Miocene climate change as a driving force for multiple origins of annual species in Astragalus (Fabaceae, Papilionoideae).

ABSTRACT

Astragalus, a highly diverse genus of flowering plants with its highest center of diversity in West Asia, is a classic example of rapid species-level radiation and adaptation to a diversity of habitats throughout the world. We examined the historical biogeography of Astragalus using molecular dating and ancestral area reconstruction to understand how past climate changes, geographical patterns and transition in life history have provoked diversification of Astragalus. Our results suggest that Astragalus probably originated during the middle Miocene in West Asia, underwent rapid diversification, subsequently and repeatedly expanded its range in the Mediterranean region, and later to North America through West Europe. This distribution range was also extended toward central and eastern Asia from the Middle Miocene to Pleistocene. Several climatic and geological processes during the Miocene-Pliocene may be implicated in the diversification of the major Astragalus clades. In particular, the annual lineages, which are important elements in the Mediterranean flora of Africa and Europe and in the deserts of southwest to central Asia, have arisen in response to progressing aridity from the late Miocene onwards (between 8.6 Ma and 2.98 Ma). Diversification rate analyses indicate three rapid and recent diversification events, one at c. 11 Ma in the clade that groups most of the Astragalus s.s. (all except the Ophiocarpus sister lineage), one at c. 5 Ma in the crown group of the Hypoglottis clade, including herbaceous annual and perennial species, and the most recent one at c. 3 Ma in the spiny cushion forming Astracantha clade. Our study highlights the complexity of processes and factors shaping diversifications in Astragalus; a complex interaction among climatic modifications providing opportunities for diversification and likely coincident with the evolution of key morphological and physiological adaptations.