Josiane Santos

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.

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.

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.

Fast evolutionary genetic differentiation during experimental colonizations

Founder effects during colonization of a novel environment are expected to change the genetic composition of populations, leading to differentiation between the colonizer population and its source population. Another expected outcome is differentiation among populations derived from repeated independent colonizations starting from the same source. We have previously detected significant founder effects affecting rate of laboratory adaptation among Drosophila subobscura laboratory populations derived from the wild. We also showed that during the first generations in the laboratory, considerable genetic differentiation occurs between foundations. The present study deepens that analysis, taking into account the natural sampling hierarchy of six foundations, derived from different locations, different years and from two samples in one of the years. We show that striking stochastic effects occur in the first two generations of laboratory culture, effects that produce immediate differentiation between foundations, independent of the source of origin and despite similarity among all founders. This divergence is probably due to powerful genetic sampling effects during the first few generations of culture in the novel laboratory environment, as a result of a significant drop in Ne. Changes in demography as well as high variance in reproductive success in the novel environment may contribute to the low values of Ne. This study shows that estimates of genetic differentiation between natural populations may be accurate when based on the initial samples collected in the wild, though considerable genetic differentiation may occur in the very first generations of evolution in a new, confined environment. Rapid and significant evolutionary changes can thus occur during the early generations of a founding event, both in the wild and under domestication, effects of interest for both scientific and conservation purposes.

Evolution of mating behavior between two populations adapting to common environmental conditions.

Populations from the same species may be differentiated across contrasting environments, potentially affecting reproductive isolation among them. When such populations meet in a novel common environment, this isolation may be modified by biotic or abiotic factors. Curiously, the latter have been overlooked. We filled this gap by performing experimental evolution of three replicates of two populations of Drosophila subobscura adapting to a common laboratorial environment, and simulated encounters at three time points during this process. Previous studies showed that these populations were highly differentiated for several life-history traits and chromosomal inversions. First, we show initial differentiation for some mating traits, such as assortative mating and male mating rate, but not others (e.g., female mating latency). Mating frequency increased during experimental evolution in both sets of populations. The assortative mating found in one population remained constant throughout the adaptation process, while disassortative mating of the other population diminished across generations. Additionally, differences in male mating rate were sustained across generations. This study shows that mating behavior evolves rapidly in response to adaptation to a common abiotic environment, although with a complex pattern that does not correspond to the quick convergence seen for life-history traits.

Tracking changes in chromosomal arrangements and their genetic content during adaptation

There is considerable evidence for an adaptive role of inversions, but how their genetic content evolves and affects the subsequent evolution of chromosomal polymorphism remains controversial. Here, we track how life‐history traits, chromosomal arrangements and 22 microsatellites, within and outside inversions, change in three replicated populations of Drosophila subobscura for 30 generations of laboratory evolution since founding from the wild. The dynamics of fitness‐related traits indicated adaptation to the new environment concomitant with directional evolution of chromosomal polymorphism. Evidence of selective changes in frequency of inversions was obtained for seven of 23 chromosomal arrangements, corroborating a role for inversions in adaptation. The evolution of linkage disequilibrium between some microsatellites and chromosomes suggested that adaptive changes in arrangements involved changes in their genetic content. Several microsatellite alleles increased in frequency more than expected by drift in targeted inversions in all replicate populations. In particular, there were signs of selection in the O3+4 arrangement favouring a combination of alleles in two loci linked to the inversion and changing along with it, although the lack of linkage disequilibrium between these loci precludes epistatic selection. Seven other alleles increased in frequency within inversions more than expected by drift, but were not in linkage disequilibrium with them. Possibly these alleles were hitchhiking along with alleles under selection that were not specific to those inversions. Overall, the selection detected on the genetic content of inversions, despite limited coverage of the genome, suggests that genetic changes within inversions play an important role in adaptation.

Playing Darwin. Part B. 20 years of domestication in Drosophila subobscura

Adaptation to a new environment (as well as its underlying mechanisms) is one of the most important topics in Evolutionary Biology. Understanding the adaptive process of natural populations to captivity is essential not only in general evolutionary studies but also in conservation programmes. Since 1990, the Group of Experimental Evolution (CBA/FCUL) has been performing long-term, real-time evolutionary studies, with the characterization of laboratory adaptation in populations of Drosophila subobscura founded in different times and from different locations. Initially, these experiments involved phenotypic assays and more recently were expanded to studies at the molecular level (microsatellite and chromosomal polymorphisms) and with different population sizes. Throughout these two decades, a clear pattern of evolutionary convergence to long-established laboratory populations has been consistently observed in several life-history traits. However, contingencies across foundations were also found during the adaptive process. In characters with complex evolutionary trajectories, the data suggested that the comparative method lacked predictive capacity relative to real-time evolutionary trajectories (experimental evolution). Microsatellite analysis revealed general similarity in gene diversity and allele number between studied populations, as well as an unclear association between genetic variability and evolutionary potential. Nevertheless, ongoing studies in all foundations are being carried out to further test this hypothesis. A comparison between recently introduced and long-term populations (founded from the same natural location) has shown higher degree of chromosomal polymorphism in recent ones. Finally, our findings suggest higher heterogeneity between small-sized populations, as well as a slower evolutionary rate in characters close to fitness (such as fecundity and mating behaviour). This comprehensive study is aimed at better understanding the processes and patterns underlying adaptation to captivity, as well as its genetic basis.

History, chance and selection during phenotypic and genomic experimental evolution: replaying the tape of life at different levels.

Ever since Darwin, understanding evolutionary processes and patterns have been major scientific quests. In the Origin of Species, Darwin explained both adaptation and diversity, and most of his arguments were based on indirect evidence, including comparative approaches. These findings led Darwin to defend that evolution in nature is extremely slow and gradual, hardly being directly observable at the scale of a human generation. Artificial selection, in contrast, was used by Darwin to illustrate the efficacy of natural selection (Darwin, 1859). During the last decades, evolution has been observed in real time. This opened new research possibilities and gave rise to Experimental Evolution, a rapidly expanding field that covers many topics and organisms (Garland and Rose, 2009; Kawecki et al., 2012). The joint power of experimental evolution and recently developed genome-wide tools may now lead us a step further in understanding real-time evolutionary dynamics of populations, both at phenotypic and genomic levels (Baldwin-Brown et al., 2014; Schlotterer et al., 2014). Our contribution to this special issue of Frontiers in Genetics focuses on the power of these approaches to assess the role of historical contingencies during adaptation to novel environments, a fundamental subject that has been neglected.