A Widespread Chromosomal Inversion Polymorphism Contributes to a Major Life-History Transition, Local Adaptation, and Reproductive Isolation
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{"title"=>"A widespread chromosomal inversion polymorphism contributes to a major life-history transition, local adaptation, and reproductive isolation", "type"=>"journal", "authors"=>[{"first_name"=>"David B.", "last_name"=>"Lowry", "scopus_author_id"=>"24577746300"}, {"first_name"=>"John H.", "last_name"=>"Willis", "scopus_author_id"=>"7402590016"}], "year"=>2010, "source"=>"PLoS Biology", "identifiers"=>{"scopus"=>"2-s2.0-77957898021", "sgr"=>"77957898021", "issn"=>"15449173", "doi"=>"10.1371/journal.pbio.1000500", "pmid"=>"20927411", "isbn"=>"15449173", "pui"=>"359761822"}, "id"=>"33e22d1a-8703-3a69-ba63-8ed94cca6b52", "abstract"=>"The role of chromosomal inversions in adaptation and speciation is controversial. Historically, inversions were thought to contribute to these processes either by directly causing hybrid sterility or by facilitating the maintenance of co-adapted gene complexes. Because inversions suppress recombination when heterozygous, a recently proposed local adaptation mechanism predicts that they will spread if they capture alleles at multiple loci involved in divergent adaptation to contrasting environments. Many empirical studies have found inversion polymorphisms linked to putatively adaptive phenotypes or distributed along environmental clines. However, direct involvement of an inversion in local adaptation and consequent ecological reproductive isolation has not to our knowledge been demonstrated in nature. In this study, we discovered that a chromosomal inversion polymorphism is geographically widespread, and we test the extent to which it contributes to adaptation and reproductive isolation under natural field conditions. Replicated crosses between the prezygotically reproductively isolated annual and perennial ecotypes of the yellow monkeyflower, Mimulus guttatus, revealed that alternative chromosomal inversion arrangements are associated with life-history divergence over thousands of kilometers across North America. The inversion polymorphism affected adaptive flowering time divergence and other morphological traits in all replicated crosses between four pairs of annual and perennial populations. To determine if the inversion contributes to adaptation and reproductive isolation in natural populations, we conducted a novel reciprocal transplant experiment involving outbred lines, where alternative arrangements of the inversion were reciprocally introgressed into the genetic backgrounds of each ecotype. Our results demonstrate for the first time in nature the contribution of an inversion to adaptation, an annual/perennial life-history shift, and multiple reproductive isolating barriers. These results are consistent with the local adaptation mechanism being responsible for the distribution of the two inversion arrangements across the geographic range of M. guttatus and that locally adaptive inversion effects contribute directly to reproductive isolation. Such a mechanism may be partially responsible for the observation that closely related species often differ by multiple chromosomal rearrangements.", "link"=>"http://www.mendeley.com/research/widespread-chromosomal-inversion-polymorphism-contributes-major-lifehistory-transition-local-adaptat", "reader_count"=>384, "reader_count_by_academic_status"=>{"Unspecified"=>5, "Professor > Associate Professor"=>33, "Researcher"=>90, "Student > Doctoral Student"=>13, "Student > Ph. D. 