Margarida Matos

HOW REPEATABLE IS ADAPTIVE EVOLUTION? THE ROLE OF GEOGRAPHICAL ORIGIN AND FOUNDER EFFECTS IN LABORATORY ADAPTATION

Abstract The importance of contingency versus predictability in evolution has been a long-standing issue, particularly the interaction between genetic background, founder effects, and selection. Here we address experimentally the effects of genetic background and founder events on the repeatability of laboratory adaptation in Drosophila subobscura populations for several functional traits. We found disparate starting points for adaptation among laboratory populations derived from independently sampled wild populations for all traits. With respect to the subsequent evolutionary rate during laboratory adaptation, starvation resistance varied considerably among foundations such that the outcome of laboratory evolution is rather unpredictable for this particular trait, even in direction. In contrast, the laboratory evolution of traits closely related to fitness was less contingent on the circumstances of foundation. These findings suggest that the initial laboratory evolution of weakly selected characters may be unpredictable, even when the key adaptations under evolutionary domestication are predictable with respect to their trajectories.

Methuselah Flies: A Case Study in the Evolution of Aging

Creation and Long-Term Evolution of Methuselah Flies Stress Resistance, Physiology, and Aging Reproduction, Nutrition, and Aging Genetics and Molecular Biology of Methuselah Flies Reverse Evolution of Methuselah Flies Aging, Development, and Crowding.

Hamilton's forces of natural selection after forty years

Abstract In 1966, William D. Hamilton published a landmark paper in evolutionary biology: “The Moulding of Senescence by Natural Selection.” It is now apparent that this article is as important as his better-known 1964 articles on kin selection. Not only did the 1966 article explain aging, it also supplied the basic scaling forces for natural selection over the entire life history. Like the Lorentz transformations of relativistic physics, Hamiltons Forces of Natural Selection provide an overarching framework for understanding the power of natural selection at early ages, the existence of aging, the timing of aging, the cessation of aging, and the timing of the cessation of aging. His twin Forces show that natural selection shapes survival and fecundity in different ways, so their evolution can be somewhat distinct. Hamiltons Forces also define the context in which genetic variation is shaped. The Forces of Natural Selection are readily manipulable using experimental evolution, allowing the deceleration or acceleration of aging, and the shifting of the transition ages between development, aging, and late life. For these reasons, evolutionary research on the demographic features of life history should be referred to as “Hamiltonian.”

Reverse evolution of fitness in Drosophila melanogaster

Abstract The evolution of fitness is central to evolutionary theory, yet few experimental systems allow us to track its evolution in genetically and environmentally relevant contexts. Reverse evolution experiments allow the study of the evolutionary return to ancestral phenotypic states, including fitness. This in turn permits well‐defined tests for the dependence of adaptation on evolutionary history and environmental conditions. In the experiments described here, 20 populations of heterogeneous evolutionary histories were returned to their common ancestral environment for 50 generations, and were then compared with both their immediate differentiated ancestors and populations which had remained in the ancestral environment. One measure of fitness returned to ancestral levels to a greater extent than other characters did. The phenotypic effects of reverse evolution were also contingent on previous selective history. Moreover, convergence to the ancestral state was highly sensitive to environmental conditions. The phenotypic plasticity of fecundity, a character directly selected for, evolved during the experimental time frame. Reverse evolution appears to force multiple, diverged populations to converge on a common fitness state through different life‐history and genetic changes.

SYMMETRY BREAKING IN INTERSPECIFIC DROSOPHILA HYBRIDS IS NOT DUE TO DEVELOPMENTAL NOISE

Abstract Hybrids from crosses of different species have been reported to display decreased developmental stability when compared to their pure species, which is conventionally attributed to a breakdown of coadapted gene complexes. Drosophila subobscura and its close relative D. madeirensis were hybridized in the laboratory to test the hypothesis that genuine fluctuating asymmetry, measured as the within‐individual variance between right and left wings that results from random perturbations in development, would significantly increase after interspecific hybridization. When sires of D. subobscura were mated to heterospecific females following a hybrid half‐sib breeding design, F1 hybrid females showed a large bilateral asymmetry with a substantial proportion of individuals having an asymmetric index larger than 5% of total wing size. Such an anomaly, however, cannot be plainly explained by an increase of developmental instability in hybrids but is the result of some aberrant developmental processes. Our findings suggest that interspecific hybrids are as able as their parents to buffer developmental noise, notwithstanding the fact that their proper bilateral development can be harshly compromised. Together with the low correspondence between the covariation structures of the interindividual genetic components and the within‐individual ones from a Procrustes analysis, our data also suggest that the underlying processes that control (genetic) canalization and developmental stability do not share a common mechanism. We argue that the conventional account of decreased developmental stability in interspecific hybrids needs to be reappraised.

From nature to the laboratory: the impact of founder effects on adaptation.

