Evolution of Dispersal, Habit, and Pollination in Africa Pushed Apocynaceae Diversification After the Eocene-Oligocene Climate Transition

Abstract

Apocynaceae (the dogbane and milkweed family) is one of the ten largest flowering plant families, with approximately 5,350 species and diverse morphology and ecology, ranging from large trees and lianas that are emblematic of tropical rainforests, to herbs in temperate grasslands, to succulents in dry, open landscapes, and to vines in a wide variety of habitats. Despite a specialized and conservative basic floral architecture, Apocynaceae are hyperdiverse in flower size, corolla shape, and especially derived floral morphological features. These are mainly associated with the development of corolline and/or staminal coronas and a spectrum of integration of floral structures culminating with the formation of a gynostegium and pollinaria—specialized pollen dispersal units. To date, no detailed analysis has been conducted to estimate the origin and diversification of this lineage in space and time. Here, we use the most comprehensive time-calibrated phylogeny of Apocynaceae, which includes approximately 20% of the species covering all major lineages, and information on species number and distributions obtained from the most up-to-date monograph of the family to investigate the biogeographical history of the lineage and its diversification dynamics. South America, Africa, and Southeast Asia (potentially including Oceania), were recovered as the most likely ancestral area of extant Apocynaceae diversity; this tropical climatic belt in the equatorial region retained the oldest extant lineages and these three tropical regions likely represent museums of the family. Africa was confirmed as the cradle of pollinia-bearing lineages and the main source of Apocynaceae intercontinental dispersals. We detected 12 shifts toward accelerated species diversification, of which 11 were in the APSA clade (apocynoids, Periplocoideae, Secamonoideae, and Asclepiadoideae), eight of these in the pollinia-bearing lineages and six within Asclepiadoideae. Wind-dispersed comose seeds, climbing growth form, and pollinia appeared sequentially within the APSA clade and probably work synergistically in the occupation of drier and cooler habitats. Overall, we hypothesize that temporal patterns in diversification of Apocynaceae was mainly shaped by a sequence of morphological innovations that conferred higher capacity to disperse and establish in seasonal, unstable, and open habitats, which have expanded since the Eocene-Oligocene climate transition.