UNVEILing connections between genotype, phenotype, and fitness in natural populations

Nelson, Thomas C.; Jones, Matthew R.; Velotta, Jonathan P.; Dhawanjewar, Abhilesh S; Schweizer, Rena M.

doi:10.1111/mec.15067

Cited by 15 publications

(11 citation statements)

References 86 publications

(117 reference statements)

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“…A growing number of studies have found evidence for convergent adaptation within and between species (Hoekstra and Nachman 2003;Steiner et al 2008;Rosenblum et al 2010;Dobler et al 2012;Marques et al 2017;Giska et al 2019;Nelson et al 2019;Harris et al 2020), although we often lack an understanding of the forces that determine whether local adaptation occurs through independent de novo mutations or migration of pre-existing alleles from other populations (Ralph and Coop 2015). Our study provides rare empirical insights into how gene flow, mutation, allelic dominance, and selection interact to shape the spatial scale and pace of local adaptation to new or changing environments.…”

Section: Discussionmentioning

confidence: 93%

Convergent evolution of seasonal camouflage in response to reduced snow cover across the snowshoe hare range*

et al. 2020

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Determining how different populations adapt to similar environments is fundamental to understanding the limits of adaptation under changing environments. Snowshoe hares (Lepus americanus) typically molt into white winter coats to remain camouflaged against snow. In some warmer climates, hares have evolved brown winter camouflage—an adaptation that may spread in response to climate change. We used extensive range‐wide genomic data to (1) resolve broad patterns of population structure and gene flow and (2) investigate the factors shaping the origins and distribution of winter‐brown camouflage variation. In coastal Pacific Northwest (PNW) populations, winter‐brown camouflage is known to be determined by a recessive haplotype at the Agouti pigmentation gene. Our phylogeographic analyses revealed deep structure and limited gene flow between PNW and more northern Boreal populations, where winter‐brown camouflage is rare along the range edge. Genome sequencing of a winter‐brown snowshoe hare from Alaska shows that it lacks the winter‐brown PNW haplotype, reflecting a history of convergent phenotypic evolution. However, the PNW haplotype does occur at low frequency in a winter‐white population from Montana, consistent with the spread of a locally deleterious recessive variant that is masked from selection when rare. Simulations of this population further show that this masking effect would greatly slow the selective increase of the winter‐brown Agouti allele should it suddenly become beneficial (e.g., owing to dramatic declines in snow cover). Our findings underscore how allelic dominance can shape the geographic extent and rate of convergent adaptation in response to rapidly changing environments.

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Section: Discussionmentioning

confidence: 93%

Convergent evolution of seasonal camouflage in response to reduced snow cover across the snowshoe hare range*

et al. 2020

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“…Understanding how organisms adapt to different environments is a major goal in evolutionary biology (Hoban et al, 2016; Nelson et al, 2019). The genetic basis of adaptative traits has been studied in several organisms, such as lactase persistence (Tishkoff et al, 2007) and skin colour in humans (Norton et al, 2007), and dark colour in the peppered moth Biston Betularia (Van't Hof et al, 2016) among many others.…”

Section: Introductionmentioning

confidence: 99%

Temperature, rainfall and wind variables underlie environmental adaptation in natural populations of Drosophila melanogaster

et al. 2021

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While several studies in a diverse set of species have shed light on the genes underlying adaptation, our knowledge on the selective pressures that explain the observed patterns lags behind. Drosophila melanogaster is a valuable organism to study environmental adaptation because this species originated in Southern Africa and has recently expanded worldwide, and also because it has a functionally well‐annotated genome. In this study, we aimed to decipher which environmental variables are relevant for adaptation of D. melanogaster natural populations in Europe and North America. We analysed 36 whole‐genome pool‐seq samples of D. melanogaster natural populations collected in 20 European and 11 North American locations. We used the BayPass software to identify single nucleotide polymorphisms (SNPs) and transposable elements (TEs) showing signature of adaptive differentiation across populations, as well as significant associations with 59 environmental variables related to temperature, rainfall, evaporation, solar radiation, wind, daylight hours, and soil type. We found that in addition to temperature and rainfall, wind related variables are also relevant for D. melanogaster environmental adaptation. Interestingly, 23%–51% of the genes that showed significant associations with environmental variables were not found overly differentiated across populations. In addition to SNPs, we also identified 10 reference transposable element insertions associated with environmental variables. Our results showed that genome‐environment association analysis can identify adaptive genetic variants that are undetected by population differentiation analysis while also allowing the identification of candidate environmental drivers of adaptation.

