LOCAL ADAPTATION, PHENOTYPIC DIFFERENTIATION, AND HYBRID FITNESS IN DIVERGED NATURAL POPULATIONS OF ARABIDOPSIS LYRATA

ABSTRACTPhenotypic differentiation among natural populations can be explained by natural selection or by neutral processes such as drift. There are many examples in the literature where comparing the effects of these processes on multiple populations has allowed the detection of local adaptation. However, these studies rarely identify the agents of selection. Whether population adaptive divergence is caused by local features of the environment, or by the environmental demand emerging at a more global scale, for example along altitudinal gradients, is a question that remains poorly investigated. Here, we measured neutral genetic (FST) and quantitative genetic (QST) differentiation among 13 populations of snapdragon plants (Antirrhinum majus) in a common garden experiment. We found low but significant genetic differentiation at putatively neutral markers, which supports the hypothesis of either ongoing pervasive homogenisation via gene flow between diverged populations or reproductive isolation between disconnected populations. Our results also support the hypothesis of local adaptation involving phenological, morphological, reproductive and functional traits. They also showed that phenotypic differentiation increased with altitude for traits reflecting the reproduction and the phenology of plants, thereby confirming the role of such traits in their adaptation to environmental differences associated with altitude. Our approach allowed us to identify candidate traits for the adaptation to climate change in snapdragon plants. Our findings imply that environmental conditions changing with altitude, such as the climatic envelope, influenced the adaptation of multiple populations of snapdragon plants on the top of their adaptation to local environmental features. They also have implications for the study of adaptive evolution in structured populations because they highlight the need to disentangle the adaptation of plant populations to climate envelopes and altitude from the confounding effects of selective pressures acting specifically at the local scale of a population.

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Testing for Effects of Recombination Rate on Nucleotide Diversity in Natural Populations of Arabidopsis lyrata

Genetics ◽

10.1534/genetics.106.062588 ◽

2006 ◽

Vol 174 (3) ◽

pp. 1421-1430 ◽

Cited By ~ 51

Author(s):

Stephen I. Wright ◽

John Paul Foxe ◽

Leah DeRose-Wilson ◽

Akira Kawabe ◽

Mark Looseley ◽

...

Keyword(s):

Recombination Rate ◽

Nucleotide Diversity ◽

Natural Populations ◽

Arabidopsis Lyrata

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Genomic Patterns of Local Adaptation under Gene Flow in Arabidopsis lyrata

Molecular Biology and Evolution ◽

10.1093/molbev/msz149 ◽

2019 ◽

Vol 36 (11) ◽

pp. 2557-2571 ◽

Cited By ~ 17

Author(s):

Tuomas Hämälä ◽

Outi Savolainen

Keyword(s):

Gene Flow ◽

Local Adaptation ◽

Demographic History ◽

Rate Variation ◽

Arabidopsis Lyrata ◽

Trade Offs ◽

Northern Latitudes ◽

Local Selection ◽

Empirical Level ◽

Selected Traits

AbstractShort-scale local adaptation is a complex process involving selection, migration, and drift. The expected effects on the genome are well grounded in theory but examining these on an empirical level has proven difficult, as it requires information about local selection, demographic history, and recombination rate variation. Here, we use locally adapted and phenotypically differentiated Arabidopsis lyrata populations from two altitudinal gradients in Norway to test these expectations at the whole-genome level. Demography modeling indicates that populations within the gradients diverged <2 kya and that the sites are connected by gene flow. The gene flow estimates are, however, highly asymmetric with migration from high to low altitudes being several times more frequent than vice versa. To detect signatures of selection for local adaptation, we estimate patterns of lineage-specific differentiation among these populations. Theory predicts that gene flow leads to concentration of adaptive loci in areas of low recombination; a pattern we observe in both lowland-alpine comparisons. Although most selected loci display patterns of conditional neutrality, we found indications of genetic trade-offs, with one locus particularly showing high differentiation and signs of selection in both populations. Our results further suggest that resistance to solar radiation is an important adaptation to alpine environments, while vegetative growth and bacterial defense are indicated as selected traits in the lowland habitats. These results provide insights into genetic architectures and evolutionary processes driving local adaptation under gene flow. We also contribute to understanding of traits and biological processes underlying alpine adaptation in northern latitudes.

