Population structure and local selection yield high genomic variation in <i>Mimulus guttatus</i>

Puzey, Joshua R.; Willis, John H.; Kelly, John K.

doi:10.1111/mec.13922

Cited by 75 publications

(120 citation statements)

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“…There is not expected to be much intrapopulation ID in populations where all plants have very nearly the same highly homozygous genotype. In contrast to DUN, the IM population studied here has one the highest levels of sequence variation yet documented in a plant population with synonymous nucleotide diversity of approximately 3.3% genome wide (Puzey et al 2017).…”

Section: Discussionmentioning

confidence: 86%

“…In contrast to DUN, the IM population studied here has one the highest levels of sequence variation yet documented in a plant population with synonymous nucleotide diversity of approximately 3.3% genome wide (Puzey et al. ).…”

Section: Discussionmentioning

confidence: 92%

“…In total, 187 lines have been whole‐genome sequenced and confirmed to be highly homozygous; population genomic results such as the allele frequency spectrum are reported in Puzey et al. () and Troth et al. ().…”

Section: Methodsmentioning

confidence: 99%

“…In total, 187 lines have been whole-genome sequenced and confirmed to be highly homozygous; population genomic results such as the allele frequency spectrum are reported in Puzey et al (2017) and Troth et al (2018). Whole-genome sequencing also revealed that several of the lines are more closely related to each other either due to splitting of a single founder into multiple inbred lines or by random sampling of close relatives in the field.…”

Section: Study System and Line Developmentmentioning

confidence: 99%

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Severe inbreeding depression is predicted by the “rare allele load” inMimulus guttatus*

Brown

Kelly

2019

Evolution

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Most flowering plants are hermaphroditic and experience strong pressures to evolve self‐pollination (automatic selection and reproductive assurance). Inbreeding depression (ID) can oppose selection for selfing, but it remains unclear if ID is typically strong enough to maintain outcrossing. To measure the full cost of sustained inbreeding on fitness, and its genomic basis, we planted highly homozygous, fully genome‐sequenced inbred lines of yellow monkeyflower (Mimulus guttatus) in the field next to outbred plants from crosses between the same lines. The cost of full homozygosity is severe: 65% for survival and 86% for lifetime seed production. Accounting for the unmeasured effect of lethal and sterile mutations, we estimate that the average fitness of fully inbred genotypes is only 3–4% that of outbred competitors. The genome sequence data provide no indication of simple overdominance, but the number of rare alleles carried by a line, especially within rare allele clusters nonrandomly distributed across the genome, is a significant negative predictor of fitness measurements. These findings are consistent with a deleterious allele model for ID. High variance in rare allele load among lines and the genomic distribution of rare alleles both suggest that migration might be an important source of deleterious alleles to local populations.

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Section: Discussionmentioning

confidence: 86%

Section: Discussionmentioning

confidence: 92%

Section: Methodsmentioning

confidence: 99%

Section: Study System and Line Developmentmentioning

confidence: 99%

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Severe inbreeding depression is predicted by the “rare allele load” inMimulus guttatus*

Brown

Kelly

2019

Evolution

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“…Understanding the processes governing heterogeneity of genomewide diversity has been a long‐standing goal in evolutionary genetics (Ellegren & Galtier, ) and is of central importance to adaptation and speciation research (Seehausen et al., ; Wolf & Ellegren, ). A plethora of recent studies characterizing genetic variation of diverging natural populations in a taxonomically diverse set of species identified strong heterogeneity in the genomewide distribution of genetic diversity, both within and between populations (e.g., in sunflowers (Renaut et al., ), monkey flowers (Puzey, Willis, & Kelly, ), stickleback fish (Roesti, Kueng, Moser, & Berner ), rabbits (Carneiro et al., ) or birds (Ellegren et al., ; Poelstra et al., )). Despite commonality in patterns seen across this wide range of taxa, elucidating the underlying processes remains challenging (Wolf & Ellegren, ).…”

Section: Introductionmentioning

confidence: 99%

Genomewide patterns of variation in genetic diversity are shared among populations, species and higher‐order taxa

et al. 2017

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Genomewide screens of genetic variation within and between populations can reveal signatures of selection implicated in adaptation and speciation. Genomic regions with low genetic diversity and elevated differentiation reflective of locally reduced effective population sizes (N ) are candidates for barrier loci contributing to population divergence. Yet, such candidate genomic regions need not arise as a result of selection promoting adaptation or advancing reproductive isolation. Linked selection unrelated to lineage-specific adaptation or population divergence can generate comparable signatures. It is challenging to distinguish between these processes, particularly when diverging populations share ancestral genetic variation. In this study, we took a comparative approach using population assemblages from distant clades assessing genomic parallelism of variation in N . Utilizing population-level polymorphism data from 444 resequenced genomes of three avian clades spanning 50 million years of evolution, we tested whether population genetic summary statistics reflecting genomewide variation in N would covary among populations within clades, and importantly, also among clades where lineage sorting has been completed. All statistics including population-scaled recombination rate (ρ), nucleotide diversity (π) and measures of genetic differentiation between populations (F , PBS, d ) were significantly correlated across all phylogenetic distances. Moreover, genomic regions with elevated levels of genetic differentiation were associated with inferred pericentromeric and subtelomeric regions. The phylogenetic stability of diversity landscapes and stable association with genomic features support a role of linked selection not necessarily associated with adaptation and speciation in shaping patterns of genomewide heterogeneity in genetic diversity.

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Population responses to a historic drought across the range of the common monkeyflower (Mimulus guttatus)

Kooyers

Morioka

Colicchio

et al. 2021

American J of Botany

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PREMISE Due to climate change, more frequent and intense periodic droughts are predicted to increasingly pose major challenges to the persistence of plant populations. When a severe drought occurs over a broad geographical region, independent responses by individual populations provide replicated natural experiments for examining the evolution of drought resistance and the potential for evolutionary rescue. METHODS We used a resurrection approach to examine trait evolution in populations of the common monkeyflower, Mimulus guttatus, exposed to a record drought in California from 2011 to 2017. Specifically, we compared variation in traits related to drought escape and avoidance from seeds collected from 37 populations pre‐ and post‐drought in a common garden. In a parallel experiment, we evaluated fitness in two populations, one which thrived and one which was nearly extirpated during the drought, under well‐watered and dry‐down conditions. RESULTS We observed substantial variation among populations in trait evolution. In the subset of populations where phenotypes changed significantly, divergence proceeded along trait correlations with some populations flowering rapidly with less vegetative tissue accumulation and others delaying flowering with greater vegetative tissue accumulation. The degree of trait evolution was only weakly correlated with drought intensity but strongly correlated with initial levels of standing variation. Fitness was higher in the post‐drought than pre‐drought accessions in both treatments for the thriving population, but lower in both treatments for the nearly extirpated population. CONCLUSIONS Together, our results indicate that evolutionary responses to drought are context dependent and reflect the standing genetic variation and genetic correlations present within populations.

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Population structure and local selection yield high genomic variation in Mimulus guttatus

Cited by 75 publications

References 104 publications

Severe inbreeding depression is predicted by the “rare allele load” inMimulus guttatus*

Severe inbreeding depression is predicted by the “rare allele load” inMimulus guttatus*

Genomewide patterns of variation in genetic diversity are shared among populations, species and higher‐order taxa

Population responses to a historic drought across the range of the common monkeyflower (Mimulus guttatus)

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