Ancient and modern stickleback genomes reveal the demographic constraints on adaptation

Kirch, Melanie; Romundset, Anders; Gilbert, M. Thomas P.; Jones, Felicity C.; Foote, Andrew

doi:10.1016/j.cub.2021.02.027

Cited by 38 publications

(50 citation statements)

References 71 publications

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“…When these glaciers melted, anadromous marine stickleback colonized freshwater to establish the permanent lake populations we study today. Using modern marine fish as a proxy for those ancestral founders (Kirch et al 2021), we are confident that those colonists were highly susceptible to S.solidus infection (high infection success rate, fast cestode growth). Although they possess the ancient genetic pathways to initiate peritoneal fibrosis (Vrtílek and Bolnick 2021), they do not do so in response to cestode infection.…”

Section: Discussionmentioning

confidence: 99%

Evolution of a costly immunity to cestode parasites is a pyrrhic victory

Weber

Steinel

Peng

et al. 2021

Preprint

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Parasites impose fitness costs on their hosts. Biologists therefore tend to assume that natural selection favors infection-resistant hosts. Yet, when the immune response itself is costly, theory suggests selection may instead favor loss of resistance. Immune costs are rarely documented in nature, and there are few examples of adaptive loss of resistance. Here, we show that when marine threespine stickleback colonized freshwater lakes they gained resistance to the freshwater-associated tapeworm, Schistocephalus solidus. Extensive peritoneal fibrosis and inflammation contribute to suppression of cestode growth and viability, but also impose a substantial cost of reduced fecundity. Combining genetic mapping and population genomics, we find that the immune differences between tolerant and resistant populations arise from opposing selection in both populations acting, respectively, to reduce and increase resistance consistent with divergent optimization.One Sentence SummaryRecently-evolved freshwater populations of stickleback frequently evolve increased resistance to tapeworms, involving extensive fibrosis that suppresses parasite growth; because this fibrosis greatly reduces fish fecundity, in some freshwater populations selection has favored an infection-tolerant strategy with fibrosis suppression.

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Section: Discussionmentioning

confidence: 99%

Evolution of a costly immunity to cestode parasites is a pyrrhic victory

Weber

Steinel

Peng

et al. 2021

Preprint

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“…1a) are a useful vertebrate species for understanding the impact of adaptation on range dynamics under climate change. In particular, the availability of a regionally downscaled climate model for the Pacific Northwest (Alexander et al, 2018; IPCC, 2014; Reynolds et al, 2007) make panmictic marine populations of G. aculeatus in the eastern Pacific Ocean (Kirch, Romundset, Gilbert, Jones, & Foote, 2021; Morris et al, 2018) an ideal system for testing how adaptive trait variation could affect projections of species range distributions under climate change (Barrett & Hendry, 2012).…”

Section: Introductionmentioning

confidence: 99%

“…It is also feasible to artificially breed multiple hybrid generations in common garden lab environments. Moreover, there is a regionally downscaled climate model for the Pacific Northwest (Alexander et al, 2018; IPCC, 2014; Reynolds et al, 2007), which makes panmictic marine populations of G. aculeatus in the eastern Pacific Ocean (Kirch et al, 2021; Morris et al, 2018) an ideal system for testing how adaptive trait variation could affect projections of species range under climate change.…”

Section: Introductionmentioning

confidence: 99%

Evolution of thermal physiology alters the projected range of threespine stickleback under climate change

Mogensen

Barry

et al. 2021

Preprint

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Species distribution models (SDMs) are widely adopted to predict range shifts but can be unreliable under climate change scenarios because they do not account for evolution. The thermal physiology of a species is a key determinant of range but the impact of thermal trait evolution on SDMs has not been addressed. We identified a genetic basis for physiological traits that evolve in response to temperature change in threespine stickleback. Using these data, we created geographic range projections under two climate change scenarios where trait data was either static (‘no evolution’ model), allowed to evolve in agreement with published evolutionary rates for the trait (‘evolution’ model), or allowed to evolve with the rate of evolution scaled in association with the variance that is explained by QTL (‘PVE’ model). Here, we show that incorporating these traits and their evolution into SDMs substantially altered the predicted ranges for a widespread panmictic marine population, with increases in area of over 7-fold. Evolution-informed SDMs should therefore improve the precision of forecasting range dynamics under climate change, thereby aiding in their application to management and the protection of biodiversity.

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“…A further insight into marine stickleback is that with both the random and neutral SNPs, the freshwater populations from North Uist appear genetically no more similar to marine fish sampled in immediate (ARDH, OBSM) or relative (IR) proximity than to the samples from the much more distant marine locations. This implies that at the genome-wide level, any Atlantic marine sampleirrespective of its precise geographic origin (and including off-shore samples like IR; Table S1) -serves as an adequate representation of ancestral Atlantic marine stickleback (see also Kirch et al 2021).…”

Section: Population Structurementioning

confidence: 99%

The maintenance of standing genetic variation: gene flow versus selective neutrality in Atlantic stickleback fish

Haenel

Guérard

MacColl

et al. 2021

Preprint

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Adaptation to derived habitats often occurs from standing genetic variation (SGV). The maintenance within ancestral populations of genetic variants favorable in derived habitats is commonly ascribed to long-term antagonism between purifying selection and gene flow resulting from hybridization across habitats. A largely unexplored alternative idea based on quantitative genetic models of polygenic adaptation is that variants favored in derived habitats are neutral in ancestral populations when their frequency is relatively low. To explore the latter, we first identify genetic variants important to the adaptation of threespine stickleback fish to a rare derived habitat – nutrient-depleted acidic lakes – based on whole-genome sequence data. Sequencing marine stickleback from six locations across the Atlantic ocean then allows us to infer that the frequency of these derived variants in the ancestral habitat is unrelated to the likely opportunity for gene flow of these variants from acidic-adapted populations. This result is consistent with the selective neutrality of derived variants within the ancestor. Our study thus supports an underappreciated explanation for the maintenance of SGV, and calls for a better understanding of the fitness consequences of adaptive genetic variation across habitats and genomic backgrounds.

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Ancient and modern stickleback genomes reveal the demographic constraints on adaptation

Cited by 38 publications

References 71 publications

Evolution of a costly immunity to cestode parasites is a pyrrhic victory

Evolution of a costly immunity to cestode parasites is a pyrrhic victory

Evolution of thermal physiology alters the projected range of threespine stickleback under climate change

The maintenance of standing genetic variation: gene flow versus selective neutrality in Atlantic stickleback fish

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