Reproductive ecology and postpollination development in the hydrophilous monocot Ruppia maritima

Abstract

Premise Water‐pollination (hydrophily) is a rare but important pollination mechanism that has allowed angiosperms to colonize marine and aquatic habitats. Hydrophilous plants face unique reproductive challenges, and many have evolved characteristic pollen traits and pollination strategies that may have downstream consequences for pollen performance. However, little is known about reproductive development in the life history stage between pollination and fertilization (the progamic phase) in hydrophilous plants. The purpose of this study was to characterize reproductive ecology and postpollination development in water‐pollinated Ruppia maritima L. Methods Naturally pollinated inflorescences of R. maritima were collected from the field. Experimental pollinations using both putatively outcross and self pollen were conducted in the greenhouse and inflorescences were collected at appropriate intervals after pollination. Pollen reception, pollen germination, pollen tube growth, and carpel morphology were characterized. Results Ruppia maritima exhibits incomplete protogyny, allowing for delayed selfing. Pollen germinated within 15 min after pollination. The average shortest possible pollen tube pathway was 425 μm and pollen tubes first reached the ovule at 45 min after pollination. The mean adjusted pollen tube growth rate was 551 μm/h. Conclusions Ruppia pollen is adapted for rapid pollen germination, which is likely advantageous in an aquatic habitat. Small effective pollen loads suggest that pollen competition intensity is low. Selection for traits such as a long period of stigma receptivity, fast pollen germination, and carpel morphology likely played a larger role in shaping postpollination reproductive development in Ruppia than evolution in pollen tube growth rates.

Low Genetic Connectivity of Strongly Inbred Ruppia brevipedunculata in Aquaculture Dominated Lagoons (Viet Nam)

“…In contrast, populations of Halophila beccarii studied in the same lagoon complex (Cau Hai) did not show evidence of inbreeding or selfing and were maintained by local seed recruitment and clonal extension (Phan et al, 2017). The strong ability of selffertilization in Ruppia is strongly determined by the location of pollen release, with hypohydrophily hypothesized to be less efficient for outcrossing than pollen transfer along the water surface (Taylor et al, 2020). Due to the very short peduncle, R. brevipedunculata may be restricted to pollen release and pollen capture under the water surface which most likely explains selffertilization as the most prevalent pollination strategy for R. brevipedunculata in our study.…”

“…Due to the very short peduncle, R. brevipedunculata may be restricted to pollen release and pollen capture under the water surface which most likely explains selffertilization as the most prevalent pollination strategy for R. brevipedunculata in our study. The ability of selfing in Ruppia may increase seed-set (Les, 1988;Taylor et al, 2020) and provides reproductive assurance when mates are scarce or vectors for pollen flow are absent or inadequate (Wright et al, 2013;Razanajatovo et al, 2016). Autogamy could therefore promote the establishment and sustainability of R. brevipedunculata populations in enclosed and isolated habitats.…”

“…Dense vegetation in stagnant water may explain the elevated levels of pollen flow between individuals in aquaculture ponds whereas pollen in open lagoon sites could be lost when not immediately used upon release for self-fertilization (Van Vierssen et al, 1984;Reusch, 2003). Geitonogamy could be an additional and important form of self-fertilization alongside autogamy (Reusch, 2001;Taylor et al, 2020), especially when pollen are released between entangled branches of a same plant. Due to the physical enclosure and dense patches within high-tide ponds, both local outcrossing, evidenced by the lower inbreeding values and the higher number of multilocus genotypes in these particular man-made habitats, and geitonogamy can be hypothesized.…”

“…Pollination in Ruppia is characterized by hydrophily with either the release of pollen underwater in an air bubble or on the water surface (Cox and Knox, 1989;Kaul, 1993;Lacroix and Kemp, 1997;Yu and den Hartog, 2014). Flexibility in pollen release and capture location has been observed in R. maritima where the location depends on local environmental conditions and the time of pollen maturation (Lacroix and Kemp, 1997;Taylor et al, 2020). Ruppia fruits, which contain negatively buoyant seeds, sink almost immediately to the bottom when ripe and detached, and contribute to local seed banks which most likely have an important role in the yearly replenishment of Ruppia populations (Strazisar et al, 2013;Triest and Sierens, 2013;Mannino et al, 2015).…”

“…Most population genetic studies focused on Ruppia species of Europe, more specifically in the Mediterranean, and recorded low levels of genetic diversity and strong inbreeding in R. maritima L. populations due to high levels of self-fertilization (Triest and Sierens, 2015). Consequently, selfing, which is promoted by bisexual flowers and the location of pollen release and capture, is considered to be the predominant reproduction strategy in those Ruppia species closely related to R. maritima (Triest et al, 2018a) though an incomplete protogyny that facilitates delayed selfing increases the potential for outcrossing before self-pollination can occur (Goodwillie and Weber, 2018;Taylor et al, 2020). Nevertheless, inter-and intraspecific variation in Ruppia has been shown in the contribution of self-fertilization, biparental inbreeding and outcrossing for population growth and sustainability (Triest and Sierens, 2015;Triest et al, 2018a;Beirinckx et al, 2020).…”