Consequences of introgression and gene flow on the genetic structure and diversity of Lima bean (Phaseolus lunatus L.) in its Mesoamerican diversity area

Abstract

We evaluated the role of gene flow and wild-crop introgression on the structure and genetic diversity of Lima bean (Phaseolus lunatus) in the Yucatan Peninsula, an important Mesoamerican diversity area for this crop, using a genotyping-by-sequencing approach (15,168 SNP markers) and two scales. At the local scale, STRUCTURE and NGSEP analyses showed predominantly crop-to-wild introgression, but also evidence of a bidirectional gene flow in the two wild-weedy-crop complexes studied (Itzinté and Dzitnup). The ABBA-BABA tests showed a higher introgression in Itzinté (the older complex) than in Dzitnup (the younger one); at the allelic level, the wild-crop introgression in Itzinté was similar in both directions, in Dzitnup it was higher from crop-to-wild; and at the chromosomal level, introgression in Itzinté was from wild-to-crop, whereas in Dzitnup it occured in the opposite direction. Also, we found H _E values slightly higher in the domesticated accessions than in the wild ones, in both complexes (Itzinté: wild = 0.31, domesticated = 0.34; Dzinup: wild = 0.27, domesticated = 0.36), but %P and π estimators were higher in the wild accessions than in the domesticated ones. At a regional scale, STRUCTURE and MIGRATE showed a low gene flow, predominantly from crop-to-wild; and STRUCTURE, Neighbor-Joining and PCoA analyses indicated the existence of two wild groups and one domesticated group, with a marked genetic structure based in the existence of domesticated MI and wild MII gene pools. Also, at the regional scale, we found a higher genetic diversity in the wild accessions than in the domesticated ones, in all estimators used (e.g., H _E = 0.27 and H _E = 0.17, respectively). Our results indicate that gene flow and introgression are playing an important role at the local scale, but its consequences on the structure and genetic diversity of the Lima bean are not clearly reflected at the regional scale, where diversity patterns between wild and domesticated populations could be reflecting historical events.

Keywords: Mayan milpa; SNPs markers; Wild-crop introgression; Wild-weedy-crop complexes; Yucatan Peninsula.

Figure 1. Geographic distribution of wild and domesticated Lima bean accessions collected in the Yucatan Peninsula, Mexico.

Domesticated accessions are shown in black circles and wild accessions in black triangles, the white boxes show the collection sites of the two studied wild-weedy-crop complexes: Dzitnup and Itzinté. Source Credit: Landsat/Copernicus INEGI Data SIO, NOAA, U.S. Navy, NGA, GEBCO.

Figure 2. Collected seeds into the two wild-weedy-crop complexes studied.

Photo taken by Pedro Ruiz-Gil.

Figure 3. Estimated ancestry coefficients for two wild-weedy-crop complexes of Lima bean studied in the Yucatan Peninsula, using STRUCTURE and 15,168 SNP markers.

(A) Itzinte; (B) Dzitnup; with optimal K = 2, green color represents the wild gene pool and red color represents the domesticated gene pool. (C) Ancestry index between domesticated (red) and wild (blue) accessions of Lima bean in Dzitnup and Itzinté complexes.

Figure 4. Distribution of introgression blocks per chromosome (PL01-PL11) detected by NGSEP.

Dzitnup (A) and (B), Itzinté (C) and (D). Domesticated chromosomes are in red, wild chromosomes are in blue. Accessions shown in figure (A) 1. CD11_218, 2. CD11_221, 3. CD12B_234, 4. CD3_150, 5. CD8_197; in (B) 1. CD1_133, 2. CD12A_226, 3. CD15_252, 4. CD2B_350, 5. CD4B_358; in (C) 1. CI3B_26, 2. CI6_375, 3. CI7_49, 4. CI8_58; in (D) 1. CI12_324, 2. CI12_326, 3. CI13A_16, 4. CI13A_20.

Figure 5. Distribution of introgression blocks along chromosomes.

The figure shows the distribution of introgression blocks along chromosomes between wild and domesticated populations within (A) the Itzinté complex and (B) the Dzitnup complex. Red, introgression blocks in the direction domesticated to wild. Yellow, introgression blocks in the direction wild to domesticated. PL01-PL11, chromosomes.

Figure 6. Neighbor-Joining analysis of Lima bean accessions from the Yucatan Peninsula, including a control group, using 15,168 SNP markers.

Figure 7. Estimated ancestry coefficients for wild and domesticated Lima bean accessions from the Yucatan Peninsula, using STRUCTURE and 15,168 SNP markers.

With optimal K = 3, green represents the Pure wild group, blue represents Admixed wild group and red represents the domesticated group.