Seagrass Radiation after Messinian Salinity Crisis Reflected by Strong Genetic Structuring and Out-of-Africa Scenario (Ruppiaceae)

Abstract

Many aquatic plant and seagrass species are widespread and the origin of their continent-wide ranges might result from high gene flow levels. The response of species when extending northwards since the Last Glacial Maximum can be opposed to the structuring of their populations that survived glaciation cycles in southern regions. The peri-Mediterranean is a complex series of sea basins, coastlines, islands and river deltas with a unique history since the Messinian Crisis that potentially influenced allopatric processes of aquatic life. We tested whether vast ranges across Europe and the peri-Mediterranean of a global seagrass group (Ruppia species complexes) can be explained by either overall high levels of gene flow or vicariance through linking population genetics, phylogeography and shallow phylogenetics. A multigene approach identified haplogroup lineages of two species complexes, of ancient and recent hybrids with most of the diversity residing in the South. High levels of connectivity over long distances were only observed at recently colonized northern ranges and in recently-filled seas following the last glaciation. A strong substructure in the southern Mediterranean explained an isolation-by-distance model across Europe. The oldest lineages of the southern Mediterranean Ruppia dated back to the period between the end of the Messinian and Late Pliocene. An imprint of ancient allopatric origin was left at basin level, including basal African lineages. Thus both vicariance in the South and high levels of connectivity in the North explained vast species ranges. Our findings highlight the need for interpreting global distributions of these seagrass and euryhaline species in the context of their origin and evolutionary significant units for setting up appropriate conservation strategies.

Climate Change Impacts on Seagrass Meadows and Macroalgal Forests: An Integrative Perspective on Acclimation and Adaptation Potential

“…In the Mediterranean, ancient vicariance events, hypothetically attributed to the Messinian Salinity Crisis, were reported in the seagrasses Posidonia oceanica (Arnaud-Haond et al, 2007b;Serra et al, 2010) and Ruppia spp. (Triest and Sierens, 2014), although niche modeling indicated that the present phylogeography of P. oceanica is also shaped by more recent climate refugia . Mediterranean-Atlantic vicariance with two glacial refugia in West Africa and the Eastern Mediterranean was suggested in Cymodocea nodosa based on allelic distributions (Alberto et al, 2008), and niche models .…”

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

“…To enhance the understanding of the phylogenetic relationships within the genus, chloroplast markers and a limited set of nuclear markers were used to study different Ruppia species and populations from different continents (Ito, Ohi‐Toma, Murata, & Tanaka, , ; Martinez‐Garrido, Serrao, Engelen, & González‐Wangüemert, ; Triest & Sierens, , , , ; Yu, Shi, & Chen, ). These markers revealed independently a high level of complexity within the genus, caused by hybridization, introgression, polyploidy, and haplotype convergence.…”

“…Ito et al (, ) circumscribes this as a single R. maritima complex, despite maternal cpDNA referring to R. cirrhosa relationship and despite ample populations of independent studies (Martinez‐Garrido et al, ; Triest & Sierens, ; Yu et al, ) confirming the separation of R. cirrhosa as a distinct gene pool at nuclear DNA level. Only three ITS variants of Ruppia were detected so far and should be complemented with additional nuclear markers to unravel delineation of Ruppia taxa (Triest & Sierens, ). Individuals belonging to R. maritima and R. drepanensis were considered diploid, whereas tetraploidy was observed in most other taxa (Martinez‐Garrido et al, ; Triest & Sierens, , ).…”

“…Only three ITS variants of Ruppia were detected so far and should be complemented with additional nuclear markers to unravel delineation of Ruppia taxa (Triest & Sierens, ). Individuals belonging to R. maritima and R. drepanensis were considered diploid, whereas tetraploidy was observed in most other taxa (Martinez‐Garrido et al, ; Triest & Sierens, , ). When used in ecological studies, populations containing different ploidy levels or cryptic species could lead to inaccurate estimations of, for example, annual versus perennial survival strategies or biomass allocation in belowground and aboveground structures (Mannino et al, ).…”

“…Throughout Europe, Ruppia cirrhosa is far more widespread and locally abundant in a much wider variety of coastal habitats than R. maritima . Likewise, identification of its evolutionary units at continental scale is rendered difficult by morphologically variable and hybridized populations, especially in Mediterranean lagoons and coastal wetlands (Triest & Sierens, ). An out‐of‐Africa hypothesis was presented for many Mediterranean lineages (Triest & Sierens, ) and the W Mediterranean can be considered as the origin of R. cirrhosa diversity (Martinez‐Garrido et al, ; Triest & Sierens, , ).…”