Shedding light on the evolution of plasticity in natural populations

Plasticity allows for changes in phenotype in response to environmental cues, often facilitating local adaptation to seasonal environments. Phenotypic plasticity alone, however, may not always be sufficient to ensure adaptation to new localities. In particular, changing cues associated with shifting seasonal regimes may no longer induce appropriate phenotypic responses in new environments ( Nicotra et al. 2010 ). Plastic responses must thus evolve to avoid being maladaptive. To date, the extent to which plastic responses can change and the genetic mechanisms by which this can happen have remained elusive. In this issue of Molecular Ecology, Blackman et al. (2011a) harness natural variation in flowering time among populations of the wild sunflower, Helianthus annuus, to demonstrate that plasticity has indeed evolved in this species. Remarkably, they are able to detect changes in gene expression that are associated with both a loss of plasticity and a reversal of the plastic response. These changes occur in two separate, but integrated, regulatory pathways controlling the transition to flowering, suggesting that complex regulatory networks that incorporate multiple environmental and developmental cues may facilitate the evolution of plastic responses. This study leverages knowledge from plant genetic models to provide a surprising level of insight into the evolution of an adaptive trait in a non‐model species. Through discoveries of the roles of gene duplication and network modularity in the evolution of plastic responses, the study raises questions about the degree to which species‐specific network architectures may act as a constraint to the potential of adaptation.     

What paths do advantageous alleles take during short‐term evolutionary change?

Combining experimental evolution with whole‐genome resequencing is a promising new strategy for investigating the dynamics of evolutionary change. Published studies that have resequenced laboratory‐selected populations of sexual organisms have typically focused on populations sampled at the end of an evolution experiment. These studies have attempted to associate particular alleles with phenotypic change and attempted to distinguish between different theoretical models of adaptation. However, neither the population used to initiate the experiment nor multiple time points sampled during the evolutionary trajectory are generally available for examination. In this issue of Molecular Ecology, Orozco‐terWengel et al. (2012) take a significant step forward by estimating genome‐wide allele frequencies at the start, 15 generations into and at the end of a 37‐generation Drosophila experimental evolution study. The authors identify regions of the genome that have responded to laboratory selection and describe the temporal dynamics of allele frequency change. They identify two common trajectories for putatively adaptive alleles: alleles either gradually increase in frequency throughout the entire 37 generations or alleles plateau at a new frequency by generation 15. The identification of complex trajectories of alleles under selection contributes to a growing body of literature suggesting that simple models of adaptation, whereby beneficial alleles arise and increase in frequency unimpeded until they become fixed, may not adequately describe short‐term response to selection.     

Somatic mutations as a useful tool for studying clonal dynamics in trees

The seemingly eternal cycles of clonal growth in many tree species, with members of Populus (aspen, poplars, cottonwoods and the like) featuring most prominently, provoke a number of questions on the interface between ecology, genetics and forestry. In this issue, two groups present their approaches to clonal dynamics ( Ally et al. 2008 and Mock et al. 2008 ), using microsatellite (or simple sequence repeat, SSR) variation in P. tremuloides. Ally et al. developed and applied a model for using microsatellites to estimate clone age and infer other community characteristics. Mock et al. used fewer microsatellites but in more individuals, to examine clone size and distribution across the landscape.     

Pushing north one bottleneck at a time: site frequency spectra tell the history of Sitka spruce

Reconstructing the history of populations is a longstanding goal of molecular ecologists. In addition to a better understanding of the past, it is hoped that this knowledge would also facilitate predictions regarding species’ responses to future events such as climate change. The traditional way of doing this is through the fossil record, but these historical records are often incomplete. Inferring historical demography from patterns of nucleotide variability can help to fill these gaps. In this issue of Molecular Ecology, Holliday et al. (2010) glimpse into the demographic past of Sitka spruce, Picea sitchensis, an economically and ecologically important species native to northwestern United States and Canada, by examining the site frequency spectrum (SFS) of 153 loci in six populations covering the species entire range.     

Genetic diversity of small populations: Not always “doom and gloom”?

