Gene flow and cross-incompatibility in maize and teosinte
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Maize and teosinte introgression, gametophytic factors, cross-incompatibility, adaptation.
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Gene flow and cross-incompatibility in maize and teosinte
- 1. Adaptive (and not so adaptive) introgression between maize and teosinte Jeffrey Ross-Ibarra @jrossibarra • www.rilab.org Dept. Plant Sciences • Center for Population Biology • Genome Center University of California Davis photo by lady_lbrty
- 2. Servedio 2004 PloS Bio
- 3. Hopkins 2013 New Phyt.Servedio 2004 PloS Bio
- 4. Hopkins 2013 New Phyt.Servedio 2004 PloS Bio with little population differentiation, even though trait frequencies may differ greatly due to local adaptation. This creates relatively greater mating opportunities for foreign, rare males in each pop- ulation, directly countering the effects of local adaptation and re- ducing population differentiation at a trait locus. Importantly, stronger preferences exaggerate this effect. Fisherian sexual selec- tion is thus a double-edged sword in the development of isolation under these conditions, potentially driving differentiation in allop- atry but removing it if there is contact. Ultimately its role in allo- patric speciation is tenuous, failing even if contact is initiated after substantive trait and preference divergence has occurred. Model and Results We consider a two-locus population genetic model with polygyny (Methods). Locus T has alleles T1 and T2, which control two sexually selected phenotypes in males. Locus P determines a fe- male preference; P1 females are 1 + α1 times as likely to mate with a T1 than a T2 male upon encounter, whereas P2 females similarly prefer T2 males with preference strength 1 + α2. Our basic model, in accordance with the Fisherian models of Lande (4) and Kirkpatrick (13), does not include costs to preferences (this assumption is varied below). Our models are haploid to facilitate analyses, but the key factors that lead to our qualitative results should be readily generalizable to diploids. We assume that two allopatric populations have diverged such that individ- uals in population 1 have primarily P1 and T1 alleles and those in population 2 have primarily P2 and T2 alleles. Secondary contact occurs between these populations by symmetric migration with rate m. The onset of migration leads to variation in preferences and traits within each population, and linkage disequilibrium Fig. 1. Male trait and female preference frequencies show a decrease i their differentiation between populations when sexual selection is strong Servedio and Bürger 2014 PNAS
- 6. Beadle 1979 Field Museum of Natural History parviglumis mays
- 9. ssp. mexicana ssp. parviglumis ssp. mays Matsuoka et al. 2002 PNAS Piperno et al. 2009 PNAS the presence of maize (Table 2; Fig. 1); for comparison, Fig. S1A–C shows modern teosinte and maize starch grains. For example, the grains isolated from the preceramic- and ceramic- Fig. 1. Starch grains from maize recovered from early preceramic grinding stones 318d (A and B) and 318e (C and D). The grains have irregular shapes and surface contours, along with defined compression facets and transverse fis- sures (A) or y-shaped and other fissures (B–D). Table 2. Morphology of maize starch grains recovered from the Xihu Provenience Tool Cat. no. Shape Round Oval Bell Irregular Unit 1 Ceramic Layer B 310a 0 17 0 83 312a 0 0 0 100 Layer C 314c 46 0 0 54 315c 11 0 0 89 Preceramic Layer D 316c 0 0 0 100 316d 9 0 3 88 Layer E 318e 13 1 0 86 318d 5 0 0 90 319d 12 0 0 88 322c 9 0 0 91 Unit 2 Ceramic
