George W. Gilchrist

Specialists and Generalists in Changing Environments. I. Fitness Landscapes of Thermal Sensitivity

Animals and plants often exhibit narrow ranges of thermal preference in variable environments; fitness-enhancing activities such as reproduction and growth tend to be concentrated during times in which body temperature lies within that narrow range. The relation between fitness-associated performance and temperature is modeled by a performance curve defined by two traits: performance breadth (Tbr), a measure of thermal specialization, and the critical maximum temperature for performance (Tmax). Optimality models are used to define the fitness landscape for these two traits under several different patterns of within- and among-generation variation in temperature. In constant environments and environments in which there is significant within-generation variation, specialists with narrow preference ranges are the favored phenotype. In environments in which there is considerable among-generation but little within-generation variation, generalists with broad preference ranges are favored. Specialists in a constant environment have a mean fitness an order of magnitude higher than any phenotype in more variable environments, demonstrating that homeostatic mechanisms can confer a large fitness advantage. In contrast to previous models of environmental tolerance, these performance models suggest that increasing temporal environmental variation can favor the evolution of thermal specialization.

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.

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°C (10+ yr), 25°C (9+ yr), or 29°C (4+ yr). The 16.5°C and 25°C lines are known to have diverged in fitness at 16.5°C versus 25°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 breadth 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.

A QUANTITATIVE GENETIC ANALYSIS OF THERMAL SENSITIVITY IN THE LOCOMOTOR PERFORMANCE CURVE OF APHIDIUS ERVI

The thermal sensitivity of locomotor performance in Aphidius ervi, a parasitic hymenopteran, conforms to the “jack‐of‐all‐trades is master of none” model of specialist‐generalist trade‐offs. Performance breadth and maximal performance at the phenotypic level are negatively correlated in both sexes. A strong, negative genetic correlation was found for males, but not for females. In males, the broad‐sense heritability of performance breadth was about 0.16, and that of maximum walking velocity was about 0.29. Neither heritability was significantly different from zero in females. The broad‐sense heritability of body mass was about 0.3 in females and 0.6 in males, with a strong negative genetic correlation between size and maximum velocity in males only. These data provide the first quantitative genetic analysis of performance curves in eukaryotic animals, and one of the few demonstrations of the specialist‐generalist trade‐off that underlies much theory in evolutionary ecology.

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 C) and were tested at different temperatures (18, 25, and 29°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.

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 ≈37°C) had largely lost the upper mode. The realized heritability of Tkd computed over the first 10 selection episodes was ≈0.12 in the Up-selected and ≈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.

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°C, 25°C, or 29°C (Tpar) and then their offspring were reared at 18°C, 25°C, or 29°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.

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.

Chapter 5 - The Evolution of Thermal Sensitivity in Changing Environments

The genetic models show that oscillating selection imposed by daily and seasonal environmental variation is effective in maintaining heritable genetic variation for environmental sensitivity. Fluctuating temporal variation is common to all natural habitats and may contribute to the high heritability for fitness-related traits often found in natural populations. The rates of evolution are even slower than might be expected because of conflicting selection pressures imposed by genotype-environment interactions; however, these same interactions may provide important help in maintaining genetic variation in populations. Hopefully, emerging methods in the molecular study of temperature responses will be applied to these fundamental questions that bridge the world of molecular biology, ecology, and evolutionary physiology.