Genomic insights into the origin of trans-Mediterranean disjunct distributions

Aim Two main biogeographical hypotheses have been proposed to explain the Mediterranean-Turanian disjunct distributions exhibited by numerous steppe-dwelling organisms, namely (a) dispersal during the Messinian salinity crisis (similar to 5.96-5.33 Ma) followed by range fragmentation and vicariance, and (b) Pleistocene colonization and recent processes of population subdivision (<2 Ma). Despite the two hypotheses postulate the role of climatic alterations and changes in landmass configuration on determining such disjunct distributions, estimates of the timing of lineage diversification have not been complemented so far with spatially-explicit tests providing independent evidence on the proximate processes underlying geographical patterns of population genetic connectivity/fragmentation. Location Mediterranean-Turanian region. Taxon Saltmarsh band-winged grasshopper (Mioscirtus wagneri). Methods We integrate different sources of genetic (mtDNA and ddRADseq) and spatial information (configuration of emerged lands and niche modelling) to evaluate competing hypotheses of lineage diversification in the saltmarsh band-winged grasshopper, a halophile species showing a classical Mediterranean-Turanian disjunct distribution. Results Phylogenomic analyses reveal the presence of two North African cryptic lineages and support that trans-Mediterranean populations of the species diverged in the Pleistocene, with evidence of post-Messinian permeability of the Strait of Gibraltar to gene flow likely associated with sea level drops during glacial periods. Accordingly, spatial patterns of genetic differentiation are best explained by a scenario of population connectivity defined by the configuration of emerged landmasses and environmentally suitable habitats during glacial periods, a time when effective population sizes of the species peaked as inferred by genomic-based demographic reconstructions. Main conclusions Our results support post-Messinian colonization and Pleistocene diversification as the biogeographical scenario best explaining the trans-Mediterranean disjunct distributions of halophilous organisms.

Automated summary

The study revealed the existence of two North African cryptic lineages in the genetic evolution of the saltmarsh band-winged grasshopper and supported the divergence of trans-Mediterranean populations of the species in the Pleistocene, with evidence suggesting the permeability of the Strait of Gibraltar to gene flow post-Messinian. Spatial patterns of genetic differentiation are best explained by the configuration of emerged landmasses and environmentally suitable habitats during glacial periods.