scholarly journals Polygenic adaptation fuels genetic redundancy in Drosophila

2018 ◽  
Author(s):  
Neda Barghi ◽  
Raymond Tobler ◽  
Viola Nolte ◽  
Ana Marija Jaksic ◽  
Francois Mallard ◽  
...  

AbstractThe genetic architecture of adaptive traits is of key importance to predict evolutionary responses. Most adaptive traits are polygenic – i.e. result from selection on a large number of genetic loci – but most molecularly characterized traits have a simple genetic basis. This discrepancy is best explained by the difficulty in detecting small allele frequency changes across many contributing loci. To resolve this, we use laboratory natural selection, a framework that is powerful enough to detect signatures for selective sweeps and polygenic adaptation. We exposed 10 replicates of a Drosophila simulans population to a new temperature regime and uncovered a polygenic architecture of an adaptive trait with high genetic redundancy among adaptive alleles. We observed convergent phenotypic responses, e.g. fitness, metabolic rate and fat content, and a strong polygenic response (99 selected alleles; mean s=0.061). However, each of these selected alleles increased in frequency only in a subset of the evolving replicates. Our results show that natural D. simulans populations harbor a vast reservoir of adaptive variation facilitating rapid evolutionary responses. The observed genetic redundancy potentiates this genotypic variation through multiple genetic pathways leading to phenotypic convergence. This key property of adaptive alleles requires the modification of testing strategies in natural populations beyond the search for convergence on the molecular level.

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 21 (1) ◽  
Author(s):  
Cory A. Berger ◽  
Michael S. Brewer ◽  
Nobuaki Kono ◽  
Hiroyuki Nakamura ◽  
Kazuharu Arakawa ◽  
...  

Abstract Background A striking aspect of evolution is that it often converges on similar trajectories. Evolutionary convergence can occur in deep time or over short time scales, and is associated with the imposition of similar selective pressures. Repeated convergent events provide a framework to infer the genetic basis of adaptive traits. The current study examines the genetic basis of secondary web loss within web-building spiders (Araneoidea). Specifically, we use a lineage of spiders in the genus Tetragnatha (Tetragnathidae) that has diverged into two clades associated with the relatively recent (5 mya) colonization of, and subsequent adaptive radiation within, the Hawaiian Islands. One clade has adopted a cursorial lifestyle, and the other has retained the ancestral behavior of capturing prey with sticky orb webs. We explore how these behavioral phenotypes are reflected in the morphology of the spinning apparatus and internal silk glands, and the expression of silk genes. Several sister families to the Tetragnathidae have undergone similar web loss, so we also ask whether convergent patterns of selection can be detected in these lineages. Results The cursorial clade has lost spigots associated with the sticky spiral of the orb web. This appears to have been accompanied by loss of silk glands themselves. We generated phylogenies of silk proteins (spidroins), which showed that the transcriptomes of cursorial Tetragnatha contain all major spidroins except for flagelliform. We also found an uncharacterized spidroin that has higher expression in cursorial species. We found evidence for convergent selection acting on this spidroin, as well as genes involved in protein metabolism, in the cursorial Tetragnatha and divergent cursorial lineages in the families Malkaridae and Mimetidae. Conclusions Our results provide strong evidence that independent web loss events and the associated adoption of a cursorial lifestyle are based on similar genetic mechanisms. Many genes we identified as having evolved convergently are associated with protein synthesis, degradation, and processing, which are processes that play important roles in silk production. This study demonstrates, in the case of independent evolution of web loss, that similar selective pressures act on many of the same genes to produce the same phenotypes and behaviors.


2016 ◽  
Vol 14 (3) ◽  
pp. e07SC01 ◽  
Author(s):  
Junqiang Ding ◽  
Jinliang Ma ◽  
Jiafa Chen ◽  
Tangshun Ai ◽  
Zhimin Li ◽  
...  

