Standing variation rather than recent adaptive introgression probably underlies differentiation of the texanus subspecies of Helianthus annuus

The origins of geographic races in wide‐ranging species are poorly understood. In Texas, the texanus subspecies of Helianthus annuus has long been thought to have acquired its defining phenotypic traits via introgression from a local congener, H. debilis, but previous tests of this hypothesis were inconclusive. Here, we explore the origins of H. a. texanus using whole genome sequencing data from across the entire range of H. annuus and possible donor species, as well as phenotypic data from a common garden study. We found that although it is morphologically convergent with H. debilis, H. a. texanus has conflicting signals of introgression. Genome wide tests (Patterson's D and TreeMix) only found evidence of introgression from H. argophyllus (sister species to H. annuus and also sympatric), but not H. debilis, with the exception of one individual of 109 analysed. We further scanned the genome for localized signals of introgression using PCAdmix and found minimal but nonzero introgression from H. debilis and significant introgression from H. argophyllus in some populations. Given the paucity of introgression from H. debilis, we argue that the morphological convergence observed in Texas is probably from standing genetic variation. We also found that genomic differentiation in H. a. texanus is mostly driven by large segregating inversions, several of which have signatures of natural selection based on haplotype frequencies.

[1]  H. Hoekstra,et al.  A chromosomal inversion drives evolution of multiple adaptive traits in deer mice , 2021, bioRxiv.

[2]  L. Rieseberg,et al.  Ancestral Reconstruction of Karyotypes Reveals an Exceptional Rate of Nonrandom Chromosomal Evolution in Sunflower , 2020, Genetics.

[3]  Kohske Takahashi,et al.  Welcome to the Tidyverse , 2019, J. Open Source Softw..

[4]  L. Rieseberg,et al.  Multiple chromosomal inversions contribute to adaptive divergence of a dune sunflower ecotype , 2019, bioRxiv.

[5]  L. Rieseberg,et al.  Massive haplotypes underlie ecotypic differentiation in sunflowers , 2019, Nature.

[6]  L. Rieseberg,et al.  Intraspecific genetic divergence within Helianthus niveus and the status of two new morphotypes from Mexico. , 2019, American journal of botany.

[7]  L. Rieseberg,et al.  Hybridization speeds adaptive evolution in an eight-year field experiment , 2019, Scientific Reports.

[8]  Janet Kelso,et al.  admixr—R package for reproducible analyses using ADMIXTOOLS , 2019, Bioinform..

[9]  L. Rieseberg,et al.  An evaluation of alternative explanations for widespread cytonuclear discordance in annual sunflowers (Helianthus). , 2018, The New phytologist.

[10]  F. Jiggins,et al.  Adaptive introgression underlies polymorphic seasonal camouflage in snowshoe hares , 2018, Science.

[11]  L. Bernatchez,et al.  Eco-Evolutionary Genomics of Chromosomal Inversions. , 2018, Trends in ecology & evolution.

[12]  Daniel L. Powell,et al.  Natural selection interacts with recombination to shape the evolution of hybrid genomes , 2018, Science.

[13]  Q. Cronk,et al.  Adaptive introgression: a plant perspective , 2018, Biology Letters.

[14]  M. Kirkpatrick,et al.  Chromosome Inversions, Local Adaptation and Speciation , 2017, Genetics.

[15]  Simon H. Martin,et al.  Interpreting the genomic landscape of introgression. , 2017, Current opinion in genetics & development.

[16]  Ying Zhou,et al.  Models, methods and tools for ancestry inference and admixture analysis , 2017, Quantitative Biology.

[17]  L. Rieseberg,et al.  The sunflower genome provides insights into oil metabolism, flowering and Asterid evolution , 2017, Nature.

[18]  R. Burri Interpreting differentiation landscapes in the light of long-term linked selection , 2017, bioRxiv.

[19]  Dan G. Bock,et al.  Genome-wide genotyping-by-sequencing data provide a high-resolution view of wild Helianthus diversity, genetic structure, and interspecies gene flow. , 2016, American journal of botany.

[20]  Brook T. Moyers,et al.  Remarkable life history polymorphism may be evolving under divergent selection in the silverleaf sunflower , 2016, Molecular ecology.

