Hybridization and genome size evolution: timing and magnitude of nuclear DNA content increases in Helianthus homoploid hybrid species

Abstract

Hybridization and polyploidy can induce rapid genomic changes, including the gain or loss of DNA, but the magnitude and timing of such changes are not well understood. The homoploid hybrid system in Helianthus (three hybrid-derived species and their two parents) provides an opportunity to examine the link between hybridization and genome size changes in a replicated fashion. Flow cytometry was used to estimate the nuclear DNA content in multiple populations of three homoploid hybrid Helianthus species (Helianthus anomalus, Helianthus deserticola, and Helianthus paradoxus), the parental species (Helianthus annuus and Helianthus petiolaris), synthetic hybrids, and natural hybrid-zone populations. Results confirm that hybrid-derived species have 50% more nuclear DNA than the parental species. Despite multiple origins, hybrid species were largely consistent in their DNA content across populations, although H. deserticola showed significant interpopulation differences. First- and sixth-generation synthetic hybrids and hybrid-zone plants did not show an increase from parental DNA content. First-generation hybrids differed in DNA content according to the maternal parent. In summary, hybridization by itself does not lead to increased nuclear DNA content in Helianthus, and the evolutionary forces responsible for the repeated increases in DNA content seen in the hybrid-derived species remain mysterious.

Fig. 1

Nuclear DNA content of sunflower (Helianthus) parental species and hybrid descendants. Mean 2C-value and standard deviation are shown. Differences in 2C-value significant at P < 0.0005 in a mixed model ANOVA, treating population as a random nested factor within species, are indicated by different letters. Solid bars, parental species; open bars, hybrid-derived species.

Fig. 2

Nuclear DNA content of sunflower (Helianthus) synthetic hybrid lineages, hybrid-zone plants, and (for comparison) one of the ancient homoploid hybrid species, Helianthus paradoxus. Mean 2C-value and standard deviation are shown. Synthetic lineages differed in nuclear DNA content depending on their maternal parent (P = 0.008) in a mixed model ANOVA treating each cross as a random nested factor within the maternal parent, as indicated by the different letters. Solid bars, natural hybrid-zone plants; gray-shaded bars, synthetic hybrids; open bars, hybrid-derived species.

Fig. 3

Nuclear DNA content of populations of Helianthus deserticola. Mean 2C-value and standard deviation are shown. Populations differing in mean DNA content in a one-way ANOVA (P = 0.0001) are indicated by different letters. The two populations occurring near Glen Canyon are underlined.