scholarly journals The adaptive architecture is shaped by population ancestry and not by selection regime

2020 ◽  
Author(s):  
Kathrin A. Otte ◽  
Viola Nolte ◽  
François Mallard ◽  
Christian Schlötterer

AbstractUnderstanding the genetic architecture of adaptive phenotypes is a key question in evolutionary biology. One particularly promising approach is Evolve and Resequence (E&R), which combines advantages of experimental evolution such as time series, replicate populations and controlled environmental conditions, with whole genome sequencing. The recent analysis of replicate populations from two different Drosophila simulans founder populations, which were adapting to the same novel hot environment, uncovered very different architectures - either many selection targets with large heterogeneity among replicates or fewer selection targets with a consistent response among replicates. Here, we exposed the founder population from Portugal to a cold temperature regime. Although almost no selection targets were shared between the hot and cold selection regime, the adaptive architecture was similar: we identified a moderate number of loci under strong selection (19 selected alleles, mean selection coefficient = 0.072) and very parallel responses in the cold evolved replicates. This similarity across different environments indicates that the adaptive architecture depends more on the ancestry of the founder population than the specific selection regime. These observations have a pronounced impact on our understanding of adaptation in natural populations.

2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Kathrin A. Otte ◽  
Viola Nolte ◽  
François Mallard ◽  
Christian Schlötterer

Abstract Background Understanding the genetic architecture of temperature adaptation is key for characterizing and predicting the effect of climate change on natural populations. One particularly promising approach is Evolve and Resequence, which combines advantages of experimental evolution such as time series, replicate populations, and controlled environmental conditions, with whole genome sequencing. Recent analysis of replicate populations from two different Drosophila simulans founder populations, which were adapting to the same novel hot environment, uncovered very different architectures—either many selection targets with large heterogeneity among replicates or fewer selection targets with a consistent response among replicates. Results Here, we expose the founder population from Portugal to a cold temperature regime. Although almost no selection targets are shared between the hot and cold selection regime, the adaptive architecture was similar. We identify a moderate number of targets under strong selection (19 selection targets, mean selection coefficient = 0.072) and parallel responses in the cold evolved replicates. This similarity across different environments indicates that the adaptive architecture depends more on the ancestry of the founder population than the specific selection regime. Conclusions These observations will have broad implications for the correct interpretation of the genomic responses to a changing climate in natural populations.


Author(s):  
Graham Bell

Darwin insisted that evolutionary change occurs very slowly over long periods of time, and this gradualist view was accepted by his supporters and incorporated into the infinitesimal model of quantitative genetics developed by R. A. Fisher and others. It dominated the first century of evolutionary biology, but has been challenged in more recent years both by field surveys demonstrating strong selection in natural populations and by quantitative trait loci and genomic studies, indicating that adaptation is often attributable to mutations in a few genes. The prevalence of strong selection seems inconsistent, however, with the high heritability often observed in natural populations, and with the claim that the amount of morphological change in contemporary and fossil lineages is independent of elapsed time. I argue that these discrepancies are resolved by realistic accounts of environmental and evolutionary changes. First, the physical and biotic environment varies on all time-scales, leading to an indefinite increase in environmental variance over time. Secondly, the intensity and direction of natural selection are also likely to fluctuate over time, leading to an indefinite increase in phenotypic variance in any given evolving lineage. Finally, detailed long-term studies of selection in natural populations demonstrate that selection often changes in direction. I conclude that the traditional gradualist scheme of weak selection acting on polygenic variation should be supplemented by the view that adaptation is often based on oligogenic variation exposed to commonplace, strong, fluctuating natural selection.


2019 ◽  
Vol 36 (8) ◽  
pp. 1686-1700 ◽  
Author(s):  
Covadonga Vara ◽  
Laia Capilla ◽  
Luca Ferretti ◽  
Alice Ledda ◽  
Rosa A Sánchez-Guillén ◽  
...  