Is a key theory of evolutionary and conservation biology—that loss of genetic diversity can be predicted from population size—on shaky ground? In the face of increasing human‐induced species depletion and habitat fragmentation, this question and the study of genetic diversity in small populations are paramount to understanding the limits of species’ responses to environmental change and to providing remedies to endangered species conservation. Few empirical studies have investigated to what degree some small populations might be buffered against losses of genetic diversity. Even fewer studies have experimentally tested the potential underlying mechanisms. The study of Schou, Loeschcke, Bechsgaard, Schlotterer, and Kristensen ( 2017 ) in this issue of Molecular Ecology is elegant in combining classic common garden experimentation with population genomics on an iconic experimental model species (Drosophila melanogaster). The authors reveal a slower rate of loss of genetic diversity in small populations under varying thermal regimes than theoretically expected and hence an unexpected retention of genetic diversity. They are further able to hone in on a plausible mechanism: associative overdominance, wherein homozygosity of deleterious recessive alleles is especially disfavoured in genomic regions of low recombination. These results contribute to a budding literature on the varying mechanisms underlying genetic diversity in small populations and encourage further such research towards the effective management and conservation of fragmented or endangered populations.     

Individual-based analysis opens new insights into understanding population structure and animal behaviour

Studying the movement of individuals in the wild has always been a challenge in ecology. However, estimating such movement is essential in life sciences as it is the base-line for evaluating connectivity, a major component in developing management and conservation plans. Furthermore, movement, or migration, is an essential parameter in population genetics, as it directly affects genetic differentiation. The development of highly variable markers has allowed genetic discrimination between individuals within populations and at larger scales, and the availability of high-throughput technologies means that many samples and hence many individuals can be screened. These advances mean that we can now use genetic identification for tracking individuals, and hence follow both survival and reproductive output through the life cycle. The paper by Morrissey & Ferguson (2011, this issue) is a demonstration of this new capability, as authors were able to infer the movement of salmonid fish initially captured as juveniles, and later as reproductively mature adults.     

Predicting epistasis: an experimental test of metabolic control theory with bacterial transcription and translation

Epistatic interactions between mutations are thought to play a crucial role in a number of evolutionary processes, including adaptation and sex. Evidence for epistasis is abundant, but tests of general theoretical models that can predict epistasis are lacking. In this study, I test the ability of metabolic control theory to predict epistasis using a novel experimental approach that combines phenotypic and genetic perturbations of enzymes involved in gene expression and protein synthesis in the bacterium Pseudomonas aeruginosa. These experiments provide experimental support for two key predictions of metabolic control theory: (i) epistasis between genes involved in the same pathway is antagonistic; (ii) epistasis becomes increasingly antagonistic as mutational severity increases. Metabolic control theory is a general theory that applies to any set of genes that are involved in the same linear processing chain, not just metabolic pathways, and I argue that this theory is likely to have important implications for predicting epistasis between functionally coupled genes, such as those involved in antibiotic resistance. Finally, this study highlights the fact that phenotypic manipulations of gene activity provide a powerful method for studying epistasis that complements existing genetic methods.     

Contemporary cryptic sexuality in Trypanosoma cruzi

Clonal propagation is considered to be the predominant mode of reproduction among many parasitic protozoa. However, this assumption may overlook unorthodox, infrequent or cryptic sexuality. Trypanosoma cruzi, which causes Chagas disease, is known to undergo non‐Mendelian genetic exchange in the laboratory. In the field, evidence of extant genetic exchange is limited. In this study, we undertook intensive sampling of T. cruzi Discrete Typing Unit I in endemic eastern Colombia. Using Fluorescence‐activated cell sorting, we generated 269 biological clones from 67 strains. Each clone was genotyped across 24 microsatellite loci. Subsequently, 100 representative clones were typed using 10 mitochondrial sequence targets (3.76 Kbp total). Clonal diversity among humans, reservoir hosts and vectors suggested complex patterns of superinfection and/or coinfection in oral and vector‐borne Chagas disease cases. Clonal diversity between mother and foetus in a congenital case demonstrates that domestic TcI genotypes are infective in utero. Importantly, gross incongruence between nuclear and mitochondrial markers is strong evidence for widespread genetic exchange throughout the data set. Furthermore, a confirmed mosaic maxicircle sequence suggests intermolecular recombination between individuals as a further mechanism of genetic reassortment. Finally, robust dating based on mitochondrial DNA indicates that the emergence of a widespread domestic TcI clade that we now name TcI_DOM (formerly TcIa/VEN_Dom) occurred 23 000 ± 12 000 years ago and was followed by population expansion, broadly corresponding with the earliest human migration into the Americas.