Multiple Drivers of High Species Diversity and Endemism Among Alyssum Annuals in the Mediterranean: The Evolutionary Significance of the Aegean Hotspot

Abstract

The Mediterranean Basin is a significant hotspot of species diversity and endemism, with various distribution patterns and speciation mechanisms observed in its flora. High species diversity in the Mediterranean is also manifested in the monophyletic lineage of Alyssum annuals (Brassicaceae), but little is known about its origin. These species include both diploids and polyploids that grow mainly in open and disturbed sites across a wide elevational span and show contrasting distribution patterns, ranging from broadly distributed Eurasian species to narrow island endemics. Here, we investigated the evolution of European representatives of this lineage, and aimed to reconstruct their phylogeny, polyploid and genome size evolution using flow cytometric analyses, chloroplast and nuclear high- and low-copy DNA markers. The origin and early diversification of the studied Alyssum lineage could be dated back to the Late Miocene/Pliocene and were likely promoted by the onset of the Mediterranean climate, whereas most of the extant species originated during the Pleistocene. The Aegean region represents a significant diversity center, as it hosts 12 out of 16 recognized European species and comprises several (sub)endemics placed in distinct phylogenetic clades. Because several species, including the closest relatives, occur here sympatrically without apparent niche differences, we can reject simple allopatric speciation via vicariance as well as ecological speciation for most cases. Instead, we suggest scenarios of more complex speciation processes that involved repeated range shifts in response to sea-level changes and recurrent land connections and disconnections since the Pliocene. In addition, multiple polyploidization events significantly contributed to species diversity across the entire distribution range. All seven polyploids, representing both widespread species and endemics to the western or eastern Mediterranean, were inferred to be allopolyploids. Finally, the current distribution patterns have likely been affected also by the human factor (farming and grazing). This study illustrates the complexity of evolutionary and speciation processes in the Mediterranean flora.

Out of the Balkans and Anatolia to the Western Alps? Surprising phylogenetic implications for two endemicAlyssum(Brassicaceae) species:A. cognensesp. nov. andA. rossetii

“…2A which includes most annual Alyssum spp. besides this perennial complex (Cetlová et al, 2021). This result is consistent with the conspicuously different morphology and genome size of A. rossetii compared to members of the A. montanum-A.…”

“…We have shown here that A. rossetii belongs to a different clade of the genus that includes the annuals A. dasycarpum and A. macropodum and perennial species distributed mainly in Asia and mostly classified in Alyssum section Gamosepalum (Rešetnik, et al, 2013;Li et al, 2015). These two main clades recognized in Alyssum diverged in the late Miocene, whereas the Asian clade began to diversify in the Pliocene and most of the Asian perennials (section Gamosepalum) arose in the Pleistocene (Cetlová et al, 2021). This clade of mainly Asian perennials includes a few European representatives, such as A. doerfleri, A. lenense (as identified by previous authors, Warwick, Sauder & Al-Shehbaz, 2008;Rešetnik et al, 2013;Li et al, 2015), Alyssum pulvinare Velen.…”

“…Alyssum in its recently revised circumscription (Španiel et al, 2015) includes c. 114 species distributed mainly in Eurasia, which are split into two main clades (Flynn, 2013;Rešetnik et al, 2013;Li et al, 2015;Cetlová et al, 2021). One of the clades, distributed predominantly in Europe, includes almost all annuals (with the exception of Alyssum dasycarpum Stephan ex Willd.…”

Stability in the South, Turbulence Toward the North: Evolutionary History of Aurinia saxatilis (Brassicaceae) Revealed by Phylogenomic and Climatic Modelling Data

“…They triggered bottlenecks and genetic drift during population contractions, and hybridisation during their expansions, resulting in complex genetic patterns, high plastid haplotype diversity and numerous unique haplotypes separated by multiple mutation steps ( Figure 1 ) as well as slight incongruences between the plastid and genome-wide data. These processes contributed to high genetic diversity in the central parts of the Balkan Peninsula also in other plant groups ( López-Vinyallonga et al, 2015 ; Đurović et al, 2017 ; Caković et al, 2021 ; Cetlová et al, 2021 ) and highlight this area not only as a cradle of lineage diversifications, but also as a source of lineage dispersals.…”

“…Some plants experienced stable long-term persistence without extensive differentiation and range expansion during the Holocene (e.g., Aesculus hippocastanum , Walas et al, 2019 ; Euphorbia heldreichii , Caković and Frajman, 2020 ), while other groups underwent enhanced population differentiation and speciation. Recent phylogeographic studies focusing on the southern Balkan Peninsula and adjacent Aegean Basin revealed the importance of this area for genetic diversification and speciation and indicated its marginal role in northward expansion, as seen in the Alyssum montanum-repens complex ( Španiel et al, 2017 ), annual Alyssum species ( Cetlová et al, 2021 ), Campanula ( Crowl et al, 2015 ), Cymbalaria ( Carnicero et al, 2020 ), the Euphorbia verrucosa alliance ( Caković et al, 2021 ) and the genus Nigella ( Jaros et al, 2018 ). Similarly, in Veronica chamaedrys ( Bardy et al, 2010 ) and Edraianthus graminifolius ( Surina et al, 2014 ), southern populations exhibited deeper and older differentiation not followed by lineage expansions.…”