A genetic linkage map of the mimetic butterfly Heliconius melpomene - PubMed (original) (raw)

Comparative Study

A genetic linkage map of the mimetic butterfly Heliconius melpomene

Chris D Jiggins et al. Genetics. 2005 Oct.

Abstract

Heliconius melpomene is a mimetic butterfly that exhibits great geographic variation in color pattern. We present here a genetic linkage map based on analysis of genetic markers in 73 individuals from a single F(2) family, offspring of a cross between H. m. cythera from western Ecuador and H. m. melpomene from French Guiana. A novel "three-step method" is described for the analysis of dominant markers in an F(2) cross, using outbred parental strains and taking advantage of the lack of crossing over in female Lepidoptera. This method is likely to prove useful for future mapping studies in outbred species with crossing over restricted to one sex, such as the Lepidoptera and Drosophila. The resulting linkage map has 21 linkage groups corresponding to the 21 chromosomes of H. melpomene and includes 219 AFLP markers, 23 microsatellites, 19 single-copy nuclear genes, and the color pattern switch genes Yb and Sb. The marker density is high, averaging >1/7 cM. The total map length is 1616 cM and the average chromosome length is 77 cM. The genome size of H. melpomene was estimated to be 292 Mb, giving a relationship of physical-to-map distance of 180 kb/cM. This map forms the basis for future comparative linkage analysis of color pattern evolution in Heliconius.

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Figures

Figure 1.

Figure 1.

Segregation of markers in an F2 mapping family. (a) The segregation of two markers demonstrating assignment of an F2 locus to a linkage group by the forbidden recombinant method. Two loci are shown: A, inherited as a female-informative locus and corresponding to the chromosome print for this linkage group, and B, a locus that shows a fixed difference between the two parental strains and is inherited as an F2 marker in a 3:1 ratio of band present:band absent in the mapping family. The AFLP banding pattern for the two markers alongside each diploid genotype is shown. Occurrence of forbidden recombinant genotypes, in which both bands are absent, would indicate that the two markers are not syntenic. These genotypes would be expected to occur in one-eighth of the F2 family for unlinked markers. The offspring shown in the box are those that are rescored as missing data for analysis of the recombination map. (b) In more detail, the problem of linkage analysis between dominant markers inherited in repulsion, demonstrated here by loci B and D. Locus C is a male-informative marker that can be used to link B and D into a single map. The first group of progeny, a–f, are informative with respect to linkage of B and C, with c and d being the recombinant genotypes. The second group, g–l, are informative with respect to linkage of C and D. Note that because of dominance, a–f are uninformative with respect to locus D, and g–l are uninformative with respect to locus B.

Figure 1.

Figure 1.

Segregation of markers in an F2 mapping family. (a) The segregation of two markers demonstrating assignment of an F2 locus to a linkage group by the forbidden recombinant method. Two loci are shown: A, inherited as a female-informative locus and corresponding to the chromosome print for this linkage group, and B, a locus that shows a fixed difference between the two parental strains and is inherited as an F2 marker in a 3:1 ratio of band present:band absent in the mapping family. The AFLP banding pattern for the two markers alongside each diploid genotype is shown. Occurrence of forbidden recombinant genotypes, in which both bands are absent, would indicate that the two markers are not syntenic. These genotypes would be expected to occur in one-eighth of the F2 family for unlinked markers. The offspring shown in the box are those that are rescored as missing data for analysis of the recombination map. (b) In more detail, the problem of linkage analysis between dominant markers inherited in repulsion, demonstrated here by loci B and D. Locus C is a male-informative marker that can be used to link B and D into a single map. The first group of progeny, a–f, are informative with respect to linkage of B and C, with c and d being the recombinant genotypes. The second group, g–l, are informative with respect to linkage of C and D. Note that because of dominance, a–f are uninformative with respect to locus D, and g–l are uninformative with respect to locus B.

Figure 2.

Figure 2.

Parental and hybrid phenotypes. (A) H. melpomene cythera (ventral), (B) H. melpomene melpomene (dorsal), and the four major hybrid phenotypic classes. The parental genotypes are ybc ybc sbsb AcAc KK for H. m. cythera and YbYb SbSb acac kk for H. m. melpomene. Note that the phenotypes generated by the loci K and Ac are not expressed in either parental strain.

Figure 3.

Figure 3.

Linkage map of H. melpomene. Microsatellite and SCNP markers are shown in larger type, using standard gene nomenclature for the latter. All remaining markers are AFLPs and are coded with the two selective _Eco_RI nucleotides, followed by the three selective _Mse_I nucleotides, and finally an identifier code; e.g., CT_CAGa38 is band a38 scored from the _Eco_RI-CT _Mse_I-CAG primer combination. Markers assigned to linkage groups for which there is no information on map position are shown separately below the linkage group. Possible homology with linkage groups in H. erato is shown in parentheses below each linkage group number with the H. erato linkage group number; e.g., linkage group 2 (LG2) corresponds to linkage group 13 in H. erato (EG13; see T

obler

et al. 2004) on the basis of the shared Hel.05 marker. These comparisons are based on a single marker in each case so chromosomal homology is tentative. The marker used to establish homology is underlined in each case.

Figure 3.

Figure 3.

Linkage map of H. melpomene. Microsatellite and SCNP markers are shown in larger type, using standard gene nomenclature for the latter. All remaining markers are AFLPs and are coded with the two selective _Eco_RI nucleotides, followed by the three selective _Mse_I nucleotides, and finally an identifier code; e.g., CT_CAGa38 is band a38 scored from the _Eco_RI-CT _Mse_I-CAG primer combination. Markers assigned to linkage groups for which there is no information on map position are shown separately below the linkage group. Possible homology with linkage groups in H. erato is shown in parentheses below each linkage group number with the H. erato linkage group number; e.g., linkage group 2 (LG2) corresponds to linkage group 13 in H. erato (EG13; see T

obler

et al. 2004) on the basis of the shared Hel.05 marker. These comparisons are based on a single marker in each case so chromosomal homology is tentative. The marker used to establish homology is underlined in each case.

Figure 3.

Figure 3.

Linkage map of H. melpomene. Microsatellite and SCNP markers are shown in larger type, using standard gene nomenclature for the latter. All remaining markers are AFLPs and are coded with the two selective _Eco_RI nucleotides, followed by the three selective _Mse_I nucleotides, and finally an identifier code; e.g., CT_CAGa38 is band a38 scored from the _Eco_RI-CT _Mse_I-CAG primer combination. Markers assigned to linkage groups for which there is no information on map position are shown separately below the linkage group. Possible homology with linkage groups in H. erato is shown in parentheses below each linkage group number with the H. erato linkage group number; e.g., linkage group 2 (LG2) corresponds to linkage group 13 in H. erato (EG13; see T

obler

et al. 2004) on the basis of the shared Hel.05 marker. These comparisons are based on a single marker in each case so chromosomal homology is tentative. The marker used to establish homology is underlined in each case.

Figure 4.

Figure 4.

Placement of the color pattern locus Yb on linkage group 15. The log likelihood is shown for placement of the color pattern locus in each mapping interval along the linkage group, relative to the most likely location that is set at zero and is indicated by a star. Values <−2 indicate a significantly worse fit to the data at ∼95%, so placement of the locus in all intervals except for 2 can be ruled out. The Yb locus therefore must be located in the 22-cM interval between the markers CT_GTAa22 and CT_GAAa37.

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References

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