[21]  Caroline M. Weisman,et al.  Borrowed alleles and convergence in serpentine adaptation , 2016, Proceedings of the National Academy of Sciences.

[22]  L. Rieseberg,et al.  Revisiting a classic case of introgression: hybridization and gene flow in Californian sunflowers , 2016, Molecular ecology.

[23]  J. Josse,et al.  missMDA: A Package for Handling Missing Values in Multivariate Data Analysis , 2016 .

[24]  Chrystian C. Sosa,et al.  Ecogeography and utility to plant breeding of the crop wild relatives of sunflower (Helianthus annuus L.) , 2015, Front. Plant Sci..

[25]  M. Jakobsson,et al.  Clumpak: a program for identifying clustering modes and packaging population structure inferences across K , 2015, Molecular ecology resources.

[26]  L. Donovan,et al.  Species tree estimation of diploid Helianthus (Asteraceae) using target enrichment. , 2015, American journal of botany.

[27]  Simon H. Martin,et al.  Evaluating the Use of ABBA–BABA Statistics to Locate Introgressed Loci , 2014, bioRxiv.

[28]  L. Rieseberg,et al.  Chromosomal Evolution and Patterns of Introgression in Helianthus , 2014, Genetics.

[29]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[30]  L. Rieseberg,et al.  HYBRID INCOMPATIBILITY IS ACQUIRED FASTER IN ANNUAL THAN IN PERENNIAL SPECIES OF SUNFLOWER AND TARWEED , 2014, Evolution; international journal of organic evolution.

[31]  A. Hoffmann,et al.  GENETIC ISOLATION BY ENVIRONMENT OR DISTANCE: WHICH PATTERN OF GENE FLOW IS MOST COMMON? , 2014, Evolution; international journal of organic evolution.

[32]  Kazuki Saito,et al.  The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. , 2013, Plant physiology and biochemistry : PPB.

[33]  Arndt von Haeseler,et al.  NextGenMap: fast and accurate read mapping in highly polymorphic genomes , 2013, Bioinform..

[34]  Mauricio O. Carneiro,et al.  From FastQ Data to High‐Confidence Variant Calls: The Genome Analysis Toolkit Best Practices Pipeline , 2013, Current protocols in bioinformatics.

[35]  L. Rieseberg,et al.  DIVERGENCE IS FOCUSED ON FEW GENOMIC REGIONS EARLY IN SPECIATION: INCIPIENT SPECIATION OF SUNFLOWER ECOTYPES , 2013, Evolution; international journal of organic evolution.

[36]  David Levine,et al.  A high-performance computing toolset for relatedness and principal component analysis of SNP data , 2012, Bioinform..

[37]  Swapan Mallick,et al.  Ancient Admixture in Human History , 2012, Genetics.

[38]  G. Coop,et al.  Robust Identification of Local Adaptation from Allele Frequencies , 2012, Genetics.

[39]  Jake K. Byrnes,et al.  PCAdmix: Principal Components-Based Assignment of Ancestry Along Each Chromosome in Individuals with Admixed Ancestry from Two or More Populations , 2012, Human biology.

[40]  Benjamin M. Fitzpatrick Estimating ancestry and heterozygosity of hybrids using molecular markers , 2012, BMC Evolutionary Biology.

[41]  M. Stephens,et al.  Genome-wide Efficient Mixed Model Analysis for Association Studies , 2012, Nature Genetics.

[42]  Jared L. Strasburg,et al.  RECONCILING EXTREMELY STRONG BARRIERS WITH HIGH LEVELS OF GENE EXCHANGE IN ANNUAL SUNFLOWERS , 2012, Evolution; international journal of organic evolution.

[43]  Joseph K. Pickrell,et al.  Inference of Population Splits and Mixtures from Genome-Wide Allele Frequency Data , 2012, PLoS genetics.

[44]  M. Nachman,et al.  Recombination rate variation and speciation: theoretical predictions and empirical results from rabbits and mice , 2012, Philosophical Transactions of the Royal Society B: Biological Sciences.

