Biogeography, diversification and extinction risk of cycads

Abstract

Cycads have an interesting evolutionary history since they represent the oldest lineage plants that originated ~ 300 million years ago (Ma) in the mid-Permian but re-diversified recently around 12 Ma with Cycas and Encephalartos being the most rapidly diversified lineages within the cycads group. Several studies have explored the taxonomic relationships, diversification history within the two genera but there’s a limited understanding of evolutionary history, biogeography of cycads and what drives cycads to extinction risk. The aim of this study was to provide a better explanation on what predispose cycads to high risk of extinction and also elucidate the biogeography and evolutionary diversification history of the two cycads genera (African genus Encephalartos and Asian-Pacific genus Cycas). The three main objectives addressed: firstly, the ecological factors predisposing cycads to high risk of extinction was explored. Secondly, reconstruct the most comprehensive phylogeny of the two most diversified cycad genera. Lastly, investigate the evolutionary and historical biogeography of Encephalartos and Cycas. The risk of extinction using phylogenetic comparative method and fitting cumulative link mixed model on biological, ecological and evolutionary data of cycads on the most threatened lineage in the plant kingdom were investigated. Then, assembled the most complete phylogeny and reconstructed the historical biogeography of Encephalartos and Cycas using S-DIVA and Binary Bayesian model (BBM) respectively. The nine group of threats to cycads such as habitat loss, overcollection, fire, deforestation, medicinal usages, grazing, invasive alien plants, reproduction failure and the last one linked to climate change impacts flood/drought were identified. But, habitat loss, overcollection, medicinal uses and reproduction failure were clustered on the cycad tree of life suggesting that, closely related species might be exposed to similar threats implying that ecological factors that drives cycads to high risk of extinction were anthropogenically mediated and resulted in vulnerable (VU) category. The phylogenies of the two genera were found to be well supported. Encephalartos phylogeny, revealed two major clades following species geographic origins, one southern African clade and one east-central-west African clade. The biogeographic analysis suggests that the genus may have diverged around 9 Ma from southern Africa. Then colonized east-central-west African region through vicariance, suggesting that the eastern rift system in eastern Africa and the west Africa Dahomey Gap acted as a geographical barrier limiting species dispersal. Furthermore, most species accumulated in the last 2.6 Ma and there were no significant shifts in any of the evolutionary events, suggesting that a constant-rate diversification model is best suited for Encephalartos. The phylogenetic analysis of the Cycas genus pointed to Indochina as the origin of the genus, which may have dispersed firstly across the Pacific Islands during the late Miocene aided by multiple excursions of sea levels and the development of a key innovation (a spongy endocarp) particularly in the seeds of subsection Rumphiae. The colonization of South China, which was initially thought to be the origin of the Abstract _________________________________________________________________________________________________________ genus, may have occurred more recently aided by both dispersal and vicariance events. Also, no significant shifts in the evolutionary events that shaped the diversity of Cycas was observed. The findings of this study provide the evidence of historical biogeography and the evolutionary events that shaped the current diversity of the genera Encephalartos and Cycas. Overall, this study is the first to elucidates the pattern of extinction risk in cycads and also to identify that most threats that drives extinction risk of cycads were anthropogenically mediated.