scholarly journals Highly parallel genomic selection response in replicated Drosophila melanogaster populations with reduced genetic variation

2021 ◽  
Author(s):  
Claire Burny ◽  
Viola Nolte ◽  
Marlies Dolezal ◽  
Christian Schl&oumltterer

Many adaptive traits are polygenic and frequently more loci contributing to the phenotype than needed are segregating in populations to express a phenotypic optimum. Experimental evolution provides a powerful approach to study polygenic adaptation using replicated populations adapting to a new controlled environment. Since genetic redundancy often results in non-parallel selection responses among replicates, we propose a modified Evolve and Resequencing (E&R) design that maximizes the similarity among replicates. Rather than starting from many founders, we only use two inbred Drosophila melanogaster strains and expose them to a very extreme, hot temperature environment (29°C). After 20 generations, we detect many genomic regions with a strong, highly parallel selection response in 10 evolved replicates. The X chromosome has a more pronounced selection response than the autosomes, which may be attributed to dominance effects. Furthermore, we find that the median selection coefficient for all chromosomes is higher in our two-genotype experiment than in classic E&R studies. Since two random genomes harbor sufficient variation for adaptive responses, we propose that this approach is particularly well-suited for the analysis of polygenic adaptation.


Author(s):  
Wei-Yun Lai ◽  
Christian Schlötterer

AbstractShifts in trait means are widely considered as evidence for adaptive responses, but the impact on phenotypic variance remains largely unexplored. Here, we studied gene expression variance of Drosophila simulans males before and after 100 generations of adaptation to a novel hot laboratory environment. In each of the two independently evolved replicate populations the variance of about 150 genes changed significantly (mostly reduction). Although different genes were affected in both replicates, these genes are related to digestion in the gut. This non-parallel selection response on the gene level in combination with a convergent response at a higher phenotypic level reflects genetic redundancy, a characteristic hallmark of polygenic adaptation. We propose that the constant and simple food source in the laboratory resulted in selection for reduced variance in digestive genes. In natural populations adaptation to diverse types of food may be beneficial, resulting in higher phenotypic variance. This empirical evidence of phenotypic variance being the direct target of selection during adaptation has important implications for strategies to identify selection signatures.



2021 ◽  
Vol 12 (1) ◽  
Author(s):  
Belinda van Heerwaarden ◽  
Carla M. Sgrò

AbstractForecasting which species/ecosystems are most vulnerable to climate warming is essential to guide conservation strategies to minimize extinction. Tropical/mid-latitude species are predicted to be most at risk as they live close to their upper critical thermal limits (CTLs). However, these assessments assume that upper CTL estimates, such as CTmax, are accurate predictors of vulnerability and ignore the potential for evolution to ameliorate temperature increases. Here, we use experimental evolution to assess extinction risk and adaptation in tropical and widespread Drosophila species. We find tropical species succumb to extinction before widespread species. Male fertility thermal limits, which are much lower than CTmax, are better predictors of species’ current distributions and extinction in the laboratory. We find little evidence of adaptive responses to warming in any species. These results suggest that species are living closer to their upper thermal limits than currently presumed and evolution/plasticity are unlikely to rescue populations from extinction.



2021 ◽  
Author(s):  
Mark Phillips ◽  
Kenneth R. Arnold ◽  
Zer Vue ◽  
Heather Beasley ◽  
Edgar Garza Lopez ◽  
...  

Experimental evolution with Drosophila melanogaster has been used extensively for decades to study aging and longevity. In recent years, the addition of DNA and RNA sequencing to this framework has allowed researchers to leverage the statistical power inherent to experimental evolution study the genetic basis of longevity itself. Here we incorporated metabolomic data into to this framework to generate even deeper insights into the physiological and genetic mechanisms underlying longevity differences in three groups of experimentally evolved D. melanogaster populations with different aging and longevity patterns. Our metabolomic analysis found that aging alters mitochondrial metabolism through increased consumption of NAD+ and increased usage of the TCA cycle. Combining our genomic and metabolomic data produced a list of biologically relevant candidate genes. Among these candidates, we found significant enrichment for genes and pathways associated with neurological development and function, and carbohydrate metabolism. While we do not explicitly find enrichment for aging canonical genes, neurological dysregulation and carbohydrate metabolism are both known to be associated with accelerated aging and reduced longevity. Taken together, our results in total provide very plausible genetic mechanisms for what might be driving longevity differences in this experimental system. More broadly, our findings demonstrate the value of combining multiple types of omic data with experimental evolution when attempting to dissect mechanisms underlying complex and highly polygenic traits like aging.



2019 ◽  
Author(s):  
Pedro Gaspar ◽  
Saad Arif ◽  
Lauren Sumner-Rooney ◽  
Maike Kittelmann ◽  
Andrew J. Bodey ◽  
...  