- 10. ssp. mexicana ssp. parviglumis ssp. mays Matsuoka et al. 2002 PNAS Piperno et al. 2009 PNAS the presence of maize (Table 2; Fig. 1); for comparison, Fig. S1A–C shows modern teosinte and maize starch grains. For example, the grains isolated from the preceramic- and ceramic- Fig. 1. Starch grains from maize recovered from early preceramic grinding stones 318d (A and B) and 318e (C and D). The grains have irregular shapes and surface contours, along with defined compression facets and transverse fis- sures (A) or y-shaped and other fissures (B–D). Table 2. Morphology of maize starch grains recovered from the Xihu Provenience Tool Cat. no. Shape Round Oval Bell Irregular Unit 1 Ceramic Layer B 310a 0 17 0 83 312a 0 0 0 100 Layer C 314c 46 0 0 54 315c 11 0 0 89 Preceramic Layer D 316c 0 0 0 100 316d 9 0 3 88 Layer E 318e 13 1 0 86 318d 5 0 0 90 319d 12 0 0 88 322c 9 0 0 91 Unit 2 Ceramic
- 11. mexicana parviglumis South/Caribbean West Highland 0 500 1000 1500 2000 2500 m van Heerwaarden et al. 2011 PNAS clearly separated clusters, but evidence of admixture is inferred from domesticated maize alone. Because the genetic Fig. 1. (A) Map of sampled maize accessions colored by genetic group. (B) First three genetic PCs of all sampled accessions. EVOLUTION altitude mexicana parviglumis mays
- 12. mexicana parviglumis Lauter et al. (2004) Genetics Pyhäjärvi et al. GBE 2013 Lauter et al. 2004 Genetics 0 10 20 30 40 60 80 100 120 days to pollen count subpsecies parviglumis mexicana Rodriguez et al. (2006) Maydica
- 13. Environmental Association for temperature/altitude mexicana parviglumis Lauter et al. (2004) Genetics Pyhäjärvi et al. GBE 2013 Lauter et al. 2004 Genetics
- 14. Days to Flowering highlandlowland daystoflowering HiLo field trials 2014,2016 (unpublished) Lowland Highland Photos: Ruairidh Sawers, LANGEBIO Lowland Field Highland Field
- 15. Days to Flowering highlandlowland daystoflowering HiLo field trials 2014,2016 (unpublished) Lowland Highland Photos: Ruairidh Sawers, LANGEBIO Lowland Field Highland Field
- 16. Days to Flowering highlandlowland daystoflowering HiLo field trials 2014,2016 (unpublished) Lowland Highland Photos: Ruairidh Sawers, LANGEBIO Lowland Field Highland Field
- 18. K = 2 K = 5 K = 4 K = 3 mexicana maize references K = 7 K = 8 K = 9 K = 10 Hufford et al. 2013 PLoS GeneGcs
- 20. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS GeneGcs low elevation maize mexicana allele
- 21. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS GeneGcs low elevation maize mexicana allele
- 22. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS GeneGcs low elevation maize mexicana allele
- 23. El Porvenir Opopeo Xochimilco Puruandiro Tenango del Aire Ixtlan Nabogame Santa Clara San Pedro Allopatric Hufford et al. 2013 PLoS GeneGcs low elevation maize mexicana allele0 1000 2000 3000 4000 5000 -447000 generations com 0 1000 2000 3000 4000 5000 -452000-450000 Santa Clara Likelihoods generations comp.loglikelihood 0 1000 2000 3000 4000 5000 -40650 generations com 0 1000 2000 3000 4000 5000 -420000-418500 Puruandiro Likelihoods generations comp.loglikelihood 0 1000 2000 3000 -418000 generations com 0 1000 2000 3000 -418000-416500 Opopeo Likelihoo generations comp.loglikelihood 55500-254000 San Pedro Likelihoods comp.loglikelihood 0000-288000 El Porvenir Likelihoods comp.loglikelihood -311500-310000 Ixtlan Likelihood comp.loglikelihood B 0 1000 2000 3000 4000 5000 -292 generations com 0 1000 2000 3000 4000 5000 -293000-291500-290000 Santa Clara Likelihoods generations comp.loglikelihood 0 1000 2000 300 -296500 generations com 0 1000 2000 300 -286000-284000 Puruandiro Like generations comp.loglikelihood maize into mexicana mexicana into maize generations since admixture