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Student"=>121, "Student > Postgraduate"=>17, "Student > Master"=>40, "Other"=>7, "Student > Bachelor"=>31, "Lecturer"=>3, "Lecturer > Senior Lecturer"=>1, "Professor"=>23}, "reader_count_by_subject_area"=>{"Unspecified"=>7, "Agricultural and Biological Sciences"=>316, "Philosophy"=>1, "Arts and Humanities"=>12, "Business, Management and Accounting"=>1, "Computer Science"=>1, "Earth and Planetary Sciences"=>1, "Economics, Econometrics and Finance"=>1, "Environmental Science"=>12, "Biochemistry, Genetics and Molecular Biology"=>26, "Mathematics"=>1, "Medicine and Dentistry"=>2, "Neuroscience"=>1, "Psychology"=>1, "Social Sciences"=>1}, "reader_count_by_subdiscipline"=>{"Medicine and Dentistry"=>{"Medicine and Dentistry"=>2}, "Social Sciences"=>{"Social Sciences"=>1}, "Psychology"=>{"Psychology"=>1}, "Mathematics"=>{"Mathematics"=>1}, "Unspecified"=>{"Unspecified"=>7}, "Environmental Science"=>{"Environmental Science"=>12}, "Arts and Humanities"=>{"Arts and Humanities"=>12}, "Neuroscience"=>{"Neuroscience"=>1}, "Earth and Planetary Sciences"=>{"Earth and Planetary Sciences"=>1}, "Economics, Econometrics and Finance"=>{"Economics, Econometrics and Finance"=>1}, "Agricultural and Biological Sciences"=>{"Agricultural and Biological Sciences"=>316}, "Computer Science"=>{"Computer Science"=>1}, "Business, Management and Accounting"=>{"Business, Management and Accounting"=>1}, "Biochemistry, Genetics and Molecular Biology"=>{"Biochemistry, Genetics and Molecular Biology"=>26}, "Philosophy"=>{"Philosophy"=>1}}, "reader_count_by_country"=>{"Romania"=>1, "United States"=>23, "Japan"=>1, "United Kingdom"=>5, "Switzerland"=>3, "Portugal"=>2, "Spain"=>3, "Canada"=>6, "Sweden"=>1, "Netherlands"=>1, "Norway"=>1, "Denmark"=>1, "Brazil"=>1, "Uganda"=>1, "Italy"=>1, "South Africa"=>1, "Mexico"=>1, "France"=>1, "Germany"=>2}, "group_count"=>19}

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  • {"files"=>["https://ndownloader.figshare.com/files/827450"], "description"=>"<p>For each trait: the additive effect (2a), dominance deviation (d), and the proportion of the parental population divergence explained (2a/diff).</p><p>*<i>p</i><0.05, **<i>p</i><0.01, ***<i>p</i><0.001, ****<i>p</i><0.0001.</p>", "links"=>[], "tags"=>["inversion", "locus", "flowering", "morphological"], "article_id"=>497819, "categories"=>["Ecology", "Evolutionary Biology", "Medicine", "Genetics"], "users"=>["David B. Lowry", "John H. Willis"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000500.t001", "stats"=>{"downloads"=>0, "page_views"=>3, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_The_effects_of_the_inversion_locus_on_flowering_time_and_morphological_traits_in_the_greenhouse_/497819", "title"=>"The effects of the inversion locus on flowering time and morphological traits in the greenhouse.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-09-28 02:10:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/827389"], "description"=>"a<p>Number of individuals planted per genotype.</p>b<p>Mean (±SE) number of days to first flower.</p>c<p>Percentage of plants surviving to flower.</p>d<p>Mean (±SE) number of flowers produced per plant surviving to flower.</p>e<p>Expected number of flowers (±SE) per plant at start of experiment calculated with ASTER.</p>f<p>Percentage of plants still alive at the end of the first field season.</p>g<p>Percentage of plants surviving to the end of the first season that had not yet flowered.</p>", "links"=>[], "tags"=>["inversion", "locus", "components", "reciprocal", "transplant"], "article_id"=>497754, "categories"=>["Ecology", "Evolutionary Biology", "Medicine", "Genetics"], "users"=>["David B. Lowry", "John H. Willis"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000500.t002", "stats"=>{"downloads"=>0, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_the_inversion_locus_on_components_of_fitness_in_the_field_reciprocal_transplant_experiment_/497754", "title"=>"Effects of the inversion locus on components of fitness in the field reciprocal transplant experiment.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-09-28 02:09:14"}
