Beyond balancing selection: frequent mitochondrial recombination contributes to high‐female frequencies in gynodioecious Lobelia siphilitica (Campanulaceae)

Abstract

Gynodioecy is a sexual system in which females and hermaphrodites co-occur. In most gynodioecious angiosperms, sex is determined by an interaction between mitochondrial malesterility genes (CMS) that arise via recombination and nuclear restorer alleles that evolve to suppress them. In theory, gynodioecy occurs when multiple CMS types are maintained at equilibrium frequencies by balancing selection. However, some gynodioecious populations contain very high frequencies of females. High female frequencies are not expected under balancing selection, but could be explained by the repeated introduction of novel CMS types.To test for balancing selection and/or the repeated introduction of novel CMS, we characterised cytoplasmic haplotypes from 61 populations of Lobelia siphilitica that vary widely in female frequency.We confirmed that mitotype diversity and female frequency were positively correlated across populations, consistent with balancing selection. However, while low-female populations hosted mostly common mitotypes, high-female populations and female plants hosted mostly rare, recombinant mitotypes likely to carry novel CMS types.Our results suggest that balancing selection maintains established CMS types across this species, but extreme female frequencies result from frequent invasion by novel CMS types. We conclude that balancing selection alone cannot account for extreme population sex-ratio variation within a gynodioecious species.

The ecology, evolution, and genetics of plant reproductive systems

“…1372–1380) use transcriptome sequencing and comparative population genomic analyses to show how the loss of sexual reproduction and hybridization within the genus Oenothera shapes patterns of genomic diversity and gives rise to new species. Another study in this issue (Adhikari et al ., , in this issue pp. 1381–1393) uses cytotype markers to examine mechanisms for the evolution of gynodioecy, and finds evidence implicating both negative‐frequency dependent selection and invasion of novel male sterility genes in maintaining variation in mating systems within and between populations.…”

Do Genetic Drift and Gene Flow Affect the Geographic Distribution of Female Plants in Gynodioecious Lobelia siphilitica?

“…This is because random mating is likely to result in mismatched CMS and Rf alleles in offspring, especially when there are many unique alleles at CMS and/or Rf loci [ 3 ]. Polymorphism at CMS and Rf loci appears to be primarily maintained long-term by balancing selection (specifically, negative frequency-dependent selection) [ 14 , 15 , 16 ] under a broad range of demographic conditions. However, modeling [ 16 ] and recent empirical work [ 14 ] show that balancing selection alone cannot readily account for extremely high female frequencies.…”

“…Non-selective forces, including genetic drift and gene flow, could contribute to extreme sex-ratio variation in gynodioecious species through effects on CMS– Rf polymorphism [ 3 , 17 ]. The frequent origin of novel CMS genes via mitochondrial mutation is expected to result in locally high female frequencies [ 14 ]. However, this depends on novel CMS types becoming established and spreading readily within populations [ 18 ].…”

“…Our previous research documented several aspects of L. siphilitica sex-ratio variation that make it an excellent study system. Two previous censuses of L. siphilitica populations documented sex ratios ranging from 0 to 100% female, with higher female frequencies at lower latitudes [ 14 , 31 ]. However, Caruso and Case [ 31 ] included few populations in the southern half of the species range, making it insufficient to fully document spatial structuring of female frequencies, particularly central–peripheral patterning.…”

“…However, Caruso and Case [ 31 ] included few populations in the southern half of the species range, making it insufficient to fully document spatial structuring of female frequencies, particularly central–peripheral patterning. Adhikari et al [ 14 ] examined the effects of balancing selection on population sex ratio in L. siphilitica and found that this process can explain sex ratios up to but not above ~50% female. Populations with extremely high female frequencies contained rare mitochondrial haplotypes, suggesting elevated rates of CMS origin and turnover and the absence of balancing selection.…”