- 25. 0 50 100 150 200 250 300 0.00.6 Chromosome 1 bp proportionofpopulations 0 50 100 150 200 0.00.6 Chromosome 2 bp proportionofpopulations 0 50 100 1 0.00.6 Chromosome 6 bp proportionofpopulations 0 50 100 150 0.00.6 Chromosome 7 bp proportionofpopulations Mb Mb MbMb B gt1 tb1bif2 zfl2 pbf1 zag1 ra1 Chr1: mexicana to maize 1-admixture Photo by Anna O’Brien Hufford et al. 2013 PLoS GeneGcs
- 26. 0 50 100 150 200 0.00.6 Chromosome 3 bp proportionofpopulations 0 50 100 150 200 250 0.00.6 Chromosome 4 bp proportionofpopulations 0 50 100 15 0.00.6 Chromosome 8 bp proportionofpopulations 0 50 100 0.00.6 Chromosome 9 bp proportionofpopulations Mb Mb Mb Mb zag2 ba1 su1 tga1 bt2ga1 tcb1 Mb Chr4: maize to mexicana 0 50 100 150 200 250 300 0.00.6 Chromosome 1 bp proportionofpopulations 0 50 100 150 200 0.00.6 Chromosome 2 bp proportionofpopulations 0 50 100 1 0.00.6 Chromosome 6 bp proportionofpopulations 0 50 100 150 0.00.6 Chromosome 7 bp proportionofpopulations Mb Mb MbMb B gt1 tb1bif2 zfl2 pbf1 zag1 ra1 Chr1: mexicana to maize 1-admixture Photo by Anna O’Brien Hufford et al. 2013 PLoS GeneGcs
- 27. Photo: U. Nebraska-Lincoln ♀silk Photo: Tarek Siala ♂tassel Photo: Henry Mühlpfordt Pollen Pistil M m F- ✓ ✗ ff ✓ ✓ F/f M/m tcb1
- 28. Photo: U. Nebraska-Lincoln ♀silk Photo: Tarek Siala ♂tassel Photo: Henry Mühlpfordt Pollen Pistil M m F- ✓ ✗ ff ✓ ✓ F/f M/m tcb1
- 29. Photo: U. Nebraska-Lincoln ♀silk Photo: Tarek Siala ♂tassel Photo: Henry Mühlpfordt Pollen Pistil M m F- ✓ ✗ ff ✓ ✓ F/f M/m tcb1
- 30. Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize orig TF1 allopatric maize ff;mm allopatric mexicana ff;M- M m F- ✓ ✗ ff ✓ ✓
- 31. Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize orig TF1 allopatric maize ff;mm allopatric mexicana ff;M- M m F- ✓ ✗ ff ✓ ✓
- 32. Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize orig TF1 allopatric maize ff;mm allopatric mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize ff;MM sympatry ff;mm M m F- ✓ ✗ ff ✓ ✓
- 33. Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize orig TF1 allopatric maize ff;mm allopatric mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize ff;MM sympatry FM haplotype arises & increases in frequency in sympatry due to reinforcement ff;mm FF;MM M m F- ✓ ✗ ff ✓ ✓
- 34. Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize orig TF1 allopatric maize ff;mm allopatric mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 mexicana ff;M- Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 maize origins Tripsacum extinct maizeF1F1 maize ff;MM sympatry fM increases in sympatric maize due to extra pollination afforded by M FF;MM M m F- ✓ ✗ ff ✓ ✓
- 35. A a Genotype Fitness A A 1 A a 1 – 0.5s a a 1 – s Genotype Fitness A A 1 – s A a 1 – 0.5 s a a 1 F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1 Alison Wardlaw mexicana (A) maize (a) Yaniv Brandvain r F M m A
- 36. 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 Genotype Frequency Generation Meyerowitz 1994 Current Biology maize origins Tripsacum extinct maizeF1F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1F1 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 mexicana (A) maize (a) m = 0.1 s = 1 r = 0.01 fMA FMA FmA fmA FMa fMa Fma fma
- 37. 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 Genotype Frequency Generation Meyerowitz 1994 Current Biology maize origins Tripsacum extinct maizeF1F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1F1 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 FML fML FmL fmL FMl fMl Fml fml M at high frequency in mexicana F at low frequency f,m at high frequency in maize fMA FMA fma fMa mexicana (A) maize (a) m = 0.1 s = 1 r = 0.01 fMA FMA FmA fmA FMa fMa Fma fma
