The extent and genetic basis of phenotypic divergence in life history traits in Mimulus guttatus

Differential natural selection acting on populations in contrasting environments often results in adaptive divergence in multivariate phenotypes. Multivariate trait divergence across populations could be caused by selection on pleiotropic alleles or through many independent loci with trait‐specific effects. Here, we assess patterns of association between a suite of traits contributing to life history divergence in the common monkey flower, Mimulus guttatus, and examine the genetic architecture underlying these correlations. A common garden survey of 74 populations representing annual and perennial strategies from across the native range revealed strong correlations between vegetative and reproductive traits. To determine whether these multitrait patterns arise from pleiotropic or independent loci, we mapped QTLs using an approach combining high‐throughput sequencing with bulk segregant analysis on a cross between populations with divergent life histories. We find extensive pleiotropy for QTLs related to flowering time and stolon production, a key feature of the perennial strategy. Candidate genes related to axillary meristem development colocalize with the QTLs in a manner consistent with either pleiotropic or independent QTL effects. Further, these results are analogous to previous work showing pleiotropy‐mediated genetic correlations within a single population of M. guttatus experiencing heterogeneous selection. Our findings of strong multivariate trait associations and pleiotropic QTLs suggest that patterns of genetic variation may determine the trajectory of adaptive divergence.

[1]  D. Wagner,et al.  Gibberellin Acts Positively Then Negatively to Control Onset of Flower Formation in Arabidopsis , 2014, Science.

[2]  J. Preston,et al.  Differential SPL gene expression patterns reveal candidate genes underlying flowering time and architectural differences in Mimulus and Arabidopsis. , 2014, Molecular phylogenetics and evolution.

[3]  A. Sweigart,et al.  Evolutionary genetics of plant adaptation: insights from new model systems. , 2014, Current opinion in plant biology.

[4]  B. Koseva,et al.  A High-Resolution Genetic Map of Yellow Monkeyflower Identifies Chemical Defense QTLs and Recombination Rate Variation , 2014, G3: Genes, Genomes, Genetics.

[5]  B. Janssen,et al.  Regulation of axillary shoot development. , 2014, Current opinion in plant biology.

[6]  S. Park,et al.  Meristem maturation and inflorescence architecture--lessons from the Solanaceae. , 2014, Current opinion in plant biology.

[7]  S. Park,et al.  Tomato Yield Heterosis Is Triggered by a Dosage Sensitivity of the Florigen Pathway That Fine-Tunes Shoot Architecture , 2013, PLoS genetics.

[8]  O. Savolainen,et al.  Complex Genetic Effects on Early Vegetative Development Shape Resource Allocation Differences Between Arabidopsis lyrata Populations , 2013, Genetics.

[9]  S. Kay,et al.  BRANCHED1 Interacts with FLOWERING LOCUS T to Repress the Floral Transition of the Axillary Meristems in Arabidopsis[C][W][OA] , 2013, Plant Cell.

[10]  J. Plotkin,et al.  The evolution of genetic architectures underlying quantitative traits , 2012, Proceedings of the Royal Society B: Biological Sciences.

[11]  Brent S. Pedersen,et al.  Comb-p: software for combining, analyzing, grouping and correcting spatially correlated P-values , 2012, Bioinform..

[12]  L. Hileman,et al.  Patterns of shoot architecture in locally adapted populations are linked to intraspecific differences in gene regulation. , 2012, The New phytologist.

[13]  J. Willis,et al.  Spatially and temporally varying selection on intrapopulation quantitative trait loci for a life history trade‐off in Mimulus guttatus , 2012, Molecular ecology.

[14]  B. Ayre,et al.  Manipulating plant architecture with members of the CETS gene family. , 2012, Plant science : an international journal of experimental plant biology.

[15]  G. Nesom Taxonomy of Erythranthe sect. Simiola (Phrymaceae) in the USA and Mexico , 2012 .