Abstract One of the major challenges in evolutionary biology is the identification of the genetic basis of postzygotic reproductive isolation. Given its pivotal role in this process, here we explore the drivers that may account for the evolutionary dynamics of the PRDM9 gene between continental and island systems of chromosomal variation in house mice. Using a data set of nearly 400 wild-caught mice of Robertsonian systems, we identify the extent of PRDM9 diversity in natural house mouse populations, determine the phylogeography of PRDM9 at a local and global scale based on a new measure of pairwise genetic divergence, and analyze selective constraints. We find 57 newly described PRDM9 variants, this diversity being especially high on Madeira Island, a result that is contrary to the expectations of reduced variation for island populations. Our analysis suggest that the PRDM9 allelic variability observed in Madeira mice might be influenced by the presence of distinct chromosomal fusions resulting from a complex pattern of introgression or multiple colonization events onto the island. Importantly, we detect a significant reduction in the proportion of PRDM9 heterozygotes in Robertsonian mice, which showed a high degree of similarity in the amino acids responsible for protein–DNA binding. Our results suggest that despite the rapid evolution of PRDM9 and the variability detected in natural populations, functional constraints could facilitate the accumulation of allelic combinations that maintain recombination hotspot symmetry. We anticipate that our study will provide the basis for examining the role of different PRDM9 genetic backgrounds in reproductive isolation in natural populations.


1990 ◽  
Vol 36 ◽  
pp. 567-579 ◽  

Sewall Wright's active life spanned the development of genetics from a new discipline when the principles of inheritance were still being elucidated to the technology of recombinant gene construction and insertion. He was one of the major pioneers of population genetics, which gave a quantitative basis to the studies of evolution, of variation in natural populations and of animal and plant breeding. He contributed most significantly to methods and ideas over a long period, indeed his four volume treatise was written long after he formally ‘retired’ and his last paper (211) was published a few days before his death at the age of 98. In the field of population genetics Wright developed the method of path coefficients, which he used to analyse quantitative genetic variation and relationship, but which has been applied to subjects as diverse as economics, the ideas of inbreeding coefficient and F -statistics which form the basis of analysis of population structure, the theory of variation in gene frequency among populations, and the shifting balance theory of evolution, which remains a topic of active research and controversy. Wright contributed to physiological genetics, notably analysis of the inheritance of coat colour in the guinea pig, and in particular the epistatic relationships among the genes involved. There was a critical interplay between his population and physiological work, in that the analysis of finite populations on the one hand and of epistatic interactions on the other are the bases of Wright’s development of the shifting balance theory. A full and enlightening biography of Sewall Wright which traces his influence on evolutionary biology and his interactions with other important workers was published recently (Provine 1986) and shorter appreciations have appeared since his death, notably by Crow (1988), Wright’s long-time colleague. This biography relies heavily on Provine’s volume, and does no more than summarize Wright’s extensive contributions. Many of his important papers have been reprinted recently (1986).


2017 ◽  
Vol 114 (31) ◽  
pp. 8325-8329 ◽  
Author(s):  
Mathieu Chouteau ◽  
Violaine Llaurens ◽  
Florence Piron-Prunier ◽  
Mathieu Joron

Explaining the maintenance of adaptive diversity within populations is a long-standing goal in evolutionary biology, with important implications for conservation, medicine, and agriculture. Adaptation often leads to the fixation of beneficial alleles, and therefore it erodes local diversity so that understanding the coexistence of multiple adaptive phenotypes requires deciphering the ecological mechanisms that determine their respective benefits. Here, we show how antagonistic frequency-dependent selection (FDS), generated by natural and sexual selection acting on the same trait, maintains mimicry polymorphism in the toxic butterfly Heliconius numata. Positive FDS imposed by predators on mimetic signals favors the fixation of the most abundant and best-protected wing-pattern morph, thereby limiting polymorphism. However, by using mate-choice experiments, we reveal disassortative mate preferences of the different wing-pattern morphs. The resulting negative FDS on wing-pattern alleles is consistent with the excess of heterozygote genotypes at the supergene locus controlling wing-pattern variation in natural populations of H. numata. The combined effect of positive and negative FDS on visual signals is sufficient to maintain a diversity of morphs displaying accurate mimicry with other local prey, although some of the forms only provide moderate protection against predators. Our findings help understand how alternative adaptive phenotypes can be maintained within populations and emphasize the need to investigate interactions between selective pressures in other cases of puzzling adaptive polymorphism.


