Host-driven phenotypic and phenological differentiation in sympatric races of a parasitic plant

Host specificity is a key factor influencing the ecology and evolutionary diversification of parasitic organisms. Host specialisation and geographic isolation are known to lead to the genetic differentiation of allopatric races in parasitic plants. However, how divergence can co-occur in sympatry remains largely unknown. We investigated phenological and phenotypic differentiation and potential reproductive isolation among three sympatric genetic races of Cytinus hypocistis (Cytinaceae) - an extreme endophytic holoparasite with a high degree of host specialisation. We compared spatio-temporal variations in flowering phenology, flower production, floral longevity, floral rewards, and morphology, and conducted inter-race pollinations among three races parasitising Cistus ladanifer, C. salviifolius, and Halimium halimifolium (Cistaceae) in six co-occurring populations. We found that host-defined genetic races differed significantly across multiple phenotypic and phenological aspects – a phenomenon previously overlooked due to the plants’ cryptic morphology. The race parasitising H. halimifolium showed earlier blooming, higher floral display, longer flowers, and higher pollen production and nectar concentration; the race on C. salviifolius showed later flowering, significantly lower floral display and smaller flowers with lower floral rewards; the race on C. ladanifer had intermediate characteristics. Genetic races were interfertile yet may remain differentiated by restricted gene flow and host-driven selection pressures. Together, our data point to a rare case of sympatric divergent evolution hiding in plain sight: apparently morphologically similar co-occurring parasite races can be genetically, phenotypically, and phenologically distinct. This hitherto unreported example of host-driven sympatric diversification challenges how species concepts are applied to cryptic parasitic plant races.