Different Genomic Changes Underlie Adaptive Evolution in Populations of Contrasting History

Seabra, Sofia G.; Fragata, Inês; Antunes, Marta A; Faria, Gonçalo S.; Santos, Marta A.; Sousa, Vítor C.; Simões, Pedro; Matos, Margarida

doi:10.1093/molbev/msx247

Cited by 30 publications

(28 citation statements)

References 79 publications

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“…Similar differences in repeatability at genetic and phenotypic levels has been documented in a variety of systems (Blount et al ., 2018). Beyond this, some of this variation in repeatability of adaptation to lentil at the genetic level likely stems from differences in shared genetic variation available for selection across these cases (as has also been seen in evolve-and-resequence studies in Drosophila ; Seabra et al ., 2017). Because lentil is a very stressful host, each C. maculatus line went through a severe bottleneck when it was shifted onto lentil (Gompert & Messina, 2016).…”

Section: Discussionmentioning

confidence: 96%

Dynamics of genomic change during evolutionary rescue in the seed beetleCallosobruchus maculatus

Rêgo

Messina

Gompert

2018

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1Rapid adaptation can prevent extinction when populations are exposed to extremely marginal 2 or stressful environments. Factors that a↵ect the likelihood of evolutionary rescue from ex-3 tinction have been identified, but much less is known about the evolutionary dynamics (e.g., 4 rates and patterns of allele frequency change) and genomic basis of successful rescue, par-5 ticularly in multicellular organisms. We conducted an evolve-and-resequence experiment to 6 investigate the dynamics of evolutionary rescue at the genetic level in the cowpea seed bee-7 tle, Callosobruchus maculatus, when it is experimentally shifted to a stressful host plant, 8 lentil. Low survival (⇠1%) at the onset of the experiment caused population decline. But 9 adaptive evolution quickly rescued the population, with survival rates climbing to 69% by 10 the F5 generation and 90% by the F10 generation. Population genomic data showed that 11 rescue likely was caused by rapid evolutionary change at multiple loci, with many alleles 12 fixing or nearly fixing within five generations of selection on lentil. Selection on these loci 13 was only moderately consistent in time, but parallel evolutionary changes were evident in 14 sublines formed after the lentil line had passed through a bottleneck. By comparing esti-15 mates of selection and genomic change on lentil across five independent C. maculatus lines 16 (the new lentil-adapted line, three long-established lines, and one case of failed evolutionary 17 rescue), we found that adaptation on lentil occurred via somewhat idiosyncratic evolutionary 18 changes. Overall, our results suggest that evolutionary rescue in this system can be caused 19 by very strong selection on multiple loci driving rapid and pronounced genomic change.20

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Section: Discussionmentioning

confidence: 96%

Dynamics of genomic change during evolutionary rescue in the seed beetleCallosobruchus maculatus

Rêgo

Messina

Gompert

2018

Preprint

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“…Gilligan and Frankham 2003;Rose et al 2004;Simões et al 2007, see below). The expectation of a deceleration of laboratory evolutionary trajectories in sexual organisms is sometimes justified in terms of temporal exhaustion of additive genetic variance, although genomic scans in experimentally evolved Drosophila populations have found only limited evidence of fixed alleles following selection (Burke et al 2010;Burke and Long 2012;Orozco-Terwengel et al 2012;Long et al 2015;Phillips et al 2016;Seabra et al 2018). In a previous study by our team, we found evidence for a deceleration in the evolutionary trajectory of fecundity in populations of Drosophila subobscura evolving for more than 80 generations in the lab environment (Simões et al 2007).…”

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confidence: 64%

How phenotypic convergence arises in experimental evolution

et al. 2019

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Evolutionary convergence is a core issue in the study of adaptive evolution, as well as a highly debated topic at present. Few studies have analyzed this issue using a “real‐time” or evolutionary trajectory approach. Do populations that are initially differentiated converge to a similar adaptive state when experiencing a common novel environment? Drosophila subobscura populations founded from different locations and years showed initial differences and variation in evolutionary rates in several traits during short‐term (∼20 generations) laboratory adaptation. Here, we extend that analysis to 40 more generations to analyze (1) how differences in evolutionary dynamics among populations change between shorter and longer time spans, and (2) whether evolutionary convergence occurs after 60 generations of evolution in a common environment. We found substantial variation in longer term evolutionary trajectories and differences between short‐ and longer term evolutionary dynamics. Although we observed pervasive patterns of convergence toward the character values of long‐established populations, populations still remain differentiated for several traits at the final generations analyzed. This pattern might involve transient divergence, as we report in some cases, indicating that more generations should lead to final convergence. These findings highlight the importance of longer term studies for understanding convergent evolution.

