Viral pathogens and the advantage of sex in the perennial grass Anthoxanthum odoratum

Abstract The ubiquity of sexual reproduction among plants and animals remains one of the major unresolved paradoxes of modern evolutionary biology. In order for sex to be maintained in populations, sex must confer immediate and substantial fitness benefits. Theoreticians have proposed numerous mechanisms to explain how such advantages arise, but experimental data are few. In one well-studied population of the perennial grass Anthoxanthum odoratum in a mown North Carolina field, sexual offspring have been found to have significantly higher fitness than asexual offspring. More recent field experiments show that an aphid-transmitted virus, barley yellow dwarf (BYDV)-strain SGV, specifically transmitted by Schizaphus graminum, frequently infects Anthoxanthum progeny soon after transplantation into the field, BYDV infection is asymptomatic in Anthoxanthum, but BYDV-inoculated clones planted directly in the field had significantly lower fitness than healthy controls. Sexual females have been hypothesized to gain a fitness advantage for their offspring in the presence of pathogens either by providing ‘an escape in time’ from pathogens preadapted to the parental genotype or through the production of rare genotypes, which escape frequency-dependent infection. When parental clones and seed-derived sexual offspring were planted in identical but separate arrays in sites near where the parent was collected, parental clones were twice as frequently infected as sexual offspring. Factors other than genetic variation may have contributed to differences in levels of infection between sexual and asexual progeny: in this experiment, clonally derived asexual offspring tillers were slightly larger than seed-derived sexual tillers; in field experiments, larger plants were more frequently infected than smaller plants. When different families were planted into a common site, there was evidence that genotypes were less frequently infected when locally rare than when common. Taken together, the data suggest that BYDV infection generates advantages for rare or sexually produced genotypes in Anthoxanthum. The pattern of infection is likely to result from a complex interaction between vector, host, and viral genetics and population structure, vector behaviour, and host and vector dispersal patterns. Sexually produced genotypes appear to benefit because they are both novel and rare, but the observed minority advantage was weak. Other viral, bacterial, and fungal pathogens in this Anthoxanthum population may act as frequency-dependent selective forces in different places in the field, collectively generating the substantial and observed overall fitness advantage of rare genotypes. Further study is needed to elucidate their role. Nevertheless, the data do show that viral pathogens, which are often asymptomatic, play a significant evolutionary role in plant populations.