Quantitative trait locus mapping reveals an independent genetic basis for joint divergence in leaf function, life‐history, and floral traits between scarlet monkeyflower (<i>Mimulus cardinalis</i>) populations

Nelson, Thomas C.; Muir, Christopher D.; Stathos, Angela; Vanderpool, Daniel D.; Anderson, Kayli; Angert, Amy L.; Fishman, Lila

doi:10.1002/ajb2.1660

Cited by 10 publications

(3 citation statements)

References 97 publications

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“…QTLs for different size traits were often coincident; for example, the first 5 Mb of Chr2 and Chr8 each housed overlapping UC_F 2 QTLs for 8 of the 11 floral dimensions. This co-incidence may not represent pleiotropic effects of single variants, as Mimulus chromosome ends are gene-dense and highly recombining (Nelson et al ., 2021a), but these regions are promising targets for dissection of multiple traits.…”

Section: Resultsmentioning

confidence: 99%

“…Along with bee-pollinated M. lewisii , which likely resembles the common ancestor of all three taxa, these closely related species are a model system for understanding the genetics of floral divergence and speciation (Yuan, 2019). Work in this system has provided key insights into the evolution and molecular biology of divergent pollination syndromes and their roles in local adaptation and speciation (Hiesey et al ., 1971; Bradshaw et al ., 1995; Schemske & Bradshaw, 1999; Ramsey et al ., 2003; Fishman et al ., 2013; Yuan et al ., 2013b, 2014; Stathos & Fishman, 2014; Fishman et al ., 2015; Yuan et al ., 2016; Peng et al ., 2017; Nelson et al ., 2021b,a; Liang et al ., 2023). New resources, including chromosome-scale reference genomes (www.Mimubase.org), dense linkage maps (Sotola et al ., 2023), and stable transformation protocols (Yuan, 2019), now enable genome-wide mapping, gene-scale dissection, and molecular characterization of the loci underlying Erythranthe floral diversity.…”

Section: Introductionmentioning

confidence: 99%

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The genetic architecture of floral trait divergence between hummingbird- and self-pollinated monkeyflower (Mimulus) species

Chen,

Berg,

Samuli

et al. 2024

Preprint

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SUMMARYPollination syndromes are a key component of flowering plant diversification, prompting questions about the architecture of single traits and genetic coordination among traits. Here, we investigate the genomic basis of extreme floral divergence between naturally hybridizing monkeyflowersMimulus parishii(self-pollinated) andM. cardinalis(hummingbird-pollinated).We mapped quantitative trait loci (QTLs) for 18 (nine fully shared) pigment, pollinator reward and handling, dimensional, and flowering time traits in two F2hybrid growouts and recombinant inbred lines. We independently generated nearly isogenic lines (NILs) to dissect QTLs for two dimensional traits, pistil length and corolla size.Our multi-population approach revealed a highly polygenic basis (n = 190 QTLs total) for pollination syndrome divergence. For the set of nine fully shared traits, 39% (55/140) were unique to a single population, but we also identified several QTL hotspots within and across trait categories. The complementary NIL approach refined two pistil length QTLs but selected a corolla size QTL resistant to genetic dissection.Divergence between hummingbird- and self-pollinated sister species has a highly polygenic and largely uncoordinated genetic architecture. Our results extend understanding of speciation in a classic floral radiation and provide a robust framework for further molecular dissection and ecological genomics.

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Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

The genetic architecture of floral trait divergence between hummingbird- and self-pollinated monkeyflower (Mimulus) species

Chen,

Berg,

Samuli

et al. 2024

Preprint

Self Cite

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“…The plants in this study were all derived from two highly (>10 generations) inbred lines of Sierran M. cardinalis (CE10) and M. parishii (PAR), which were also used in previous investigations of species barriers (Bradshaw et al 1998;Schemske and Bradshaw 1999;Ramsey et al 2003;Bradshaw and Schemske 2003;Fishman et al 2013Fishman et al , 2015Nelson et al 2021a). We generated PAR x CE10 F1 hybrids by hand-pollination (with prior emasculation of the PAR seed parent in the bud) and F2 hybrids by self-pollination of F1 hybrids.…”

