Transmission ratio distortion in intraspecific hybrids of Mimulus guttatus: implications for genomic divergence

Abstract

We constructed a genetic linkage map between two divergent populations of Mimulus guttatus. We genotyped an F(2) mapping population (N = 539) at 154 AFLP, microsatellite, and gene-based markers. A framework map was constructed consisting of 112 marker loci on 14 linkage groups with a total map length of 1518 cM Kosambi. Nearly half of all markers (48%) exhibited significant transmission ratio distortion (alpha = 0.05). By using a Bayesian multipoint mapping method and visual inspection of significantly distorted markers, we detected 12 transmission ratio distorting loci (TRDL) throughout the genome. The high degree of segregation distortion detected in this intraspecific map indicates substantial genomic divergence that perhaps suggests genomic incompatibilities between these two populations. We compare the pattern of transmission ratio distortion in this map to an interspecific map constructed between M. guttatus and M. nasutus. A similar level of segregation distortion is detected in both maps. Collinear regions between maps are compared to determine if there are shared genetic patterns of non-Mendelian segregation distortion within and among Mimulus species.

Figure 1.—

Framework linkage map of M. guttatus (IM) × M. guttatus (DUN) F₂ hybrid population. The names of all codominant markers are underlined. All markers and linkage groups that are shared with the interspecific M. guttatus (IM) × M. nasutus map are marked with an asterisk (*).

Figure 2.—

Transmission ratio distortion across the M. guttatus (IM) × M. guttatus (DUN) framework map. The dot and the plus symbol represent the two homozygous parental genotypes (DUN/DUN and IM/IM, respectively) at marker loci on each of the 14 linkage groups. The vertical position of each symbol shows the magnitude and direction of the deviation of genotype frequencies from the Mendelian expectation (0.25). The biases were graphed directly. DUN homozygote deviations (DUN/DUN) were graphed as positive values [deviation = f(DUN/DUN) − 0.25], and IM homozygotes (IM/IM) were graphed as negative values [deviation = −(f(IM/IM) − 0.25)]. The shaded peaks show the frequency distributions of the location of TRDL as estimated by the Bayesian mapping method of Vogl and Xu (2000). The average frequency of detecting a TRDL is indicated next to each peak. Each frequency distribution is scaled to the maximum frequency per group for visualization purposes.

Figure 3.—

Comparative map of TRDL between and within species of M. guttatus. The linkage group is indicated above both intraspecific [g × g (M. guttatus × M. guttatus)] and interspecific [g × n (M. guttatus × M. nasutus)] maps. Hatch marks indicate marker placement. Only terminal markers and communal markers are labeled on each map, with dashed lines connecting communal markers. Linkage groups with a single communal markers are matched up arbitrarily; note the orientation could be rotated. Due to placement of additional codominant markers to the previously published interspecific map (Fishman et al. 2001), several AFLP markers were ousted to maintain basic mapping criteria. The following changes were made to the g × n map: LG2, addition of MgSTS56, slight separation of BA172 and CB280; LG6, addition of MgSTS25; LG9, addition of MgSTS35 and removal of BC108, slight separation of CA261 and CB115; LG10, addition of MgSTS43 and removal of AA153c and AA100; LG11, addition of MgSTS19 and MgSTS87, removal of BA387, change in map order for CYCA, AAT356, BD100, BB124, BA196, slight separation of BB124 and BA196; and LG14, addition of MgSTS18. Arrows point to locations of TRDL or detected regions of distortion. Solid arrows represent markers distorted toward excess IM (M. guttatus) alleles, open arrows represent markers distorted toward either excess DUN or M. nasutus alleles, stippled arrow represents distortion with an excess of heterozygotes, and shaded arrow represents distortion with a deficiency of heterozygotes.