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Gene, phenotype and function: GLABROUS1 and resistance to herbivory in natural populations of Arabidopsis lyrata

Molecular Ecology ◽

10.1111/j.1365-294x.2006.03109.x ◽

2006 ◽

Vol 0 (0) ◽

pp. 061222052703001-??? ◽

Cited By ~ 1

Author(s):

MAARIT KIVIMÄKI ◽

KATRI KÄRKKÄINEN ◽

MYRIAM GAUDEUL ◽

GEIR LØE ◽

JON ÅGREN

Keyword(s):

Natural Populations ◽

Arabidopsis Lyrata ◽

Resistance To Herbivory ◽

And Function

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Limited potential for adaptation to climate change in a broadly distributed marine crustacean

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2011.0542 ◽

2011 ◽

Vol 279 (1727) ◽

pp. 349-356 ◽

Cited By ~ 175

Author(s):

Morgan W. Kelly ◽

Eric Sanford ◽

Richard K. Grosberg

Keyword(s):

Climate Change ◽

Local Adaptation ◽

Thermal Tolerance ◽

Extinction Risk ◽

Empirical Studies ◽

Natural Populations ◽

Adaptation To Climate Change ◽

Isolated Populations ◽

Tigriopus Californicus ◽

Standing Variation

The extent to which acclimation and genetic adaptation might buffer natural populations against climate change is largely unknown. Most models predicting biological responses to environmental change assume that species' climatic envelopes are homogeneous both in space and time. Although recent discussions have questioned this assumption, few empirical studies have characterized intraspecific patterns of genetic variation in traits directly related to environmental tolerance limits. We test the extent of such variation in the broadly distributed tidepool copepod Tigriopus californicus using laboratory rearing and selection experiments to quantify thermal tolerance and scope for adaptation in eight populations spanning more than 17° of latitude. Tigriopus californicus exhibit striking local adaptation to temperature, with less than 1 per cent of the total quantitative variance for thermal tolerance partitioned within populations. Moreover, heat-tolerant phenotypes observed in low-latitude populations cannot be achieved in high-latitude populations, either through acclimation or 10 generations of strong selection. Finally, in four populations there was no increase in thermal tolerance between generations 5 and 10 of selection, suggesting that standing variation had already been depleted. Thus, plasticity and adaptation appear to have limited capacity to buffer these isolated populations against further increases in temperature. Our results suggest that models assuming a uniform climatic envelope may greatly underestimate extinction risk in species with strong local adaptation.

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Outcrossing rates in an experimentally admixed population of self-compatible and self-incompatible Arabidopsis lyrata

Heredity ◽

10.1038/s41437-021-00489-8 ◽

2021 ◽

Author(s):

Christina Steinecke ◽

Courtney E. Gorman ◽

Marc Stift ◽

Marcel E. Dorken

Keyword(s):

Gene Flow ◽

Natural Populations ◽

Secondary Contact ◽

Uniform Density ◽

Evolutionary Divergence ◽

Arabidopsis Lyrata ◽

Multiple Origins ◽

Outcrossing Rates ◽

Self Fertilization ◽

Self Compatibility

AbstractThe transition to self-compatibility from self-incompatibility is often associated with high rates of self-fertilization, which can restrict gene flow among populations and cause reproductive isolation of self-compatible (SC) lineages. Secondary contact between SC and self-incompatible (SI) lineages might re-establish gene flow if SC lineages remain capable of outcrossing. By contrast, intrinsic features of SC plants that reinforce high rates of self-fertilization could maintain evolutionary divergence between lineages. Arabidopsis lyrata subsp. lyrata is characterized by multiple origins of self-compatibility and high rates of self-fertilization in SC-dominated populations. It is unclear whether these high rates of selfing by SC plants have intrinsic or extrinsic causes. We estimated outcrossing rates and examined patterns of pollinator movement for 38 SC and 40 SI maternal parents sampled from an admixed array of 1509 plants sourced from six SC and six SI populations grown under uniform density. Although plants from SI populations had higher outcrossing rates (mean tm = 0.78 ± 0.05 SE) than plants from SC populations (mean tm = 0.56 ± 0.06 SE), outcrossing rates among SC plants were substantially higher than previous estimates from natural populations. Patterns of pollinator movement appeared to contribute to lower outcrossing rates for SC plants; we estimated that 40% of floral visits were geitonogamous (between flowers of the same plant). The relatively high rates of outcrossing for SC plants under standardized conditions indicate that selfing rates in natural SC populations of A. lyrata are facultative and driven by extrinsic features of A. lyrata, including patterns of pollinator movement.

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Low genome-wide divergence between two lizard populations with high adaptive phenotypic differentiation

10.22541/au.163250123.31170409/v1 ◽

2021 ◽

Author(s):

Alejandro Llanos-Garrido ◽

Javier Pérez-Tris ◽

José Díaz

Keyword(s):