2020 ◽  
Vol 6 (39) ◽  
pp. eabb8617 ◽  
Author(s):  
James J. Lewis ◽  
Steven M. Van Belleghem ◽  
Riccardo Papa ◽  
Charles G. Danko ◽  
Robert D. Reed

Characterizing the genetic complexity of adaptation and trait evolution is a major emphasis of evolutionary biology and genetics. Incongruent findings from genetic studies have resulted in conceptual models ranging from a few large-effect loci to massively polygenic architectures. Here, we combine chromatin immunoprecipitation sequencing, Hi-C, RNA sequencing, and 40 whole-genome sequences from Heliconius butterflies to show that red color pattern diversification occurred via many genomic loci. We find that the red wing pattern master regulatory transcription factor Optix binds dozens of loci also under selection, which frequently form three-dimensional adaptive hubs with selection acting on multiple physically interacting genes. Many Optix-bound genes under selection are tied to pigmentation and wing development, and these loci collectively maintain separation between adaptive red color pattern phenotypes in natural populations. We propose a model of trait evolution where functional connections between loci may resolve much of the disparity between large-effect and polygenic evolutionary models.


1998 ◽  
Vol 46 (4) ◽  
pp. 533 ◽  
Author(s):  
Siegfried L. Krauss ◽  
Rod Peakall

The accurate assignment of paternity in natural plant populations is required to address important issues in evolutionary biology, such as the factors that affect reproductive success. Newly developed molecular fingerprinting techniques offer the potential to address these aims. Here, we evaluate the utility of a new PCR-based multi-locus fingerprinting technique called Amplified Fragment Length Polymorphism (AFLP) for paternity studies in Persoonia mollis (Proteaceae). AFLPs were initially scored for five individuals from three taxonomic levels for 64 primer pairs: between species (P. mollis and P. levis), between subspecies (P. mollis subsp. nectens and subsp. livens), between individuals within a single population of P. mollis, as well as for a naturally pollinated seed from a single P. mollis subsp. nectens plant. Overall, 1164 fragments (24.6% of all fragments) were polymorphic between species, 743 (16.5%) between subspecies, 371 (8.6%) between individuals within a single population, and 265 (6.2%) between a plant and its seed. Within a single P. mollis population of 14 plants, 42 polymorphic fragments were scored from profiles generated by a single AFLP primer pair. The mean frequency of the recessive allele (q) over these 42 loci was 0.773. Based on these observations, it will be feasible to generate well over 100 polymorphic AFLP loci with as few as three AFLP primer pairs. This level of polymorphism is sufficient to assign paternity unambiguously to more than 99% of all seed in experiments involving small, known paternity pools. More generally, the AFLP procedure is well suited to molecular ecological studies, because it produces more polymorphism than allozymes or RAPDs but, unlike conventionally developed microsatellite loci, it requires no prior sequence knowledge and minimal development time.