Most founding events entail a reduction in population size, which in turn leads to genetic drift effects that can deplete alleles. Besides reducing neutral genetic variability, founder effects can in principle shift additive genetic variance for phenotypes that underlie fitness. This could then lead to different rates of adaptation among populations that have undergone a population size bottleneck as well as an environmental change, even when these populations have a common evolutionary history. Thus, theory suggests that there should be an association between observable genetic variability for both neutral markers and phenotypes related to fitness. Here, we test this scenario by monitoring the early evolutionary dynamics of six laboratory foundations derived from founders taken from the same source natural population of Drosophila subobscura. Each foundation was in turn three‐fold replicated. During their first few generations, these six foundations showed an abrupt increase in their genetic differentiation, within and between foundations. The eighteen populations that were monitored also differed in their patterns of phenotypic adaptation according to their immediately ancestral founding sample. Differences in early genetic variability and in effective population size were found to predict differences in the rate of adaptation during the first 21 generations of laboratory evolution. We show that evolution in a novel environment is strongly contingent not only on the initial composition of a newly founded population but also on the stochastic changes that occur during the first generations of colonization. Such effects make laboratory populations poor guides to the evolutionary genetic properties of their ancestral wild populations.

Evolutionary dynamics of molecular markers during local adaptation: a case study in Drosophila subobscura

BackgroundNatural selection and genetic drift are major forces responsible for temporal genetic changes in populations. Furthermore, these evolutionary forces may interact with each other. Here we study the impact of an ongoing adaptive process at the molecular genetic level by analyzing the temporal genetic changes throughout 40 generations of adaptation to a common laboratory environment. Specifically, genetic variability, population differentiation and demographic structure were compared in two replicated groups of Drosophila subobscura populations recently sampled from different wild sources.ResultsWe found evidence for a decline in genetic variability through time, along with an increase in genetic differentiation between all populations studied. The observed decline in genetic variability was higher during the first 14 generations of laboratory adaptation. The two groups of replicated populations showed overall similarity in variability patterns. Our results also revealed changing demographic structure of the populations during laboratory evolution, with lower effective population sizes in the early phase of the adaptive process. One of the ten microsatellites analyzed showed a clearly distinct temporal pattern of allele frequency change, suggesting the occurrence of positive selection affecting the region around that particular locus.ConclusionGenetic drift was responsible for most of the divergence and loss of variability between and within replicates, with most changes occurring during the first generations of laboratory adaptation. We also found evidence suggesting a selective sweep, despite the low number of molecular markers analyzed. Overall, there was a similarity of evolutionary dynamics at the molecular level in our laboratory populations, despite distinct genetic backgrounds and some differences in phenotypic evolution.Here we present a correction to our article Evolutionary dynamics of molecular markers during local adaptation: a case study in Drosophila subobscura. We have recently detected an error concerning the application of the Ln RH formula – a test to detect positive selection – to our microsatellite data. Here we provide the corrected data and discuss its implications for our overall findings. The corrections presented here have produced some changes relative to our previous results, namely in a locus (dsub14) that presents indications of being affected by positive selection. In general, our populations present less consistent indications of positive selection for this particular locus in both periods studied – between generations 3 and 14 and between generation 14 and 40 of laboratory adaptation. Despite this, the main findings of our study regarding the possibility of positive selection acting on that particular microsatellite still hold. As previously concluded in our article, further studies should be performed on this specific microsatellite locus (and neighboring areas) to elucidate in greater detail the evolutionary forces acting on this specific region of the O chromosome of Drosophila subobscura.

