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.
Highlights
The early diversification of flowering plants, a clade comprising approximately 90% of extant land plant species (Hernández-Hernández and Wiens, 2020), was marked by a rapid increase in lineage diversity, abundance, and distribution during the Late Cretaceous, 100–66 million years ago (Ma; Friis et al, 2011)
Since we found only minor differences in ancestral area estimates under the + J models compared to estimates without this parameter (Supplementary Tables 2A,B and Supplementary Figures 2–5, besides that model fit was generally much better for the + J models), we here present and discuss the estimates of the classical models
We relied on log likelihoods and the sample size corrected Akaike information criterion (AICc), calculating the AICc ( AICc > 10 was taken as good evidence to reject a model in favor of the best one; Burnham and Anderson, 2002) and Akaike weights, which indicate the relative fit of a model in relation to all models in the set
Summary
The early diversification of flowering plants (angiosperms), a clade comprising approximately 90% of extant land plant species (Hernández-Hernández and Wiens, 2020), was marked by a rapid increase in lineage diversity, abundance, and distribution during the Late Cretaceous, 100–66 million years ago (Ma; Friis et al, 2011). Rauvolfioids and apocynoids do not produce a morphologically differentiated translator and were placed in the traditional Apocynaceae s.str These two groups, form a grade toward the pollinia-bearing subfamilies: Periplocoideae, Secamonoideae, and Asclepiadoideae (e.g., Sennblad and Bremer, 1996; Fishbein et al, 2018; Antonelli et al, 2021). We associate estimates of diversification rates, historical biogeography, and morphological evolution (Endress et al, 2018-2019; Fishbein et al, 2018) to discuss the evolutionary history of Apocynaceae and to provide an overview of potential events that boosted the diversification of the family, from the uncertain origin to the uneven distribution of extant diversity
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