AbstractThe compound eyes of insects exhibit striking variation in size, reflecting adaptation to different lifestyles and habitats. However, the genetic and developmental bases of variation in insect eye size is poorly understood, which limits our understanding of how these important morphological differences evolve. To address this, we further explored natural variation in eye size within and between four species of the Drosophila melanogaster species subgroup. We found extensive variation in eye size among these species, and flies with larger eyes generally had a shorter inter-ocular distance and vice versa. We then carried out quantitative trait loci (QTL) mapping of intra-specific variation in eye size and inter-ocular distance in both D. melanogaster and D. simulans. This revealed that different genomic regions underlie variation in eye size and inter-ocular distance in both species, which we corroborated by introgression mapping in D. simulans. This suggests that although there is a trade-off between eye size and inter-ocular distance, variation in these two traits is likely to be caused by different genes and so can be genetically decoupled. Finally, although we detected QTL for intra-specific variation in eye size at similar positions in D. melanogaster and D. simulans, we observed differences in eye fate commitment between strains of these two species. This indicates that different developmental mechanisms and therefore, most likely, different genes contribute to eye size variation in these species. Taken together with the results of previous studies, our findings suggest that the gene regulatory network that specifies eye size has evolved at multiple genetic nodes to give rise to natural variation in this trait within and among species.



2015 ◽  
Vol 112 (43) ◽  
pp. 13284-13289 ◽  
Author(s):  
Geir H. Bolstad ◽  
Jason A. Cassara ◽  
Eladio Márquez ◽  
Thomas F. Hansen ◽  
Kim van der Linde ◽  
...  

Precise exponential scaling with size is a fundamental aspect of phenotypic variation. These allometric power laws are often invariant across taxa and have long been hypothesized to reflect developmental constraints. Here we test this hypothesis by investigating the evolutionary potential of an allometric scaling relationship in drosophilid wing shape that is nearly invariant across 111 species separated by at least 50 million years of evolution. In only 26 generations of artificial selection in a population of Drosophila melanogaster, we were able to drive the allometric slope to the outer range of those found among the 111 sampled species. This response was rapidly lost when selection was suspended. Only a small proportion of this reversal could be explained by breakup of linkage disequilibrium, and direct selection on wing shape is also unlikely to explain the reversal, because the more divergent wing shapes produced by selection on the allometric intercept did not revert. We hypothesize that the reversal was instead caused by internal selection arising from pleiotropic links to unknown traits. Our results also suggest that the observed selection response in the allometric slope was due to a component expressed late in larval development and that variation in earlier development did not respond to selection. Together, these results are consistent with a role for pleiotropic constraints in explaining the remarkable evolutionary stability of allometric scaling.



eLife ◽  
2019 ◽  
Vol 8 ◽  
Author(s):  
João PL Castro ◽  
Michelle N Yancoskie ◽  
Marta Marchini ◽  
Stefanie Belohlavy ◽  
Layla Hiramatsu ◽  
...  

Evolutionary studies are often limited by missing data that are critical to understanding the history of selection. Selection experiments, which reproduce rapid evolution under controlled conditions, are excellent tools to study how genomes evolve under selection. Here we present a genomic dissection of the Longshanks selection experiment, in which mice were selectively bred over 20 generations for longer tibiae relative to body mass, resulting in 13% longer tibiae in two replicates. We synthesized evolutionary theory, genome sequences and molecular genetics to understand the selection response and found that it involved both polygenic adaptation and discrete loci of major effect, with the strongest loci tending to be selected in parallel between replicates. We show that selection may favor de-repression of bone growth through inactivating two limb enhancers of an inhibitor, Nkx3-2. Our integrative genomic analyses thus show that it is possible to connect individual base-pair changes to the overall selection response.



2015 ◽  
Vol 186 (5) ◽  
pp. 582-593 ◽  
Author(s):  
Vanessa Kellermann ◽  
Ary A. Hoffmann ◽  
Torsten Nygaard Kristensen ◽  
Neda Nasiri Moghadam ◽  
Volker Loeschcke


PLoS Biology ◽  
2019 ◽  
Vol 17 (2) ◽  
pp. e3000128 ◽  
Author(s):  
Neda Barghi ◽  
Raymond Tobler ◽  
Viola Nolte ◽  
Ana Marija Jakšić ◽  
François Mallard ◽  
...  


2020 ◽  
Vol 12 (6) ◽  
pp. 890-904 ◽  
Author(s):  
Neda Barghi ◽  
Christian Schlötterer

Abstract In molecular population genetics, adaptation is typically thought to occur via selective sweeps, where targets of selection have independent effects on the phenotype and rise to fixation, whereas in quantitative genetics, many loci contribute to the phenotype and subtle frequency changes occur at many loci during polygenic adaptation. The sweep model makes specific predictions about frequency changes of beneficial alleles and many test statistics have been developed to detect such selection signatures. Despite polygenic adaptation is probably the prevalent mode of adaptation, because of the traditional focus on the phenotype, we are lacking a solid understanding of the similarities and differences of selection signatures under the two models. Recent theoretical and empirical studies have shown that both selective sweep and polygenic adaptation models could result in a sweep-like genomic signature; therefore, additional criteria are needed to distinguish the two models. With replicated populations and time series data, experimental evolution studies have the potential to identify the underlying model of adaptation. Using the framework of experimental evolution, we performed computer simulations to study the pattern of selected alleles for two models: 1) adaptation of a trait via independent beneficial mutations that are conditioned for fixation, that is, selective sweep model and 2) trait optimum model (polygenic adaptation), that is adaptation of a quantitative trait under stabilizing selection after a sudden shift in trait optimum. We identify several distinct patterns of selective sweep and trait optimum models in populations of different sizes. These features could provide the foundation for development of quantitative approaches to differentiate the two models.



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