Morphological Innovations and Vast Extensions of Mountain Habitats Triggered Rapid Diversification Within the Species-Rich Irano-Turanian Genus Acantholimon (Plumbaginaceae)

Abstract

The Irano-Turanian floristic region spans a topographically complex and climatically continental territory, which has served as a source of xerophytic taxa for neighboring regions and is represented by a high percent of endemics. Yet, a comprehensive picture of the abiotic and biotic factors that have driven diversification within this biota remains to be established due to the scarcity of phylogenetic studies. Acantholimon is an important component of the subalpine steppe flora of the Irano-Turanian region, containing c. 200 cushion-forming sub-shrubby pungent-leaved species. Our recent molecular phylogenetic study has led to enlarging the circumscription of this genus to include eight mono- or oligospecific genera lacking the characteristic life-form and leaves. Using the same molecular phylogeny, here we investigate the tempo and mode of diversification as well as the biogeographic patterns in this genus, to test the hypothesis that a combination of key morphological innovations and abiotic factors is behind Acantholimon high species diversity. Molecular dating analysis indicates that Acantholimon s.l. started to diversify between the Late Miocene and the Pliocene and the biogeographic analysis points to an Eastern Iran–Afghanistan origin. Macroevolutionary models support the hypothesis that the high diversity of the genus is explained by accelerated diversification rates in two clades associated with the appearance of morphological key innovations such as a cushion life-form and pungent leaves; this would have favored the colonization of water-stressed, substrate-poor mountainous habitats along the newly uplifted IT mountains during the Mio-Pliocene. Given the apparent similarity of mountain habitats for most species of Acantholimon, we hypothesize that its current high species diversity responds to a scenario of non-adaptive radiation fueled by allopatric speciation rather than evolutionary radiation driven by ecological opportunity. Similar scenarios might underlie the high diversity of other speciose genera in the topographically complex Irano-Turanian landscape, though this remains to be tested with fine-grained distribution and climatic data.

Diversification dynamics of hypermetamorphic blister beetles (Meloidae): Are homoplastic host shifts and phoresy key factors of a rushing forward strategy to escape extinction?

“…While trying to understand why certain groups diversify more than others, the idea of a single key factor promoting elevated diversification rates (e.g., the evolution of a morphological innovation, the invasion of a new isolated environment, or the effect of a mass extinction event depleting extant diversity) has been a dominant one in the literature (Hodges & Arnold 1995; Hunter & Jernvall 1995; De Queiroz 2002; Donoghue 2005). Yet, despite the numerous recent studies testing for an association between trait evolution and diversification, few of them have found evidence of a single trait driving a shift in diversification rates (Lagomarsino et al 2017; Condamine et al 2018; Moharrek et al 2019). Instead, the dominant pattern is one in which bursts of diversification are explained by the confluence of multiple factors, sometimes acting at unison (Donoghue & Sanderson 2015), sometimes in a sequence (Donoghue 2005), or contingent upon one another (Givnish et al 2015).…”

Secretory structures in plants: Lessons from the Plumbaginaceae on their origin, evolution and roles in stress tolerance

“…Goniolimon species that thrives in steppe-like habitats (xerophilous pastures and rocky grounds) in hilly regions has salt glands on its leaves and stems (Buzurovic, Stevanovic, Niketic, Jakovljevic, & Tomovic, 2013;Faraday & Thomson, 1986c;Waisel, 1972), although glands are not present in Acantholimon that colonised mountainous regions in dry habitats on gravelly and stony soils or on exposed rocks (Moharrek et al, 2019).…”

“…Genera of the Limonoideae are thought to have initially diversified in the Mediterranean and Irano-Turian regions, although a few genera also occur in the Southern Hemisphere (Lledó, Crespo, Fay, & Chase, 2005;Malekmohammadi, Akhani, & Borsch, 2017;Moharrek et al, 2019; Table S2): Aegialitis is the only genus of the Limonioideae with a tropical distribution (two mangrove species in Asia and Oceania). Within the Plumbaginoideae, its members predominantly occur in arid and saline environments and often in coastal habitats (Hernandez-Ledesma et al, 2015;Kubitzki, 1993;Malekmohammadi et al, 2017;Moharrek et al, 2019). Of the nearly 940 species in the family as a whole, 5% display salt tolerance (Table S2), ranking the family fourth in a list based on the proportion of species within a family that are halophytes (Santos, Al-Azzawi, Aronson, & Flowers, 2016).…”

The first bioactivity studies of Acantholimon lycopodioides from high altitude Karakoram-Himalayan desert

“…are pulvinate to densely branched shrubs/subshrubs that bear spike-like inflorescences with rigid acuminate or paniculate leaves ( Baker, 1948 ). Most of them are geographically restricted in mid to high altitude mountains of southeastern Russia, Kazakhstan, Tajikistan, Western Iran, Afghanistan, northwest China, southern Mongolia, western Pakistan and northern India, and to little extent in the Mediterranean region ( Moharrek et al, 2019 ). In the mountainous Wakhan and Pamir in northeastern Afghanistan, Acantholimon is an important fuel source ( Soelberg and Jäger, 2016 ).…”

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Fig. 1 Acantholimon lycopodioides : (A) its geographical distribution in high altitude Karakoram-Himalayan ranges ( Moharrek et al, 2019 ; https://www.gbif.org/occurrence/download?taxon_key=4089167 ); (B) its collection location in Ladakh, India; and (C) the whole flowering plant.

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