Local Adaptation ◽

Genetic Divergence ◽

Elevational Gradient ◽

Phenotypic Differentiation ◽

Genome Wide ◽

Isolation By Environment ◽

Psammodromus Algirus ◽

Low Levels ◽

Two Populations ◽

Degree Of Isolation

Usually, adaptive phenotypic differentiation is paralleled by genetic divergence between locally adapted populations. However, adaptation can also happen in a scenario of non-significant genetic divergence due to intense gene flow and/or recent differentiation. While this phenomenon is rarely published, findings on incipient ecologically-driven divergence or isolation by adaptation are relatively common, which could confound our understanding about the frequency at which they actually occur in nature. Here, we explore genome-wide traces of divergence between two populations of the lacertid lizard Psammodromus algirus separated by a 600 m elevational gradient. These populations seem to be differentially adapted to their environments despite showing low levels of genetic differentiation (according to previously studies of mtDNA and microsatellite data). We performed a search for outliers (i.e. loci subject to selection) trying to identify specific loci with FST statistics significantly higher than those expected on the basis of overall, genome-wide estimates of genetic divergence. We find that local phenotypic adaptation (in terms of a wide diversity of characters) was not accompanied by genome-wide differentiation, even when we maximized the chances of unveiling such differentiation at particular loci with FST-based outlier detection tests. Instead, our analyses confirmed the lack of differentiation on the basis of more than 70,000 SNPs, which is concordant with a scenario of local adaptation without any degree of isolation by environment. Our results add evidence to previous studies in which local adaptation does not lead to any kind of isolation (or early stages of ecological speciation), but maintains phenotypic divergence despite the lack of a differentiated genomic background.

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Evolution of polygenic traits under global vs local adaptation

Genetics ◽

10.1093/genetics/iyab134 ◽

2022 ◽

Vol 220 (1) ◽

Author(s):

Sam Yeaman

Keyword(s):

Local Adaptation ◽

Complex Traits ◽

Genetic Architecture ◽

Population Genomics ◽

Natural Populations ◽

Evolutionary Process ◽

Frequency Effect ◽

Theoretical Predictions ◽

Using Data ◽

And Migration

Abstract Observations about the number, frequency, effect size, and genomic distribution of alleles associated with complex traits must be interpreted in light of evolutionary process. These characteristics, which constitute a trait’s genetic architecture, can dramatically affect evolutionary outcomes in applications from agriculture to medicine, and can provide a window into how evolution works. Here, I review theoretical predictions about the evolution of genetic architecture under spatially homogeneous, global adaptation as compared with spatially heterogeneous, local adaptation. Due to the tension between divergent selection and migration, local adaptation can favor “concentrated” genetic architectures that are enriched for alleles of larger effect, clustered in a smaller number of genomic regions, relative to expectations under global adaptation. However, the evolution of such architectures may be limited by many factors, including the genotypic redundancy of the trait, mutation rate, and temporal variability of environment. I review the circumstances in which predictions differ for global vs local adaptation and discuss where progress can be made in testing hypotheses using data from natural populations and lab experiments. As the field of comparative population genomics expands in scope, differences in architecture among traits and species will provide insights into how evolution works, and such differences must be interpreted in light of which kind of selection has been operating.

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Faculty Opinions recommendation of Patterns of polymorphism and demographic history in natural populations of Arabidopsis lyrata.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.1120459.576660 ◽

2008 ◽

Author(s):

Thomas Mitchell-Olds

Keyword(s):

Demographic History ◽

Natural Populations ◽

Arabidopsis Lyrata

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Intercontinental karyotype–environment parallelism supports a role for a chromosomal inversion in local adaptation in a seaweed fly

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2018.0519 ◽

2018 ◽

Vol 285 (1881) ◽

pp. 20180519 ◽

Cited By ~ 15

Author(s):

Claire Mérot ◽

Emma L. Berdan ◽

Charles Babin ◽

Eric Normandeau ◽

Maren Wellenreuther ◽

...

Keyword(s):

North America ◽

Local Adaptation ◽

Environmental Gradients ◽

Balancing Selection ◽

Chromosomal Rearrangements ◽

Natural Populations ◽

Inversion Polymorphism ◽

Life History Strategies ◽

Heterogeneous Environments ◽

Adult Size

Large chromosomal rearrangements are thought to facilitate adaptation to heterogeneous environments by limiting genomic recombination. Indeed, inversions have been implicated in adaptation along environmental clines and in ecotype specialization. Here, we combine classical ecological studies and population genetics to investigate an inversion polymorphism previously documented in Europe among natural populations of the seaweed fly Coelopa frigida along a latitudinal cline in North America. We test if the inversion is present in North America and polymorphic, assess which environmental conditions modulate the inversion karyotype frequencies, and document the relationship between inversion karyotype and adult size. We sampled nearly 2000 flies from 20 populations along several environmental gradients to quantify associations of inversion frequencies to heterogeneous environmental variables. Genotyping and phenotyping showed a widespread and conserved inversion polymorphism between Europe and America. Variation in inversion frequency was significantly associated with environmental factors, with parallel patterns between continents, indicating that the inversion may play a role in local adaptation. The three karyotypes of the inversion are differently favoured across micro-habitats and represent life-history strategies likely to be maintained by the collective action of several mechanisms of balancing selection. Our study adds to the mounting evidence that inversions are facilitators of adaptation and enhance within-species diversity.

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