Lagoons and saltwater wetlands getting more diversity: A molecular approach reveals cryptic lineages of a euryhaline submerged macrophyte (Ruppia)

Abstract

Abstract Ruppia species are distantly related to seagrasses and occur in saltwater coastal and inland lagoons, mostly as monospecific beds. The diversity of euryhaline Ruppia populations from different continents recently became better understood from a suite of chloroplast sequences but limited nuclear markers. These revealed a high complexity from hybridization, introgression, polyploidy and haplotypic divergence. Because of this complexity within the genus and multiple allelic states in polyploids, three multiplexed sets of 24 nuclear microsatellites were developed from four Ruppia provenances and cross‐amplified on 130 individuals from a wide range of taxa in various aquatic habitats on different continents. Secondly, pure R. cirrhosa and R. maritima individuals could be unambiguously identified from their introgressed hybrids and from other known or yet unidentified taxa, using diagnostic markers that referred to autotetraploid individuals in R. cirrhosa and allotetraploidy in an ancient hybrid complex ‘haplogroup E’. Thirdly, a phenetic barcoding approach of trnH‐psbA chloroplast haplotypes taking into account insertion–deletion variations, revealed lineages of recently described taxa from lagoons in different continents (i.e. R. sinensis, R. brevipedunculata, R. mexicana) in addition to separate lineages of hybrid origin. Congruence between pollination mode and diversification of lineages, allows one to hypothesize whether selfing underwater leads to clearly separated lineages whereas outcrossing at the water surface allows hybridization and extensive introgression with potential chloroplast capture. This study raises a renewed interest in cryptic lineages, hybrid taxa and shallow phylogenies of Ruppia lineages, thereby critically questioning worldwide distributions of least concern species. Recognition and monitoring of unique Ruppia lineages will support further studies on connectivity, survival strategies and movement ecology to aid in determining the conservation status of a wide variety of lagoon and coastal wetland habitats.