[45]  Heng Li,et al.  A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data , 2011, Bioinform..

[46]  David H. Alexander,et al.  Enhancements to the ADMIXTURE algorithm for individual ancestry estimation , 2011, BMC Bioinformatics.

[47]  L. Rieseberg,et al.  Adaptive introgression of abiotic tolerance traits in the sunflower Helianthus annuus. , 2010, The New phytologist.

[48]  L. Rieseberg,et al.  Genome scan of hybridizing sunflowers from Texas (Helianthus annuus and H. debilis) reveals asymmetric patterns of introgression and small islands of genomic differentiation , 2010, Molecular ecology.

[49]  Michael S. Barker,et al.  Comparative Genomic and Population Genetic Analyses Indicate Highly Porous Genomes and High Levels of Gene Flow between Divergent Helianthus Species , 2009, Evolution; international journal of organic evolution.

[50]  Jared L. Strasburg,et al.  Molecular Demographic History Oo the Annual Sunflowers Helianthus Annuus and H. Petiolaris—Large Effective Population Sizes and Rates of Long-Term Gene Flow , 2008, Evolution; international journal of organic evolution.

[51]  Sébastien Lê,et al.  FactoMineR: An R Package for Multivariate Analysis , 2008 .

[52]  B. Browning,et al.  Rapid and accurate haplotype phasing and missing-data inference for whole-genome association studies by use of localized haplotype clustering. , 2007, American journal of human genetics.

[53]  Manuel A. R. Ferreira,et al.  PLINK: a tool set for whole-genome association and population-based linkage analyses. , 2007, American journal of human genetics.

[54]  L. Rieseberg,et al.  Rampant Gene Exchange Across a Strong Reproductive Barrier Between the Annual Sunflowers, Helianthus annuus and H. petiolaris , 2007, Genetics.

[55]  L. Rieseberg,et al.  Hybridization and the colonization of novel habitats by annual sunflowers , 2007, Genetica.

[56]  L. Rieseberg,et al.  Adaptive Introgression of Herbivore Resistance Traits in the Weedy Sunflower Helianthus annuus , 2006, The American Naturalist.

[57]  P. Donnelly,et al.  Inference of population structure using multilocus genotype data. , 2000, Genetics.

[58]  L. Rieseberg,et al.  PATTERNS OF MATING IN WILD SUNFLOWER HYBRID ZONES , 1998, Evolution; international journal of organic evolution.

[59]  C. Jan,et al.  Chromosomal Differentiation among the Annual Helianthus Species , 1986 .

[60]  J. Chandler,et al.  Transfer of Powdery Mildew Resistance from Helianthus debilis Nutt. to Cultivated Sunflower 1 , 1985 .

[61]  B. Weir,et al.  ESTIMATING F‐STATISTICS FOR THE ANALYSIS OF POPULATION STRUCTURE , 1984, Evolution; international journal of organic evolution.

[62]  C. Heiser HYBRIDIZATION IN THE ANNUAL SUNFLOWERS: HELIANTHUS ANNUUS x H. DEBILIS VAR. CUCUMERIFOLIUS , 1951 .

[63]  C. Heiser Hybridization in the Annual Sunflowers: Helianthus annuus x H. argophyllus , 1951, The American Naturalist.

[64]  C. Heiser HYBRIDIZATION BETWEEN THE SUNFLOWER SPECIES HELIANTHUS ANNUUS AND H. PETIOLARIS , 1947 .

[65]  S. Wright,et al.  Isolation by Distance. , 1943, Genetics.

[66]  R Core Team,et al.  R: A language and environment for statistical computing. , 2014 .

[67]  John S. Heywood,et al.  SPATIAL ANALYSIS OF GENETIC VARIATION IN PLANT POPULATIONS , 1991 .

[68]  L. Rieseberg,et al.  Helianthus annuus ssp. texanus has chloroplast DNA and nuclear ribosomal RNA genes of Helianthus debilis ssp. cucumerifolius. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[69]  D. Smith,et al.  The North American sunflowers (Helianthus) , 1969 .

[70]  C. Heiser Variation and Subspeciation in the Common Sunflower, Helianthus Annuus , 1954 .