Barren tip on corn ear is an important agronomic trait in maize, which is highly associated with grain yield. Understanding the genetic basis of tip-barrenness may help to reduce the ear tip-barrenness in breeding programs. In this study, ear tip-barrenness was evaluated in two environments in a F2:3 population, and it showed significant genotypic variation for ear tip-barrenness in both environments. Using mixed-model composite interval mapping method, three additive effects quantitative trait loci (QTL) for ear tip-barrenness were mapped on chromosomes 2, 3 and 6, respectively. They explained 16.6% of the phenotypic variation, and no significant QTL × Environment interactions and digenic interactions were detected. The results indicated that additive effect was the main genetic basis for ear tip-barrenness in maize. This is the first report of QTL mapped for ear tip-barrenness in maize.


2020 ◽  
Vol 60 (2) ◽  
pp. 318-331
Author(s):  
April D Garrett ◽  
Reid S Brennan ◽  
Anya L Steinhart ◽  
Aubrey M Pelletier ◽  
Melissa H Pespeni

Synopsis Environmental variation experienced by a species across space and time can promote the maintenance of genetic diversity that may be adaptive in future global change conditions. Selection experiments have shown that purple sea urchin, Strongylocentrotus purpuratus, populations have adaptive genetic variation for surviving pH conditions at the “edge” (pH 7.5) of conditions experienced in nature. However, little is known about whether populations have genetic variation for surviving low-pH events beyond those currently experienced in nature or how variation in pH conditions affects organismal and genetic responses. Here, we quantified survival, growth, and allele frequency shifts in experimentally selected developing purple sea urchin larvae in static and variable conditions at three pH levels: pH 8.1 (control), pH 7.5 (edge-of-range), and pH 7.0 (extreme). Variable treatments recovered body size relative to static treatments, but resulted in higher mortality, suggesting a potential tradeoff between survival and growth under pH stress. However, within each pH level, allele frequency changes were overlapping between static and variable conditions, suggesting a shared genetic basis underlying survival to mean pH regardless of variability. In contrast, genetic responses to pH 7.5 (edge) versus pH 7.0 (extreme) conditions were distinct, indicating a unique genetic basis of survival. In addition, loci under selection were more likely to be in exonic regions than regulatory, indicating that selection targeted protein-coding variation. Loci under selection in variable pH 7.5 conditions, more similar to conditions periodically experienced in nature, performed functions related to lipid biosynthesis and metabolism, while loci under selection in static pH 7.0 conditions performed functions related to transmembrane and mitochondrial processes. While these results are promising in that purple sea urchin populations possess genetic variation for surviving extreme pH conditions not currently experienced in nature, they caution that increased acidification does not result in a linear response but elicits unique physiological stresses and survival mechanisms.


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.


2000 ◽  
Vol 90 (1) ◽  
pp. 3-7 ◽  
Author(s):  
J.A. McKenzie

AbstractIn this critique it is argued that the genetic basis of the evolution of resistance is dependent on how the phenotypic, and underlying genotypic, variation is channelled during a selective response. A polygenic response is preferentially favoured if selection acts within the phenotypic distribution of susceptibles; a monogenic response is predicted if selection screens rare mutations with phenotypes outside that susceptible distribution. The relevance of this model to the method of genetic analysis, the prediction of resistance mechanisms to novel insecticides, the generation of resistant beneficial insects and the development of the most effective resistance and integrated pest management programmes is discussed.


2012 ◽  
Vol 279 (1747) ◽  
pp. 4551-4558 ◽  
Author(s):  
William E. Bradshaw ◽  
Kevin J. Emerson ◽  
Julian M. Catchen ◽  
William A. Cresko ◽  
Christina M. Holzapfel

Identifying regions of the genome contributing to phenotypic evolution often involves genetic mapping of quantitative traits. The focus then turns to identifying regions of ‘major’ effect, overlooking the observation that traits of ecological or evolutionary relevance usually involve many genes whose individual effects are small but whose cumulative effect is large. Herein, we use the power of fully interfertile natural populations of a single species of mosquito to develop three quantitative trait loci (QTL) maps: one between two post-glacially diverged populations and two between a more ancient and a post-glacial population. All demonstrate that photoperiodic response is genetically a highly complex trait. Furthermore, we show that marker regressions identify apparently ‘non-significant’ regions of the genome not identified by composite interval mapping, that the perception of the genetic basis of adaptive evolution is crucially dependent upon genetic background and that the genetic basis for adaptive evolution of photoperiodic response is highly variable within contemporary populations as well as between anciently diverged populations.


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