Amphicarphic species produce both aboveground and belowground seeds; the belowground seeds have been proposed to be an adaptation to disturbed sites because they are protected belowground, enabling them to persist and recolonize a site after disturbance. However, it is unknown whether such seeds indeed serve as the main colonizers after a disturbance. The amphicarpic species Polygala lewtonii is endemic to fire-prone Florida sandhill and scrub and is among only a few species with three flower types (aboveground chasmogamous flowers and both above and belowground cleistogamous flowers). The goal of this study was to understand whether recolonization of sites by P. lewtonii was accomplished primarily through germination of belowground seed. First, we quantified the outcrossing rate in seeds produced by aboveground chasmogamous flowers to determine whether we could detect differences in colonization of between seeds produced aboveground vs. belowground. Approximately 25% of seeds from aboveground chasmogamous flowers showed evidence of cross pollination and the seeds showed greater heterozygosity and lower inbreeding coefficients than pure selfing, indicating that it is possible to differentiate between selfed and non-selfed seed types in postfire colonization. Second, we analyzed genetic diversity, inbreeding, and genetic structure of the populations before and after a prescribed fire. If heterozygosity and admixture increased, and spatial population genetic structure and inbreeding decreased, this would indicate that fire promoted germination of outcrossed seed from aboveground flowers. However, inbreeding increased and spatial genetic structure and admixture decreased after fire, suggesting that selfed seed produced by belowground flowers predominantly recolonized the site after fire. Thus, amphicarpy is a powerful adaptation to fire-maintained environments by producing seeds that are well suited to the range of conditions presented by a highly variable, disturbance prone habitat.
Amphicarpic plants produce both aboveground and belowground seeds. Because belowground seeds are protected in the soil and may maintain viability when aboveground conditions are stressful, they were proposed as an adaptation to recolonize a site after disturbance. However, whether belowground seeds are the main colonizers after a disturbance remains unknown. Our goal was to understand whether recolonization by an amphicarpic species after fire was accomplished primarily through germination of seeds produced aboveground or belowground. We investigated Polygala lewtonii, an amphicarpic, perennial species endemic to fire-prone Florida sandhill and scrub, where fire kills plants but subsequently increases recruitment and population sizes. P. lewtonii produces three flower types: aboveground chasmogamous flowers and aboveground and belowground cleistogamous flowers, with previous research demonstrating chasmogamous flowers produce a much greater proportion of seeds than cleistogamous flowers. We quantified outcrossing in seeds produced by chasmogamous flowers to determine whether it differed from the 100% self-fertilized belowground seeds. Approximately 25% of seeds from chasmogamous flowers showed evidence of cross-pollination. Assuming that chasmogamous flowers produce the majority of the aboveground seeds, as was shown previously, this indicates it is possible to differentiate between germination by aboveground vs. belowground seeds in post-fire colonization. We next compared genetic diversity, admixture, inbreeding, and population genetic structure pre- and post-fire. If fire promoted germination of chasmogamous seeds, heterozygosity and admixture would increase, and genetic structure and inbreeding would decrease. Instead, inbreeding and genetic structure increased and admixture decreased, suggesting that the belowground selfed seeds (with limited dispersal ability) increased their contribution to the population after fire, possibly because fire reduced aboveground seed viability. Additionally, new alleles not found previously in rangewide analyses emerged from the seed bank post-fire. These results suggest that amphicarpy is a powerful adaptation to preserve genetic variation, maintain adaptive potential, and promote rapid post-fire colonization.
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