An evolutionary no man’s land

The gap between evolutionary studies in laboratory versus natural populations is a persistent problem1xSee all References, 2xLaboratory selection experiments using Drosophila: what do they really tell us?. Harshman, L.G. and Hoffmann, A.A. Trends Ecol. Evol. 200; 15: 32–36See all References. In an attempt to bridge this gap, some researchers in the early 1980s studied the quantitative genetics of laboratory populations recently founded from the wild, with and without inbreeding3xSee all References, 4xGenetic correlation structure of life history variables in outbred, wild Drosophila melanogaster: effects of photoperiod regimen. Giesel, J.T. Am. Nat. 1986; 128: 593–603CrossrefSee all References. The dangers of such approaches were soon demonstrated experimentally5xGenetic covariation in Drosophila life history: untangling the data. Rose, M.R. Am. Nat. 1984; 123: 565–569CrossrefSee all References, 6xGenetic covariation among life-history components: the effect of novel environments. Service, P.M. and Rose, M.R. Evolution. 1985; 39: 943–945CrossrefSee all References. Inbreeding depression and genotype-by-environment interactions make such studies unreliable guides to the evolution of populations long-established in any environment. This conclusion is reiterated to some extent in Harshman and Hoffmann’s recent TREE perspective2xLaboratory selection experiments using Drosophila: what do they really tell us?. Harshman, L.G. and Hoffmann, A.A. Trends Ecol. Evol. 200; 15: 32–36See all References2, where the authors state that, ‘The nature of laboratory selection regimes is unnatural.’ But, they then go on to propose complementing selection experiments in long-established laboratory populations with selection experiments in recently introduced ones. It is not clear how one could disentangle the causes of possible differences from the results of such disparate studies. Furthermore, from first principles and extant experimental studies, we expect a conflation of evolutionary effects in the recently introduced populations because of adaptation to the laboratory environment, and because of genetic and evolutionary disequilibrium. In particular, interactions between adaptation to the general laboratory environment and any particular selective regime under study could be a source of unresolvable evolutionary outcomes, as we will now explain.Two evolutionary processes are at work in the transition from the wild to the laboratory. First, placing a population in a novel environment can cause a change in genetic variances and covariances between traits, as a result of genotype-by-environment interactions. Second, continued maintenance in this novel environment might bring about evolutionary change, perhaps because of new selection pressures or changes in breeding structure. A recently founded laboratory population will thus be in a ‘no man’s land’. We cannot use it to provide information about the original wild population, nor can we test evolutionary models that rely on the assumption that the newly transplanted population is near genetic or selective equilibrium. Surprisingly, like Harshman and Hoffmann, several recent studies have essentially repeated these mistakes7xFluctuating asymmetry, body size and sexual selection in the dung fly Sepsis cynipsea – testing the good genes assumptions and predictions. Blanckenhorn, W.U. et al. J. Evol. Biol. 1998; 11: 735–753Crossref | Scopus (59)See all References, 8xQuantitative genetics of the dung fly Sepsis cynipsea: Cheverud’s conjecture revisited. Reusch, T. and Blanckenhorn, W.U. Heredity. 1998; 81: 111–119CrossrefSee all References, 9xTrade-offs between melanization, development time and adult size in Inachis io and Araschnia levana (Lepidoptera: Nymphalidae)?. Windig, J.J. Heredity. 1999; 82: 57–68CrossrefSee all References.Let us conclude with an example. The empirical challenge posed by the transition from wild to laboratory conditions led us to study the evolution of a newly founded laboratory population of Drosophila subobscura10xAdaptation to the laboratory environment in Drosophila subobscura. Matos, M. et al. J. Evol. Biol. 2000; 13: 9–19Crossref | Scopus (48)See all References10. We found that adaptation to the novel, laboratory environment occurred at a relatively fast rate. As an illustration, fecundity around the age of reproduction increased steadily in the generations after establishment in the laboratory, showing convergence to the values of a long-established population serving as a control (maintained in the lab for 24 generations before the foundation of the new one); the fecundity of the new population became similar to that of the long-established population after just 14 generations of adaptation to the laboratory. In this no man’s land between the wild and the laboratory, the population evolved extremely rapidly. Instead of straining for dubious interpretations of the uncertain results afforded by studies of recently sampled populations, we might use the gap between the wild and the laboratory as an evolutionary tool – recognizing that, after all, the lab is just another environment to which populations adapt, albeit a very peculiar one10xAdaptation to the laboratory environment in Drosophila subobscura. Matos, M. et al. J. Evol. Biol. 2000; 13: 9–19Crossref | Scopus (48)See all References10. To this extent, we can agree with Harshman and Hoffmann.

Laboratory Selection Quickly Erases Historical Differentiation

The roles of history, chance and selection have long been debated in evolutionary biology. Though uniform selection is expected to lead to convergent evolution between populations, contrasting histories and chance events might prevent them from attaining the same adaptive state, rendering evolution somewhat unpredictable. The predictability of evolution has been supported by several studies documenting repeatable adaptive radiations and convergence in both nature and laboratory. However, other studies suggest divergence among populations adapting to the same environment. Despite the relevance of this issue, empirical data is lacking for real-time adaptation of sexual populations with deeply divergent histories and ample standing genetic variation across fitness-related traits. Here we analyse the real-time evolutionary dynamics of Drosophila subobscura populations, previously differentiated along the European cline, when colonizing a new common environment. By analysing several life-history, physiological and morphological traits, we show that populations quickly converge to the same adaptive state through different evolutionary paths. In contrast with other studies, all analysed traits fully converged regardless of their association with fitness. Selection was able to erase the signature of history in highly differentiated populations after just a short number of generations, leading to consistent patterns of convergent evolution.

What is Aging

In 1991, the book Evolutionary Biology of Aging offered the following definition of aging: a persistent decline in the age-specific fitness components of an organism due to internal physiological deterioration (Rose, 1991). This definition has since been used by others a number of times. However, it was only a modest generalization of a definition proffered by Alex Comfort over three editions (1956–1979) of his key book The Biology of Senescence (Comfort, 1979): “a progressive increase throughout life, or after a given stadium, in the likelihood that a given individual will die, during the next succeeding unit of time, from randomly distributed causes.” The 1991 definition chiefly added reproductive fitness components to Comforts definition, while adding the qualifiers that the fitness-component decline should be persistent and should be “due to internal physiological deterioration,” where the latter phrase was meant fairly broadly. Thus increases in mortality with age due to chronic infections such as HIV/AIDS were excluded by the 1991 definition.