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“…At the time of analysis, assembled genomic resources were not available for the obscura and subobscura subgroups, and our analysis of transcriptomic data did not identify duplications in those genes. Following submission, draft genome assemblies became available for D. obscura [39] and D. subobscura [40]. A search of these genomes confirmed that duplicates are undetectable for all genes except vreteno, but that two copies of vreteno are only detectable in D. obscura (not shown).…”

Section: Six Pirna Pathway Genes Are Duplicated and Asterix And Cutomentioning

confidence: 99%

Widespread gene duplication and adaptive evolution in the RNA interference pathways of the Drosophila obscura group

Crysnanto

Obbard

2018

Preprint

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Background: RNA interference (RNAi) related pathways provide defense against viruses and transposable elements, and have been implicated in the suppression of meiotic drive elements.Genes in these pathways often exhibit high levels of adaptive substitution, and over longer timescales show gene duplication and loss-most likely as a consequence of their role in mediating conflict with these parasites. This is particularly striking for Argonaute 2 (Ago2), which is ancestrally the key effector of antiviral RNAi in insects, but has repeatedly formed new testis-specific duplicates in the recent history of the obscura species-group of Drosophila.Results: Here we take advantage of publicly available genomic and transcriptomic data to identify six further RNAi-pathway genes that have duplicated in this clade of Drosophila, and examine their evolutionary history. As seen for Ago2, we observe high levels of adaptive amino-acid substitution and changes in sex-biased expression in many of the paralogs. However, our phylogenetic analysis suggests that co-duplications of the RNAi machinery were not synchronous, and our expression analysis fails to identify consistent male-specific expression.Conclusions: These results confirm that RNAi genes, including genes of the antiviral and piRNA pathways, have undergone multiple independent duplications and that their history has been particularly labile within the obscura group. However, they also suggest that the selective pressures driving these changes have not been consistent, implying that more than one selective agent may be responsible.Gene duplication is an important process in molecular evolution, providing raw genetic material for evolutionary innovation. The evolutionary dynamics following gene duplication are often described in terms of two alternative models, 'neofunctionalization' and 'sub-functionalization' [1]. Under neofunctionalization, the functional redundancy following duplication provides relaxed selective constraint, and allows new mutations to accumulate through genetic drift. Most such mutations will reduce the functionality of the gene (resulting in pseudogenization), but some paralogs can be selected for novel or derived functions. Under sub-functionalization, the duplicates independently accumulate mutations that allow them to specialise in a subset of ancestral functions of a pleiotropic gene. Neo-functionalization leads to asymmetrical evolutionary rates among paralogs (with faster evolution in paralogs that gain derived function), whereas equal rates are expected for the latter [2].It has been suggested that both processes have played an important role in the rapid evolution of RNA interference-related pathways, including the long-and short-term evolutionary history of the Argonautes, the effectors of RNAi [3][4][5].The RNAi-related pathways comprise a range of small-RNA mechanisms best known for their roles in mediating the control of gene expression, antiviral responses, and defence against mobile genetic elements. Respectively, these include the miRNA pa...

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Different Genomic Changes Underlie Adaptive Evolution in Populations of Contrasting History

Cited by 30 publications

References 79 publications

Dynamics of genomic change during evolutionary rescue in the seed beetleCallosobruchus maculatus

Dynamics of genomic change during evolutionary rescue in the seed beetleCallosobruchus maculatus

How phenotypic convergence arises in experimental evolution

Widespread gene duplication and adaptive evolution in the RNA interference pathways of the Drosophila obscura group

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