Contribution of transition and stabilization processes to speciation is a function of the ancestral trait state and selective environment in Hakea (Reprint)
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Currently the origin and trajectories of novel traits are emphasised in evolutionary studies, the role of stabilization is neglected, and interpretations are often post hoc rather than as hypothesised responses to stated agents of selection. Here we evaluated the impact of changing environmental conditions on trait evolution and stabilization and their relative contribution to diversification in a prominent Australian genus, Hakea (Proteaceae). We assembled a time-based phylogeny for Hakea, reconstructed its ancestral traits for six attributes and determined their evolutionary trajectories in response to the advent or increasing presence of fire, seasonality, aridity, nectar-feeding birds and (in)vertebrate herbivores/granivores. The ancestral Hakea arose 18 million years ago (Ma) and was broad-leaved, non-spinescent, insect-pollinated, had medium-sized, serotinous fruits and resprouted after fire. Of the 190 diversification events that yielded the 82 extant species analysed, 850% involved evolution, stabilization or re-evolution (reversal) of individual novel traits. Needle leaves appeared 14 Ma and increased through the Neogene/Quaternary coinciding with intensifying seasonality and aridity. Spinescence arose 12 Ma consistent with the advent of vertebrate herbivores. Bird-pollination appeared 14 Ma in response to advent of the Meliphagidae in the early Miocene. Small and large woody fruits evolved from 12 Ma as alternative defenses against granivory. Fire-caused death evolved 14 Ma, accounting for 50% of subsequent events, as fire became less stochastic. Loss of serotiny began in the late Miocene as non-fireprone habitats became available but only contributed 8% of events. Innovation and subsequent stabilization of functional traits promoted the overall species diversification rate in Hakea by 15 times such that only three species now retain the ancestral phenotype. Our approach holds great promise for understanding the processes responsible for speciation of organisms when the ancestral condition can be identified and the likely selective agents are understood.
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