Section: Study System and Plant Linesmentioning

confidence: 99%

Genomic mechanisms and consequences of diverse postzygotic barriers between monkeyflower species

Sotola

Berg

Samuli

et al. 2023

Preprint

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The evolution of genomic incompatibilities causing postzygotic barriers to hybridization is a key step in species divergence. Incompatibilities take two general forms structural divergence between chromosomes leading to severe hybrid sterility in F1hybrids and epistatic interactions between genes causing reduced fitness of hybrid gametes or zygotes (Dobzhansky-Muller incompatibilities). Despite substantial recent progress in understanding the molecular mechanisms and evolutionary origins of both types of incompatibility, how each behaves across multiple generations of hybridization remains relatively unexplored. Here, we use genetic mapping in F2and RIL hybrid populations between the phenotypically divergent but naturally hybridizing monkeyflowersMimulus cardinalisandM. parishiito characterize the genetic basis of hybrid incompatibility and examine its changing effects over multiple generations of experimental hybridization. In F2s, we found severe hybrid pollen inviability (< 50% reduction vs. parental genotypes) and pseudolinkage caused by a reciprocal translocation between Chromosomes 6 and 7 in the parental species. RILs retained excess heterozygosity around the translocation breakpoints, which caused substantial pollen inviability when interstitial crossovers had not created compatible heterokaryotypic configurations. Strong transmission ratio distortion and inter-chromosomal linkage disequilibrium in both F2s and RILs identified a novel two-locus genic incompatibility causing sex-independent gametophytic (haploid) lethality. The latter interaction completely eliminated three of the expected nine F2genotypic classes without detectable effects on the pollen number or viability of double heterozygotes. Along with the mapping of numerous milder incompatibilities, these key findings illuminate the complex genetics of plant hybrid breakdown and are an important step toward understanding the genomic consequences of natural hybridization in this model system.

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Selection on early survival does not explain germination rate clines in Mimulus cardinalis

Muir

Elzen

Angert

2022

American J of Botany

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Premise: Many traits covary with environmental gradients to form phenotypic clines. While local adaptation to the environment can generate phenotypic clines, other nonadaptive processes may also. If local adaptation causes phenotypic clines, then the direction of genotypic selection on traits should shift from one end of the cline to the other. Traditionally, genotypic selection on non-Gaussian traits like germination rate have been hampered because it is challenging to measure their genetic variance. Methods: Here we used quantitative genetics and reciprocal transplants to test whether a previously discovered cline in germination rate showed additional signatures of adaptation in the scarlet monkeyflower (Mimulus cardinalis). We measured genotypic and population level covariation between germination rate and early survival, a component of fitness. We developed a novel discrete log-normal model to estimate genetic variance in germination rate. Results: Contrary to our adaptive hypothesis, we found no evidence that genetic variation in germination rate contributed to variation in early survival. Across populations, southern populations in both gardens germinated earlier and survived more. Conclusions: Southern populations have higher early survival but it is not caused by faster germination. This pattern is consistent with nonadaptive forces driving the phenotypic cline in germination rate, but future work will need to assess whether there is selection at other life stages. This statistical framework should help expand quantitative genetic analyses for other waiting-time traits.

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Quantitative trait locus mapping reveals an independent genetic basis for joint divergence in leaf function, life‐history, and floral traits between scarlet monkeyflower (Mimulus cardinalis) populations

Abstract: 2021. Quantitative trait locus mapping reveals an independent genetic basis for joint divergence in leaf function, life-history, and floral traits between scarlet monkeyflower (Mimulus cardinalis) populations.

Cited by 10 publications

References 97 publications

The genetic architecture of floral trait divergence between hummingbird- and self-pollinated monkeyflower (Mimulus) species

The genetic architecture of floral trait divergence between hummingbird- and self-pollinated monkeyflower (Mimulus) species

Genomic mechanisms and consequences of diverse postzygotic barriers between monkeyflower species

Selection on early survival does not explain germination rate clines in Mimulus cardinalis

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