- 38. 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 Genotype Frequency Generation Meyerowitz 1994 Current Biology maize origins Tripsacum extinct maizeF1F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1F1 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 FML fML FmL fmL FMl fMl Fml fml fMA FMA fma fMa mexicana (A) maize (a) m = 0.1 s = 1 r = 0.01 fMA FMA FmA fmA FMa fMa Fma fma F increases in mexicana due to selection against maize pollen
- 39. 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 Genotype Frequency Generation Meyerowitz 1994 Current Biology maize origins Tripsacum extinct maizeF1F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1F1 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 FML fML FmL fmL FMl fMl Fml fml fMA FMA fma fMa mexicana (A) maize (a) m = 0.1 s = 1 r = 0.01 fMA FMA FmA fmA FMa fMa Fma fma F increases in mexicana due to selection against maize pollen M increases in maize due to sexual selection for increased pollination
- 40. 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 Genotype Frequency Generation Meyerowitz 1994 Current Biology maize origins Tripsacum extinct maizeF1F1 Meyerowitz 1994 Current Biology Duvick et al. 1999 US 6639132 B1 Tripsacum extinct maizeF1F1 0 200 400 600 800 1000 0.0 0.2 0.4 0.6 0.8 1.0 FML fML FmL fmL FMl fMl Fml fml fMA FMA fma fMa mexicana (A) maize (a) m = 0.1 s = 1 r = 0.01 fMA FMA FmA fmA FMa fMa Fma fma M in maize overcomes rep. isolation; allele frequencies equilibrate
- 41. Reinforcement Generation 0 200 400 600 800 1000 0.2 0.4 0.6 0.8 1.0
- 42. Lu et al. 2014 Plant Repro. of the tested tubes had clustered callose plugs (Fig. 6). Incompatible pollen tube growth in Ga2-s was distinct from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the Ga2-s barrier caused clustered callose plugs (18 % of Ga2-s 8 HAP (55) 9) (60) nts after Ga1-s Ga2-stcb1 Phenotype )94(27)05(69)05(001 98 (50) Tcb1-s * Silks Pollen tcb1 ga1 ga2 d n r e e of the silk length in Ga1-s and 8 % of the silk length in Ga2-s (Fig. 3b). All three barriers are pre-zygotic and caused by arrest of pollen tube growth. However, these crossing barriers have different strengths in blocking incompatible pollen. 0 20 40 60 80 100 tcb1 Tcb1-s Ga1-s Ga2-s tcb1pollentubelength (%ofthesilk) (b) Silk genotype (40) (50) (62) (55) Ga1-F Ga2-F FF ff m
- 43. Allopatry Sympatry Locus mex maize mex maize tcb1 fM fm FM fm ga1 fM fm FM fM ga2 fM fm FM fM Lu et al. 2014 Plant Repro. of the tested tubes had clustered callose plugs (Fig. 6). Incompatible pollen tube growth in Ga2-s was distinct from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the Ga2-s barrier caused clustered callose plugs (18 % of Ga2-s 8 HAP (55) 9) (60) nts after Ga1-s Ga2-stcb1 Phenotype )94(27)05(69)05(001 98 (50) Tcb1-s * Silks Pollen tcb1 ga1 ga2 d n r e e of the silk length in Ga1-s and 8 % of the silk length in Ga2-s (Fig. 3b). All three barriers are pre-zygotic and caused by arrest of pollen tube growth. However, these crossing barriers have different strengths in blocking incompatible pollen. 0 20 40 60 80 100 tcb1 Tcb1-s Ga1-s Ga2-s tcb1pollentubelength (%ofthesilk) (b) Silk genotype (40) (50) (62) (55) Ga1-F Ga2-F FF ff m