[16]  J. Willis,et al.  Five anthocyanin polymorphisms are associated with an R2R3-MYB cluster in Mimulus guttatus (Phrymaceae). , 2012, American journal of botany.

[17]  R. L. Baker,et al.  Node-specific branching and heterochronic changes underlie population-level differences in Mimulus guttatus (Phrymaceae) shoot architecture. , 2011, American journal of botany.

[18]  Paul M. Magwene,et al.  The Statistics of Bulk Segregant Analysis Using Next Generation Sequencing , 2011, PLoS Comput. Biol..

[19]  K. Donohue,et al.  Population differentiation and plasticity in vegetative ontogeny: effects on life-history expression in Erysimum capitatum (Brassicaceae). , 2011, American journal of botany.

[20]  J. Abelenda,et al.  Control of flowering and storage organ formation in potato by FLOWERING LOCUS T , 2011, Nature.

[21]  B. Grant,et al.  How and Why Species Multiply: The Radiation of Darwin's Finches , 2011 .

[22]  David A. Rasmussen,et al.  Contributions of Flowering Time Genes to Sunflower Domestication and Improvement , 2011, Genetics.

[23]  J. Willis,et al.  A Widespread Chromosomal Inversion Polymorphism Contributes to a Major Life-History Transition, Local Adaptation, and Reproductive Isolation , 2010, PLoS biology.

[24]  J. Willis,et al.  Is local adaptation in Mimulus guttatus caused by trade‐offs at individual loci? , 2010, Molecular ecology.

[25]  A. Fernie,et al.  SlCCD7 controls strigolactone biosynthesis, shoot branching and mycorrhiza-induced apocarotenoid formation in tomato. , 2009, The Plant journal : for cell and molecular biology.

[26]  N. Warthmann,et al.  Cis-regulatory Changes at FLOWERING LOCUS T Mediate Natural Variation in Flowering Responses of Arabidopsis thaliana , 2009, Genetics.

[27]  E. Stone,et al.  The genetics of quantitative traits: challenges and prospects , 2009, Nature Reviews Genetics.

[28]  Gonçalo R. Abecasis,et al.  The Sequence Alignment/Map format and SAMtools , 2009, Bioinform..

[29]  J. Bowman,et al.  The flowering hormone florigen functions as a general systemic regulator of growth and termination , 2009, Proceedings of the National Academy of Sciences.

[30]  Richard Durbin,et al.  Sequence analysis Fast and accurate short read alignment with Burrows – Wheeler transform , 2009 .

[31]  Kosuke M. Teshima,et al.  Variations in Hd1 proteins, Hd3a promoters, and Ehd1 expression levels contribute to diversity of flowering time in cultivated rice , 2009, Proceedings of the National Academy of Sciences.

[32]  J. Willis,et al.  Ecological Reproductive Isolation of Coast and Inland Races of Mimulus guttatus , 2008, Evolution; international journal of organic evolution.

[33]  D. Goldstein,et al.  Which evolutionary processes influence natural genetic variation for phenotypic traits? , 2007, Nature Reviews Genetics.

[34]  M. Purugganan,et al.  The Genetic Architecture of Shoot Branching in Arabidopsis thaliana: A Comparative Assessment of Candidate Gene Associations vs. Quantitative Trait Locus Mapping , 2007, Genetics.

[35]  M. Kleunen Adaptive genetic differentiation in life-history traits between populations of Mimulus guttatus with annual and perennial life-cycles , 2007, Evolutionary Ecology.

[36]  J. Willis,et al.  DIVERGENT SELECTION ON FLOWERING TIME CONTRIBUTES TO LOCAL ADAPTATION IN MIMULUS GUTTATUS POPULATIONS , 2006, Evolution; international journal of organic evolution.

[37]  Qi Xie,et al.  The rice HIGH-TILLERING DWARF1 encoding an ortholog of Arabidopsis MAX3 is required for negative regulation of the outgrowth of axillary buds. , 2006, The Plant journal : for cell and molecular biology.

