The genetic architecture of temperature adaptation is shaped by population ancestry and not by selection regime

Otte, Kerstin; Nolte, Viola; Mallard, François; Schlötterer, Christian

doi:10.1186/s13059-021-02425-9

Cited by 18 publications

(17 citation statements)

References 110 publications

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“…This observation is highly consistent with a series of publications, which focused on laboratory adaptation in Drosophila subobscura and found strong phenotypic and genomic responses [70,77]. The abundant evidence for laboratory adaptation in this study contrasts the observation of an E&R study in D. simulans , which found no shared haplotype block moving in the same direction between hot and cold temperatures [66].…”

Section: Discussionsupporting

confidence: 92%

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Genome-wide selection signatures reveal widespread synergistic effects of two different stressors in Drosophila melanogaster

et al. 2022

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Experimental evolution combined with whole-genome sequencing (evolve and resequence (E&R)) is a powerful approach to study the adaptive architecture of selected traits. Nevertheless, so far the focus has been on the selective response triggered by a single stressor. Building on the highly parallel selection response of founder populations with reduced variation, we evaluated how the presence of a second stressor affects the genomic selection response. After 20 generations of adaptation to laboratory conditions at either 18°C or 29°C, strong genome-wide selection signatures were observed. Only 38% of the selection signatures can be attributed to laboratory adaptation (no difference between temperature regimes). The remaining selection responses are either caused by temperature-specific effects, or reflect the joint effects of temperature and laboratory adaptation (same direction, but the magnitude differs between temperatures). The allele frequency changes resulting from the combined effects of temperature and laboratory adaptation were more extreme in the hot environment for 83% of the affected genomic regions—indicating widespread synergistic effects of the two stressors. We conclude that E&R with reduced genetic variation is a powerful approach to study genome-wide fitness consequences driven by the combined effects of multiple environmental factors.

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Section: Discussionsupporting

confidence: 92%

“…direction differs from an E&R study in Drosophila simulans, which found no shared haplotype block that was selected in the opposite direction in hot and cold environments [66].…”

Section: Discussioncontrasting

confidence: 89%

Genome-wide selection signatures reveal widespread synergistic effects of two different stressors in Drosophila melanogaster

et al. 2022

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“…In an attempt to shed more light on this different behaviour, replicate populations from the same Portuguese founder population were studied for approximately the same number of generations in a cold selection regime (10–20°C) [ 35 ]. Interestingly, the genomic response at the cold temperature was also highly parallel, similar to the hot temperature regime [ 28 ].…”

Section: The Degree Of Parallelism Depends On the Founder Population ...mentioning

confidence: 99%

How predictable is adaptation from standing genetic variation? Experimental evolution in Drosophila highlights the central role of redundancy and linkage disequilibrium

Schlötterer

2023

Phil. Trans. R. Soc. B

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Experimental evolution is well-suited to test the predictability of evolution without the confounding effects of inaccurate forecasts about future environments. Most of the literature about parallel (and thus predictable) evolution has been carried out in asexual microorganisms, which adapt by de novo mutations. Nevertheless, parallel evolution has also been studied in sexual species at the genomic level. Here, I review the evidence for parallel evolution in Drosophila , the best-studied obligatory outcrossing model for adaptation from standing genetic variation in the laboratory. Similar to asexual microorganisms, evidence for parallel evolution varies between the focal hierarchical levels. Selected phenotypes consistently respond in a very predicable way, but the underlying allele frequency changes are much less predictable. The most important insight is that the predictability of the genomic selection response for polygenic traits depends highly on the founder population and to a much lesser extent on the selection regime. This implies that predicting adaptive genomic response is challenging and requires a good understanding of the adaptive architecture (including linkage disequilibrium) in the ancestral populations. This article is part of the theme issue ‘Interdisciplinary approaches to predicting evolutionary biology’.

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“…Subtle shifts of allele frequencies across the genome can lead to divergent genomic backgrounds that give populations access to different ecological niches (e.g. [ 47 , 48 ]).…”

Section: Discussionmentioning

confidence: 99%

We get by with a little help from our friends: shared adaptive variation provides a bridge to novel ecological specialists during adaptive radiation

Richards

Martin

2022

Proc. R. Soc. B.

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Adaptive radiations involve astounding bursts of phenotypic, ecological and species diversity. However, the microevolutionary processes that underlie the origins of these bursts are still poorly understood. We report the discovery of an intermediate C. sp. ‘wide-mouth’ scale-eating ecomorph in a sympatric radiation of Cyprinodon pupfishes, illuminating the transition from a widespread algae-eating generalist to a novel microendemic scale-eating specialist. We first show that this ecomorph occurs in sympatry with generalist C. variegatus and scale-eating specialist C. desquamator on San Salvador Island, Bahamas, but is genetically differentiated, morphologically distinct and often consumes scales. We then compared the timing of selective sweeps on shared and unique adaptive variants in trophic specialists to characterize their adaptive walk. Shared adaptive regions swept first in both the specialist desquamator and the intermediate ‘wide-mouth’ ecomorph, followed by unique sweeps of introgressed variation in ‘wide-mouth’ and de novo variation in desquamator . The two scale-eating populations additionally shared 9% of their hard selective sweeps with the molluscivore C. brontotheroides , despite no single common ancestor among specialists. Our work provides a new microevolutionary framework for investigating how major ecological transitions occur and illustrates how both shared and unique genetic variation can provide a bridge for multiple species to access novel ecological niches.

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The genetic architecture of temperature adaptation is shaped by population ancestry and not by selection regime

Cited by 18 publications

References 110 publications

Genome-wide selection signatures reveal widespread synergistic effects of two different stressors in Drosophila melanogaster

Genome-wide selection signatures reveal widespread synergistic effects of two different stressors in Drosophila melanogaster

How predictable is adaptation from standing genetic variation? Experimental evolution in Drosophila highlights the central role of redundancy and linkage disequilibrium

We get by with a little help from our friends: shared adaptive variation provides a bridge to novel ecological specialists during adaptive radiation

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