- 44. Allopatry Sympatry Locus mex maize mex maize tcb1 fM fm FM fm ga1 fM fm FM fM ga2 fM fm FM fM Lu et al. 2014 Plant Repro. of the tested tubes had clustered callose plugs (Fig. 6). Incompatible pollen tube growth in Ga2-s was distinct from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the Ga2-s barrier caused clustered callose plugs (18 % of Ga2-s 8 HAP (55) 9) (60) nts after Ga1-s Ga2-stcb1 Phenotype )94(27)05(69)05(001 98 (50) Tcb1-s * Silks Pollen tcb1 ga1 ga2 d n r e e of the silk length in Ga1-s and 8 % of the silk length in Ga2-s (Fig. 3b). All three barriers are pre-zygotic and caused by arrest of pollen tube growth. However, these crossing barriers have different strengths in blocking incompatible pollen. 0 20 40 60 80 100 tcb1 Tcb1-s Ga1-s Ga2-s tcb1pollentubelength (%ofthesilk) (b) Silk genotype (40) (50) (62) (55) Ga1-F Ga2-F FF ff m
- 45. Allopatry Sympatry Locus mex maize mex maize tcb1 fM fm FM fm ga1 fM fm FM fM ga2 fM fm FM fM Lu et al. 2014 Plant Repro. of the tested tubes had clustered callose plugs (Fig. 6). Incompatible pollen tube growth in Ga2-s was distinct from both Tcb1-s and Ga1-s. Like Tcb1-s and Ga1-s, the Ga2-s barrier caused clustered callose plugs (18 % of Ga2-s 8 HAP (55) 9) (60) nts after Ga1-s Ga2-stcb1 Phenotype )94(27)05(69)05(001 98 (50) Tcb1-s * Silks Pollen tcb1 ga1 ga2 d n r e e of the silk length in Ga1-s and 8 % of the silk length in Ga2-s (Fig. 3b). All three barriers are pre-zygotic and caused by arrest of pollen tube growth. However, these crossing barriers have different strengths in blocking incompatible pollen. 0 20 40 60 80 100 tcb1 Tcb1-s Ga1-s Ga2-s tcb1pollentubelength (%ofthesilk) (b) Silk genotype (40) (50) (62) (55) Ga1-F Ga2-F FF ff m
- 50. maize mexicana B73:g/g sample:?/? x 19 F1 g/? GBS, identify both alleles ♀ ♂ ♂ x B73:s/s ♀ ? x ? ♂ x B73:g/g ♀ ? x ? A B unknown sample tester: ff;mm 19 F1 genotype to find both alleles maize mexicana B73:g/g sample:?/? x 19 F1 g/? GBS, identify both alleles ♀ ♂ ♂ x B73:s/s ♀ ? x ? ♂ x B73:g/g ♀ ? x ? A B tester: ff;mmtester: FF;MM • how different are dynamics of funcXonal haplotypes among populaXons? • inbreeding depression, local selecXon, migraXon differences • how does evoluXon of reinforcement change with 3 interrelated loci? • pollen compeXXon, epistasis, mutaXon change stability? • how do alleles at these loci evolve? • M in maize should originate from local mexicana • M in allopatric mexicana arises de novo? • M,F should show selecXon in maize, mexicana
- 54. • gene flow plays key role in maize landraces and teosinte • adapXve introgression associated with maize colonizaXon of highlands • likely selecXon against hybrids and for reinforcement in teosinte
- 55. • gene flow plays key role in maize landraces and teosinte • adapXve introgression associated with maize colonizaXon of highlands • likely selecXon against hybrids and for reinforcement in teosinte • sexual selecXon seems to prevent stable reinforcement
- 56. • gene flow plays key role in maize landraces and teosinte • adapXve introgression associated with maize colonizaXon of highlands • likely selecXon against hybrids and for reinforcement in teosinte • sexual selecXon seems to prevent stable reinforcement • great system to study dynamics of post-maXng prezygoXc isolaXon • geneXc tools (mulXple references, mapping populaXons) • natural populaXons • experimental inbreds with all combinaXons of alleles at all loci
- 57. Acknowledgments HiLo Group Graham Coop Sherry Flint-Garcia Matt Hufford Ruben Rellan Dan Runcie Ruairidh Sawers Lab Alumni Matt Hufford (Iowa State) Tanja Pyhäjärvi (Oulu) Joost van Heerwaarden (Wageningen) PanZea Ed Buckler John Doebley Mike McMullen UMN Yaniv Brandvain Alison Wardlaw UCR Norm Ellstrand Pesach Lubinsky Carnegie Institution Matt Evans
- 60. K = 2 K = 7 K = 6 K = 5 K = 4 K = 3 K = 8 K = 9 K = 10 mexicana maize references
- 64. Photos: Matt Hufford, Brandon Gaut, Anna O’Brien