[38]  J. Willis,et al.  Pleiotropic Quantitative Trait Loci Contribute to Population Divergence in Traits Associated With Life-History Variation in Mimulus guttatus , 2006, Genetics.

[39]  C. Turnbull,et al.  MAX1 encodes a cytochrome P450 family member that acts downstream of MAX3/4 to produce a carotenoid-derived branch-inhibiting hormone. , 2005, Developmental cell.

[40]  O. Leyser,et al.  Shoot branching. , 2005, Annual review of plant biology.

[41]  LANDEl,et al.  THE GENETIC COVARIANCE BETWEEN CHARACTERS MAINTAINED BY PLEIOTROPIC MUTATIONS , 2003 .

[42]  B. Sinervo,et al.  Correlational selection and the evolution of genomic architecture , 2002, Heredity.

[43]  J. Willis,et al.  MINOR QUANTITATIVE TRAIT LOCI UNDERLIE FLORAL TRAITS ASSOCIATED WITH MATING SYSTEM DIVERGENCE IN MIMULUS , 2002, Evolution; international journal of organic evolution.

[44]  S. Via,et al.  The Genetic Architecture of Ecological Specialization: Correlated Gene Effects on Host Use and Habitat Choice in Pea Aphids , 2002, The American Naturalist.

[45]  G. Turner The Ecology of Adaptive Radiation , 2001, Heredity.

[46]  Burt,et al.  Natural selection in the wild. , 2000, Trends in ecology & evolution.

[47]  W. Ewens Genetics and analysis of quantitative traits , 1999 .

[48]  P. Diggle,et al.  Developmental analysis of the evolutionary origin of vegetative propagules in Mimulus gemmiparus (Scrophulariaceae). , 1999, American journal of botany.

[49]  D. Carr,et al.  THE RELATIONSHIP BETWEEN MATING‐SYSTEM CHARACTERS AND INBREEDING DEPRESSION IN MIMULUS GUTTATUS , 1997, Evolution; international journal of organic evolution.

[50]  R. Michelmore,et al.  Identification of markers linked to disease-resistance genes by bulked segregant analysis: a rapid method to detect markers in specific genomic regions by using segregating populations. , 1991, Proceedings of the National Academy of Sciences of the United States of America.

[51]  M. Geber THE COST OF MERISTEM LIMITATION IN POLYGONUM ARENASTRUM: NEGATIVE GENETIC CORRELATIONS BETWEEN FECUNDITY AND GROWTH , 1990, Evolution; international journal of organic evolution.

[52]  K. Ritland CORRELATED MATINGS IN THE PARTIAL SELFER MIMULUS GUTTATUS , 1989, Evolution; international journal of organic evolution.

[53]  M. Watson Developmental Constraints: Effect on Population Growth and Patterns of Resource Allocation in a Clonal Plant , 1984, The American Naturalist.

[54]  R. Lande The Genetic Covariance between Characters Maintained by Pleiotropic Mutations. , 1980, Genetics.

[55]  R. Primack Reproductive Effort in Annual and Perennial Species of Plantago (Plantaginaceae) , 1979, The American Naturalist.

[56]  R. Lande QUANTITATIVE GENETIC ANALYSIS OF MULTIVARIATE EVOLUTION, APPLIED TO BRAIN:BODY SIZE ALLOMETRY , 1979, Evolution; international journal of organic evolution.

[57]  R. K. Vickery Case Studies in the Evolution of Species Complexes in Mimulus , 1978 .

[58]  D. Tinkle,et al.  Natural selection and the evolution of reproductive effort. , 1975, Proceedings of the National Academy of Sciences of the United States of America.

[59]  Arthur Cronquist,et al.  Flora of the Pacific Northwest , 1974 .

[60]  J. Harper A Darwinian Approach to Plant Ecology , 1967 .