily fecundities than did those laying at 18 degrees C. Developmental temperature had no significant effect either on overall fecundity or on the pattern of daily egg production. Dam temperature had a slight effect on the pattern of daily egg production, but not on overall fecundity. In contrast, sire temperature slightly influenced both overall fecundity and the pattern of daily egg production. Our results demonstrate that early fecundity is extraordinarily sensitive to laying temperature (360 per cent increase if laying at 25 degrees C vs. at 18 degrees C), but is relatively well buffered against developmental and cross-generational effects (maximum effect only 7 per cent, for sire temperature).