Genomic insights into the origin of trans‐Mediterranean disjunct distributions

Abstract

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 (∼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.

Genomic inferences in a thermophilous grasshopper provide insights into the biogeographic connections between northern African and southern European arid‐dwelling faunas

“…Accordingly, our palaeodistribution reconstructions at fine temporal resolution supported the presence of corridors of suitable habitats across the Mediterranean coast of Africa that connected the central Maghreb region and the Middle East during the warmer stages of the Pleistocene (i.e., the Holocene Climate Optimum; Figure 5d). This distribution gap in northeastern Africa is analogous to that reported for two other arid‐dwelling taxa with trans‐Mediterranean disjunct distributions of Pleistocene origin: the saltmarsh grasshopper ( Mioscirtus wagneri ; Noguerales et al, 2021) and the spur‐thighed tortoise ( Testudo graeca ; Fritz et al, 2009). Collectively, these results suggest that the contraction of suitable habitats in northeastern Africa is the most parsimonious explanation for the contemporary disjunct distributions observed in some thermophilous organisms that probably presented wider distributions across the Mediterranean region during the warmest stages of the Pleistocene (Noguerales et al, 2021; Ribera & Blasco‐Zumeta, 1998).…”

“…Our results support the Pleistocene connectivity between northern African and southern European arid habitats and the strong genetic cohesiveness of thermophilous terrestrial faunas shared between the two continents (Husemann et al, 2014;e.g., Graciá, Giménez, et al, 2013;Habel et al, 2010;Noguerales et al, 2021). Divergence ing with sea-level lowering during glacial maxima Noguerales et al, 2021). Although these grasshoppers are good flyers and have a high intrinsic dispersal capacity, the…”

“…In some instances, these taxa show remarkable genetic distinctiveness (i.e., vicariant lineages, subspecies or even species) with respect to core distributions in Central Asia or North Africa, representing a unique evolutionary legacy of high conservation value (Husemann et al, 2014;Kajtoch et al, 2016;Kirschner et al, 2020). Despite recent advances, the temporal and geographic origin of thermophilous and arid-dwelling European species is not yet well understood, which in part might be due to the extraordinarily dynamic geological history of the region and the difficulty to distinguish among alternative biogeographical scenarios (Noguerales et al, 2021;Ribera & Blasco-Zumeta, 1998).…”

“…Miocene‐Pliocene movements of African and Asian continental plates led to the permanent closing of the eastern end of the current Mediterranean Sea (c. 23–14 Ma) and the temporal closure of the Mediterranean‐Atlantic seaways during the Messinian Salinity Crisis (c. 5.96–5.33 Ma; Bialik et al, 2019; Meulenkamp & Sissingh, 2003), which contributed to faunal and floral exchanges between Africa, Europe and Asia (e.g., Faille et al, 2014; Manafzadeh et al, 2014; Sanmartín, 2003). However, several studies have also found post‐Messinian colonization and considerable genetic cohesiveness between thermophilous and arid‐adapted biotas of Europe and those from North Africa (Husemann et al, 2014) and Central Asia steppes (Kirschner et al, 2020), indicating that their current disjunct distributions are most likely a consequence of range expansion‐fragmentation dynamics linked to Pleistocene climatic oscillations (e.g., Habel et al, 2010; Noguerales et al, 2021). In some other cases, the role of human‐mediated dispersal or historical introductions in the distribution of some thermophilous organisms in southern Europe cannot be discarded (Husemann et al, 2014).…”

The hidden landscape: Evidence that sea‐level change shaped the present population genomic patterns of marginal marine species

“…Growing evidence suggests that sea‐level change has dramatically affected the evolution of marginal marine species (Keyse et al, 2018; Noguerales et al, 2020; Stiller et al, 2017, 2020; Thomaz & Knowles, 2020). One of the most important lessons from this study is that to understand present patterns of coastal species requires looking beyond the present‐day landscape to consider the “hidden” coastline and how it changed during ice age cycles.…”