Abstract
Lagoonal environments exhibit high levels of instability depending on hydrological, climatic and ecological factors, thereby influencing the distribution and structure of submerged plant communities. Conditions typically fluctuate widely due to the interaction of freshwater from rivers with saltwater from the sea, as well as from aquaculture activities that together influence submerged hydrophyte community spatial and temporal variability depending on plant survival strategies. Ruppia species feature either underwater pollination mediated by an air bubble or by the release of pollen floating at the water surface, the former promoting self-pollination. Tropical Asian Ruppia brevipedunculata Yu and den Hartog was assumed to pollinate below the water surface and identified as a separate lineage among selfed Ruppia taxa. We used nine nuclear microsatellites to estimate inbreeding levels and connectivity of R. brevipedunculata within a large SE Asian lagoon complex. Ruppia brevipedunculata meadows were strongly inbred as could be derived from the many monomorphic or totally fixed loci for unique alleles in different parts of the lagoon, which appears consistent with selfing behavior. Those from aquaculture ponds were highly inbred (FIS = 0.620), though less than open lagoon sites that showed nearly total inbreeding (FIS = 0.942). Ruppia brevipedunculata from two major lagoon parts were highly differentiated with spatially structured gene pools and a strong barrier between parts of the lagoon over a 30 km distance. Migration-n analysis indicated unidirectional though limited gene flow and following potential hydrological connectivity. Overall, private alleles under homozygote conditions explained a stronger genetic differentiation of populations situated inside aquaculture ponds than of open lagoon populations. Kinship values were only relevant up to 5 km distance in the open lagoon. Within a confined area of aquaculture ponds featuring dense vegetation in stagnant water, there would be opportunity for mixed pollination, thereby explaining the higher diversity of unique multilocus genotypes of aquaculture pond habitats. Low connectivity prevents gene pools to homogenize however promoted sites with private alleles across the lagoon. Complex hydrodynamic systems and human-made habitats enclosed by physical structures impose barriers for propagule dispersal though may create refugia and contribute to conserving regional genetic diversity.
Highlights
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)
Summary values of the Deviance Information Criterion (DIC) as obtained from INEST further allowed for comparison of seven models to explain the large homogeneity encountered or potential null alleles considering “f ” the inbreeding; “n” the null alleles; and “b” genotyping failures and all combinations thereof
The very high levels of inbreeding in all sites with selfing rate estimations exceeding 0.90 are presumed to be the result of the self-pollination mating system of R. brevipedunculata. These findings are consistent with a broad-scale study on R. maritima populations in the Mediterranean where low genetic diversity, a high number of monomorphic and fixed loci and significant though lower levels of inbreeding were attributed to selffertilization (Triest and Sierens, 2015)
Summary
Physical alterations of the environment due to coastal development (Waycott et al, 2009; Grech et al, 2011; Unsworth et al, 2019), run-off from urban, agricultural and industrial areas (Waycott et al, 2009; Grech et al, 2011; Unsworth et al, 2019) together with ocean warming (Duarte et al, 2018; Kendrick et al, 2019) are the main stressors resulting in worldwide seagrass decline. Ruppia species appear to be more resistant toward environmental perturbations because of their high tolerance toward fluctuations in salinity, temperature and turbidity (Verhoeven, 1979; Mannino et al, 2015), their high colonization potential due the capability of self-pollination, large seed sets (Kendrick et al, 2012), fast rhizome growth rates (Marbà and Duarte, 1998), and the possibility of recovery after disturbance from seed banks (Strazisar et al, 2013). 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). 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)
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