  • {"files"=>["https://ndownloader.figshare.com/files/827151"], "description"=>"<p>Crossing design for production of backcross lines with the LMC (shades of yellow/orange) genetic background. Breeding of plants with SWB (shades of blue) genetic background not shown. Note that the size of introgressed region around the inversion should vary among lines due to different recombination locations during breeding. Different shades are used to indicate that original parental inbred lines have a unique genetic composition. (A) Three pairs of independently derived inbred LMC and SWB lines were crossed to create F1 progeny. (B) F1s backcrossed to parental inbred lines. (C) Marker-assisted selection used for four generations of backcrossing to move the inversion into alternate genetic backgrounds. (D) Heterozygous lines were self-fertilized. (E) Backcross lines that are homozygous with (blue oval) and without (orange oval) the introgressed inversion arrangements were selected for further breeding. (F) Intercrosses conducted among the three independent groups to create outbred backcross lines with and without the introgressed inverted region. (G) Backcrossed lines now ready to be planted into field reciprocal transplant experiment.</p>", "links"=>[], "tags"=>["backcross", "introgression"], "article_id"=>497519, "categories"=>["Ecology", "Evolutionary Biology", "Medicine", "Genetics"], "users"=>["David B. Lowry", "John H. Willis"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000500.g003", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Breeding_design_for_creation_of_backcross_introgression_lines_/497519", "title"=>"Breeding design for creation of backcross introgression lines.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-09-28 02:05:19"}
  • {"files"=>["https://ndownloader.figshare.com/files/412197", "https://ndownloader.figshare.com/files/412211", "https://ndownloader.figshare.com/files/412220", "https://ndownloader.figshare.com/files/412227", "https://ndownloader.figshare.com/files/412247", "https://ndownloader.figshare.com/files/412271", "https://ndownloader.figshare.com/files/412278", "https://ndownloader.figshare.com/files/412281", "https://ndownloader.figshare.com/files/412287"], "description"=>"<div><p>The role of chromosomal inversions in adaptation and speciation is controversial. Historically, inversions were thought to contribute to these processes either by directly causing hybrid sterility or by facilitating the maintenance of co-adapted gene complexes. Because inversions suppress recombination when heterozygous, a recently proposed local adaptation mechanism predicts that they will spread if they capture alleles at multiple loci involved in divergent adaptation to contrasting environments. Many empirical studies have found inversion polymorphisms linked to putatively adaptive phenotypes or distributed along environmental clines. However, direct involvement of an inversion in local adaptation and consequent ecological reproductive isolation has not to our knowledge been demonstrated in nature. In this study, we discovered that a chromosomal inversion polymorphism is geographically widespread, and we test the extent to which it contributes to adaptation and reproductive isolation under natural field conditions. Replicated crosses between the prezygotically reproductively isolated annual and perennial ecotypes of the yellow monkeyflower, <em>Mimulus guttatus</em>, revealed that alternative chromosomal inversion arrangements are associated with life-history divergence over thousands of kilometers across North America. The inversion polymorphism affected adaptive flowering time divergence and other morphological traits in all replicated crosses between four pairs of annual and perennial populations. To determine if the inversion contributes to adaptation and reproductive isolation in natural populations, we conducted a novel reciprocal transplant experiment involving outbred lines, where alternative arrangements of the inversion were reciprocally introgressed into the genetic backgrounds of each ecotype. Our results demonstrate for the first time in nature the contribution of an inversion to adaptation, an annual/perennial life-history shift, and multiple reproductive isolating barriers. These results are consistent with the local adaptation mechanism being responsible for the distribution of the two inversion arrangements across the geographic range of <em>M. guttatus</em> and that locally adaptive inversion effects contribute directly to reproductive isolation. Such a mechanism may be partially responsible for the observation that closely related species often differ by multiple chromosomal rearrangements.