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“…standing genetic variation (Jones et al 2012;Roesti et al 2012;Feulner et al 2015;Schrider and Kern 2017;Barrett and Schluter 2008;Nelson and Cresko 2018;Nelson et al 2019;Bassham et al 2018). However, it is still not clear how variation in evolutionary processessuch as gene flow, recombination, selection and mutationcan promote the maintenance and re-use of standing genetic variation, particularly during colonization and adaptation to new environments (Nelson and Cresko 2018;Pritchard 2010;Yeaman and Whitlock 2011;Schrider and Kern 2017).…”

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confidence: 99%

“…The ancestral marine form of threespine stickleback fish (Gasterosteus aculeatus) has given rise to hundreds of thousands to millions of independently derived freshwater populations in recently de-glaciated regions around the Northern Hemisphere (Bell and Foster 1994;Thompson 1997;Cresko et al 2007;Hunt et al 2008). This model organism has provided some of the earliest data showing the heterogeneous nature of divergence across genomes and the much more extensive use of standing genetic variation than once thought (Schluter and Conte 2009;DeFaveri et al 2011DeFaveri et al , 2013Roesti et al 2014;Nelson and Cresko 2018;Bassham et al 2018;Nelson et al 2019;Hohenlohe et al 2010;Terekhanova et al 2014;Marques et al 2016). While geographic isolation often prevents direct migration between freshwater populations, threespine stickleback in them frequently evolve similar phenotypes (Cresko et al 2004;Colosimo et al 2004;Stuart et al 2017;Hanson et al 2016Hanson et al , 2017Hirase et al 2014).…”

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confidence: 99%

A Few Stickleback Suffice for the Transport of Alleles to New Lakes

Galloway¹,

Cresko²,

Ralph

2020

G3 Genes|Genomes|Genetics

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Threespine stickleback populations provide a striking example of local adaptation to divergent habitats in populations that are connected by recurrent gene flow. These small fish occur in marine and freshwater habitats throughout the Northern Hemisphere, and in numerous cases the smaller freshwater populations have been established “de novo” from marine colonists. Independently evolved freshwater populations exhibit similar phenotypes that have been shown to derive largely from the same standing genetic variants. Geographic isolation prevents direct migration between the freshwater populations, strongly suggesting that these shared locally adaptive alleles are transported through the marine population. However it is still largely unknown how gene flow, recombination, and selection jointly impact the standing variation that might fuel this adaptation. Here we use individual-based, spatially explicit simulations to determine the levels of gene flow that best match observed patterns of allele sharing among habitats in stickleback. We aim to better understand how gene flow and local adaptation in large metapopulations determine the speed of adaptation and re-use of standing genetic variation. In our simulations we find that repeated adaptation uses a shared set of alleles that are maintained at low frequency by migration-selection balance in oceanic populations. This process occurs over a realistic range of intermediate levels of gene flow that match previous empirical population genomic studies in stickleback. Examining these simulations more deeply reveals how lower levels of gene flow leads to slow, independent adaptation to different habitats, whereas higher levels of gene flow leads to significant mutation load – but an increased probability of successful population genomic scans for locally adapted alleles. Surprisingly, we find that the genealogical origins of most freshwater adapted alleles can be traced back to the original generation of marine individuals that colonized the lakes, as opposed to subsequent migrants. These simulations provide deeper context for existing studies of stickleback evolutionary genomics, and guidance for future empirical studies in this model. More broadly, our results support existing theory of local adaptation but extend it by more completely documenting the genealogical history of adaptive alleles in a metapopulation.

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UNVEILing connections between genotype, phenotype, and fitness in natural populations

Cited by 15 publications

References 86 publications

Convergent evolution of seasonal camouflage in response to reduced snow cover across the snowshoe hare range*

Convergent evolution of seasonal camouflage in response to reduced snow cover across the snowshoe hare range*

Temperature, rainfall and wind variables underlie environmental adaptation in natural populations of Drosophila melanogaster

A Few Stickleback Suffice for the Transport of Alleles to New Lakes

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