The origin and diversification of Amaryllidaceae: A phylogenetic and biogeographic analysis

Abstract

Premise: Previous angiosperm-wide studies estimated that the geophytic family Amaryllidaceae diverged in Africa 87.00-46.77 million years ago (mya), spanning the Cretaceous and Palaeogene periods, including multiple important climatic and geological events. Greater precision on when and where this divergence occurred is lacking due to limited sampling of Amaryllidaceae and the paucity of the monocot fossil record. A robust phylogeny is required to estimate the age and origin of suprageneric groups; however, the evolutionary relationships within Amaryllidaceae are unclear.

Methods: We used 78 plastome protein-coding genes to infer the phylogenetic relationships of Amaryllidaceae and estimated the age of the family using four fossils and five secondary calibration points from across the Asparagales. We conducted a new biogeographic analysis to determine the ancestral origins of Amaryllidaceae and suprageneric groups, providing insights into the drivers of diversification.

Results: Our phylogenetic analyses recovered Amaryllidaceae as monophyletic, with Agapanthoideae sister to Amaryllidoideae and Allioideae. We estimate that Amaryllidaceae diverged in southern Africa 48.6 mya (50.3-46.6 mya) during the early Eocene, a period of elevated global temperatures with increasing seasonal aridity. Our biogeographic analyses indicate that taxa migrated from Africa via the Arabian Peninsula to temperate Asia and beyond during the Miocene.

Conclusions: The comprehensive taxon sampling across Amaryllidaceae, the greater number of genes, and the placement of fossils has made it possible to substantially refine estimates of lineage divergence. Establishing a robust age estimate and reconstructing the biogeographic history has led to a better understanding of evolution within the family, of present-day distributions, and of possible drivers of diversification.

Keywords: Amaryllidaceae; biogeography; divergence times; geophyte; molecular phylogeny; monocot evolution; plastid DNA.

Figure 1

Members of each Amaryllidaceae tribe, showing examples of morphological variation across the family. Photos belong to Zoë Dennehy‐Carr, Alastair Culham, and John David, except for Calostemmateae (Melburnian, 2012). Geophytic habit(s) are represented for each tribe (bulb = ; rhizome = ).

Figure 2

Approximated maximum likelihood phylogeny of Amaryllidaceae based on 78 plastid protein‐coding genes collapsed at genus level. Paraphyletic and polyphyletic genera were collapsed at each of their monophyletic groups. Bootstrap support values are 100% unless otherwise indicated.

Figure 3

Chronogram of Amaryllidaceae inferred using MrBayes based on 78 plastome protein‐coding genes. Numbers represent median divergence ages in millions of years ago (mya). Nodes constrained by a fossil are denoted by a pink circle at the cusp of the relevant note. Nodes constrained by a secondary calibration point are denoted by a yellow circle at the cusp of the relevant node. Timings of epochs and ages listed in mya were acquired from Geological Society of America Geological Time Scale version 5.0.

Figure 4

Ancestral state reconstruction of Amaryllidaceae under the BAYAREALIKE +j model using BioGeoBEARS as implemented in RASP version 4.2. Most likely ancestral area shown at internal nodes and terminal tips. A = northern Africa; B = Europe; C = Cape Provinces, South Africa; D = South Africa (excluding Cape Provinces); E = southern Africa (excluding South Africa); and south tropical Africa; F = North America; G = temperate Asia; H = west central and east tropical Africa; I = west tropical, northeast Africa, and Arabian Peninsula; J = western South America; K = Australasia and Southwest Pacific; L = tropical Asia; M = Chile; N = Argentina, Brazil, Paraguay, and Uruguay; and O = Central America and the Caribbean.

Figure 5

(A) Geological timeline from the Eocene to the present day. Key climatic and geological events that may have influenced Amaryllidaceae evolution are listed along with mean crown divergence ages for Amaryllidaceae, all subfamilies, and key groups. Timings of epochs and ages (in millions of years ago) were acquired from the Geological Society of America Geological Time Scale version 5.0. Initial timeline was generated using TSCreator version 8.0. (B) Illustration of predicted ancestral dispersal pathways of Amaryllidoideae groups from the Cape Provinces, South Africa, southern Africa, and south tropical Africa. Dashed lines indicate secondary colonization event.