</p></div>", "links"=>[], "tags"=>["chromosomal", "inversion", "polymorphism", "contributes", "life-history", "reproductive"], "article_id"=>141422, "categories"=>["Ecology", "Evolutionary Biology", "Medicine", "Genetics"], "users"=>["David B. Lowry", "John H. Willis"], "doi"=>["https://dx.doi.org/10.1371/journal.pbio.1000500.s001", "https://dx.doi.org/10.1371/journal.pbio.1000500.s002", "https://dx.doi.org/10.1371/journal.pbio.1000500.s003", "https://dx.doi.org/10.1371/journal.pbio.1000500.s004", "https://dx.doi.org/10.1371/journal.pbio.1000500.s005", "https://dx.doi.org/10.1371/journal.pbio.1000500.s006", "https://dx.doi.org/10.1371/journal.pbio.1000500.s007", "https://dx.doi.org/10.1371/journal.pbio.1000500.s008", "https://dx.doi.org/10.1371/journal.pbio.1000500.s009"], "stats"=>{"downloads"=>1, "page_views"=>28, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/A_Widespread_Chromosomal_Inversion_Polymorphism_Contributes_to_a_Major_Life_History_Transition_Local_Adaptation_and_Reproductive_Isolation/141422", "title"=>"A Widespread Chromosomal Inversion Polymorphism Contributes to a Major Life-History Transition, Local Adaptation, and Reproductive Isolation", "pos_in_sequence"=>0, "defined_type"=>4, "published_date"=>"2010-09-28 00:23:42"}
  • {"files"=>["https://ndownloader.figshare.com/files/826926"], "description"=>"<p>(A) Map of western North America with the locations of populations of coastal perennials (blue), inland annuals (orange), and inland perennials (purple), as well as obligate self-fertilizing species <i>M. nasutus</i> (yellow). (B) Marker order of the AN and PE inversion arrangements along linkage group eight. Inland annuals and <i>M. nasutus</i> had the AN arrangement while coastal and inland perennials all had the PE arrangement.</p>", "links"=>[], "tags"=>["chromosomal"], "article_id"=>497291, "categories"=>["Ecology", "Evolutionary Biology", "Medicine", "Genetics"], "users"=>["David B. Lowry", "John H. Willis"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000500.g001", "stats"=>{"downloads"=>1, "page_views"=>2, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Geographic_distribution_of_the_chromosomal_inversion_/497291", "title"=>"Geographic distribution of the chromosomal inversion.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-09-28 02:01:31"}
  • {"files"=>["https://ndownloader.figshare.com/files/827224"], "description"=>"<p>(A) Proportion of plants surviving to flower and (B) expected fitness produced per plants across field sites. Values plotted are maximum likelihood estimates ±1 SE calculated with ASTER. (C) Cumulative proportion of plants surviving to flower and (D) expected fitness per individual at the inland field site. Survival over time at the (E) coastal perennial and (F) inland annual field sites. Parental lines: yellow, inland annual parent; blue, coastal perennial parent. Backcross lines: orange, PE arrangement in annual genetic background; red, AN arrangement in annual genetic background; green, AN arrangement in perennial genetic background; pink, PE arrangement in perennial genetic background.</p>", "links"=>[], "tags"=>["inversion", "locus", "sites"], "article_id"=>497596, "categories"=>["Ecology", "Evolutionary Biology", "Medicine", "Genetics"], "users"=>["David B. Lowry", "John H. Willis"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000500.g004", "stats"=>{"downloads"=>1, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_the_inversion_locus_across_field_sites_in_different_genetic_backgrounds_/497596", "title"=>"Effects of the inversion locus across field sites in different genetic backgrounds.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-09-28 02:06:36"}
