Genetics of hybrid incompatibility between Lycopersicon esculentum and L. hirsutum

Abstract

We examined the genetics of hybrid incompatibility between two closely related diploid hermaphroditic plant species. Using a set of near-isogenic lines (NILs) representing 85% of the genome of the wild species Lycopersicon hirsutum (Solanum habrochaites) in the genetic background of the cultivated tomato L. esculentum (S. lycopersicum), we found that hybrid pollen and seed infertility are each based on 5-11 QTL that individually reduce hybrid fitness by 36-90%. Seed infertility QTL act additively or recessively, consistent with findings in other systems where incompatibility loci have largely been recessive. Genetic lengths of introgressed chromosomal segments explain little of the variation for hybrid incompatibility among NILs, arguing against an infinitesimal model of hybrid incompatibility and reinforcing our inference of a limited number of discrete incompatibility factors between these species. In addition, male (pollen) and other (seed) incompatibility factors are roughly comparable in number. The latter two findings contrast strongly with data from Drosophila where hybrid incompatibility can be highly polygenic and complex, and male sterility evolves substantially faster than female sterility or hybrid inviability. The observed differences between Lycopersicon and Drosophila might be due to differences in sex determination system, reproductive and mating biology, and/or the prevalence of sexual interactions such as sexual selection.

Figure 1.—

Distributions of NIL mean phenotypes for pollen and seed traits for 71 NILs. For each trait, the mean phenotypic value of each parental accession (LE; LH, if applicable) and the grand mean phenotypic value of all 71 NILs are indicated with arrows. (a) Total pollen grains per flower (PN); note that LH (an outcrosser) produces substantially more pollen per flower than LE (a selfer). (b) Proportion of fertile pollen grains per flower (PF). (c) Selfed seed set per fruit (SSS). (d) LE-cross seed set per fruit (SSC).

Figure 2.—

QTL for pollen and seed fertility traits, with their location on the L. esculentum × L. hirsutum linkage map. Hatched chromosomal regions on the linkage map indicate areas of the genome fixed for LE alleles (i.e., genomic regions not represented in the NIL population). The self-incompatibility (S) locus and self-pruning (sp) locus are indicated to the left of the chromosomes. The shaded bars to the right of the chromosomes show the individual analyses for the following traits: PN, total pollen count per flower; PF, proportion of fertile pollen per flower; SSS, self (homozygous) seed set; and SSC, LE-cross (heterozygous) seed set. Levels of percentage difference (Δ%) from the LE control parent for 20 > Δ < 50 and Δ > 50 are indicated by the intensity of shading (see key on figure). Putative QTL are indicated by symbols to the right of each chromosome, marked at the center of the chromosomal region showing a significant effect for the trait. Self-seed set traits in brackets are those that are nonsignificant once the effect of pollen fertility is removed statistically (see text).

Figure 2.—

QTL for pollen and seed fertility traits, with their location on the L. esculentum × L. hirsutum linkage map. Hatched chromosomal regions on the linkage map indicate areas of the genome fixed for LE alleles (i.e., genomic regions not represented in the NIL population). The self-incompatibility (S) locus and self-pruning (sp) locus are indicated to the left of the chromosomes. The shaded bars to the right of the chromosomes show the individual analyses for the following traits: PN, total pollen count per flower; PF, proportion of fertile pollen per flower; SSS, self (homozygous) seed set; and SSC, LE-cross (heterozygous) seed set. Levels of percentage difference (Δ%) from the LE control parent for 20 > Δ < 50 and Δ > 50 are indicated by the intensity of shading (see key on figure). Putative QTL are indicated by symbols to the right of each chromosome, marked at the center of the chromosomal region showing a significant effect for the trait. Self-seed set traits in brackets are those that are nonsignificant once the effect of pollen fertility is removed statistically (see text).

Figure 3.—

Relationships between the size of LH introgression (in centimorgans) and mean NIL (a) pollen or (b) seed fertility. (a) Pollen fertility measures shown are total pollen count per flower (PN; in open circles with thin line) and (for convenience of representation) number of viable pollen per flower (PV; in solid circles with thick line). (b) Seed fertility measures are LE-cross seed set per fruit (SSC; in open squares with thin line) and self-seed set per fruit (SSS; in solid squares with thick line). Double asterisks indicate significant negative regression at P < 0.001; NS, not significant. Note that regression results for proportion of fertile pollen (PF; arcsine square-root transformed) were equivalent to PV results.