2018 ◽  
Author(s):  
Bin Li ◽  
Sakiko Yaegashi ◽  
Thaddeus M Carvajal ◽  
Maribet Gamboa ◽  
Kozo Watanabe

AbstractAdaptive divergence is a key mechanism shaping the genetic variation of natural populations. A central question linking ecology with evolutionary biology concerns the role of environmental heterogeneity in determining adaptive divergence among local populations within a species. In this study, we examined adaptive the divergence among populations of the stream mayfly Ephemera strigata in the Natori River Basin in northeastern Japan. We used a genome scanning approach to detect candidate loci under selection and then applied a machine learning method (i.e. Random Forest) and traditional distance-based redundancy analysis (dbRDA) to examine relationships between environmental factors and adaptive divergence at non-neutral loci. We also assessed spatial autocorrelation at neutral loci to quantify the dispersal ability of E. strigata. Our main findings were as follows: 1) random forest shows a higher resolution than traditional statistical analysis for detecting adaptive divergence; 2) separating markers into neutral and non-neutral loci provides insights into genetic diversity, local adaptation and dispersal ability and 3) E. strigata shows altitudinal adaptive divergence among the populations in the Natori River Basin.


2021 ◽  
Vol 118 (37) ◽  
pp. e2023801118
Author(s):  
Jae Young Choi ◽  
Xiaoguang Dai ◽  
Ornob Alam ◽  
Julie Z. Peng ◽  
Priyesh Rughani ◽  
...  

Some of the most spectacular adaptive radiations begin with founder populations on remote islands. How genetically limited founder populations give rise to the striking phenotypic and ecological diversity characteristic of adaptive radiations is a paradox of evolutionary biology. We conducted an evolutionary genomics analysis of genus Metrosideros, a landscape-dominant, incipient adaptive radiation of woody plants that spans a striking range of phenotypes and environments across the Hawaiian Islands. Using nanopore-sequencing, we created a chromosome-level genome assembly for Metrosideros polymorpha var. incana and analyzed whole-genome sequences of 131 individuals from 11 taxa sampled across the islands. Demographic modeling and population genomics analyses suggested that Hawaiian Metrosideros originated from a single colonization event and subsequently spread across the archipelago following the formation of new islands. The evolutionary history of Hawaiian Metrosideros shows evidence of extensive reticulation associated with significant sharing of ancestral variation between taxa and secondarily with admixture. Taking advantage of the highly contiguous genome assembly, we investigated the genomic architecture underlying the adaptive radiation and discovered that divergent selection drove the formation of differentiation outliers in paired taxa representing early stages of speciation/divergence. Analysis of the evolutionary origins of the outlier single nucleotide polymorphisms (SNPs) showed enrichment for ancestral variations under divergent selection. Our findings suggest that Hawaiian Metrosideros possesses an unexpectedly rich pool of ancestral genetic variation, and the reassortment of these variations has fueled the island adaptive radiation.


2017 ◽  
Author(s):  
Emily L. Behrman ◽  
Virginia M. Howick ◽  
Martin Kapun ◽  
Fabian Staubach ◽  
Alan O. Bergland ◽  
...  

AbstractUnderstanding the rate of evolutionary change and the genetic architecture that facilitates rapid adaptation is a current challenge in evolutionary biology. Comparative studies show that genes with immune function are among the most rapidly evolving genes in a range of taxa. Here, we use immune defense in natural populations of D. melanogaster to understand the rate of evolution in natural populations and the genetics underlying the rapid change. We probed the immune system using the natural pathogens Enterococcus faecalis and Providencia rettgeri to measure post-infection survival and bacterial load of wild D. melanogaster populations collected across seasonal time along a latitudinal transect on the eastern North America (Massachusetts, Pennsylvania, and Virginia). There are pronounced and repeatable changes in the immune response over approximately 10 generations between the spring and fall populations with a significant but less distinct difference among geographic locations. Genes with known immune function are not enriched among alleles that cycle with seasonal time, but the immune function of a subset of seasonally cycling alleles in immune genes was tested using reconstructed outbred populations. We find that flies containing seasonal alleles in Thioester-containing protein 3 (Tep3) have different functional responses to infection and that epistatic interactions among seasonal Tep3 and Drosomycin-like 6 (Dro6) alleles produce the immune phenotypes observed in natural populations. This rapid, cyclic response to seasonal environmental pressure broadens our understanding of the complex ecological and genetic interactions determining the evolution of immune defense in natural populations.


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