  • {"files"=>["https://ndownloader.figshare.com/files/827315"], "description"=>"<p>Tests of the inversion locus effect on survival over the course of the season using ASTER, where survival is modeled with the following directional graph: 1 -> survival at census one -> survival at census two -> … -> survival at census x, where x = 16 for the inland field site and 11 for the coastal field site.</p>", "links"=>[], "tags"=>["inversion"], "article_id"=>497689, "categories"=>["Ecology", "Evolutionary Biology", "Medicine", "Genetics"], "users"=>["David B. Lowry", "John H. Willis"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000500.t004", "stats"=>{"downloads"=>1, "page_views"=>6, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Effects_of_inversion_on_survival_over_the_field_season_at_each_field_site_/497689", "title"=>"Effects of inversion on survival over the field season at each field site.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-09-28 02:08:09"}
  • {"files"=>["https://ndownloader.figshare.com/files/827350"], "description"=>"a<p>Overall reproductive isolation between inland annual and coastal perennial ecological races at coast or inland field sites.</p>b<p>The individual locus contribution to reproductive isolation by the inversion at the coast or inland field sites.</p>c<p>Quantified separately at the coast field site for two fitness components: expected number of flowers/survival to second season.</p>", "links"=>[], "tags"=>["reproductive", "isolating", "barriers"], "article_id"=>497720, "categories"=>["Ecology", "Evolutionary Biology", "Medicine", "Genetics"], "users"=>["David B. Lowry", "John H. Willis"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000500.t005", "stats"=>{"downloads"=>0, "page_views"=>8, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Overall_strength_of_reproductive_isolating_barriers_and_individual_contribution_by_the_inversion_/497720", "title"=>"Overall strength of reproductive isolating barriers and individual contribution by the inversion.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-09-28 02:08:40"}
  • {"files"=>["https://ndownloader.figshare.com/files/827419"], "description"=>"<p>Factors tested with ASTER using the composite of two dependent components of fitness, survival to flowering, and number of flowers produced, with the following directional graph: 1 -> survival to flowering -> number of flowers produced. All factors are tested by likelihood ratio tests using nested null models.</p>", "links"=>[], "tags"=>["inversion", "locus"], "article_id"=>497788, "categories"=>["Ecology", "Evolutionary Biology", "Medicine", "Genetics"], "users"=>["David B. Lowry", "John H. Willis"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000500.t003", "stats"=>{"downloads"=>1, "page_views"=>4, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Analysis_of_effect_of_genetic_background_field_site_and_inversion_locus_by_ASTER_/497788", "title"=>"Analysis of effect of genetic background, field site, and inversion locus by ASTER.", "pos_in_sequence"=>0, "defined_type"=>3, "published_date"=>"2010-09-28 02:09:48"}
  • {"files"=>["https://ndownloader.figshare.com/files/827054"], "description"=>"<p>(A) F2 progeny with parental ecotypic phenotypes, from a cross between the SWB (coastal perennial) and LMC (inland annual) populations. (B–E) Effect of the inversion on flowering time in four independently derived F2 mapping populations created through crosses between independent inland annual and coastal perennial populations. (F) Effects of the inversion on flowering time in cross between inland annual and inland perennial populations. The mean flowering times (±1 SE) of F2s that were homozygous for the AN arrangement (AA), heterozygous (AB), and homozygous for the PE arrangement (BB) at Micro6046 are indicated. The percentage of F2 variance/parental divergence explained by the inversion is presented above each bar graph. Note: <i>y</i>-axes do not originate at zero.</p>", "links"=>[], "tags"=>["inversion"], "article_id"=>497433, "categories"=>["Ecology", "Evolutionary Biology", "Medicine", "Genetics"], "users"=>["David B. Lowry", "John H. Willis"], "doi"=>"https://dx.doi.org/10.1371/journal.pbio.1000500.g002", "stats"=>{"downloads"=>0, "page_views"=>7, "likes"=>0}, "figshare_url"=>"https://figshare.com/articles/_Replicated_effect_of_the_inversion_locus_/497433", "title"=>"Replicated effect of the inversion locus.", "pos_in_sequence"=>0, "defined_type"=>1, "published_date"=>"2010-09-28 02:03:53"}

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