Pollinator-driven divergence among populations of a self-fertilizing lily, Hesperantha coccinea (Iridaceae).

Abstract

Two major trends in floral evolution – pollinator shifts and the evolution of autonomous selffertilisation – are generally considered alternative evolutionary responses to pollen-limitation of plant reproductive success. However, pollinator-specialised species often are also autofertile. The apparent contradiction of “opposing contrivances” for attracting pollinators and reproducing independently of them, may represent an optimal Best-of-Both-Worlds strategy whereby delayed self-fertilisation provides reproductive assurance in unpredictable pollination environments. In this thesis, I demonstrate pollinator-driven divergence among autofertile populations of Hesperantha coccinea (Iridaceae) based on evidence of local adaptation to different pollinators and experimental quantification of the contributions of pollinators and autonomous self-fertilisation to reproductive success. Floral colour, morphology, orientation and nectar characteristics differ between populations pollinated by a butterfly or a longproboscid fly. Reciprocal translocation of plants, assessment of pollinator effectiveness and preference experiments demonstrate that this intraspecific divergence involved adaptation to the morphology and preferences of the locally-dominant pollinators at low and high elevations, creating a geographic mosaic of floral variation. Despite this divergence, reproduction by both ecotypes involves a combination of pollinator-mediated outcrossing and autonomous self-fertilisation. Hand-pollinations showed self-compatibility and high autofertility in both ecotypes. Nevertheless, analysis of SSR markers revealed mixed selfing and outcrossing in populations of both colour forms. Most autonomous self-pollination occurred late during a flower’s lifespan, as expected for Best-of- Both-Worlds reproduction. Furthermore, similar performance of selfed and outcrossed progeny from three populations in a greenhouse indicated little genetic cost of selfing. Emasculation experiments showed extensive variation in the relative contributions of autonomous self-pollination and pollinators to fecundity among populations and flowering seasons. Overall, pollinator activity and autonomous self-fertilisation accounted for 75% and 25% of fecundity, respectively. The contribution of autonomous self-fertilisation varied among populations from zero to more than 90% of seed set and differed within populations between years by an average of 30%. The relative importance of pollinators and autonomous self-fertilisation did not vary geographically in relation to proximity to range edge, flower number, size, or herkogamy. This independence identifies autonomous self-fertilisation as part of a stable Best-of-Both-Worlds strategy employed by H. coccinea to contend with unpredictable pollination. Weak inbreeding depression in combination with conditions otherwise consistent with Best-of-Both-Worlds reproduction suggests that the importance of siring advantages of pollinator-mediated pollen transfer have been underestimated in these systems.