Divide to Conquer: Evolutionary History of Allioideae Tribes (Amaryllidaceae) Is Linked to Distinct Trends of Karyotype Evolution

Abstract

Allioideae (e.g., chives, garlics, onions) comprises three mainly temperate tribes: Allieae (800 species from the northern hemisphere), Gilliesieae (80 South American species), and Tulbaghieae (26 Southern African species). We reconstructed the phylogeny of Allioideae (190 species plus 257 species from Agapanthoideae and Amaryllidoideae) based on ITS, matK, ndhF, and rbcL to investigate its historical biogeography and karyotype evolution using newly generated cytomolecular data for Chilean Gilliesieae genera Gethyum, Miersia, Solaria, and Speea. The crown group of Allioideae diversified ∼62 Mya supporting a Gondwanic origin for the subfamily and vicariance as the cause of the intercontinental disjunction of the tribes. Our results support the hypothesis of the Indian tectonic plate carrying Allieae to northern hemisphere ('out-of-India' hypothesis). The colonization of the northern hemisphere (∼30 Mya) is correlated with a higher diversification rate in Allium associated to stable x = 8, increase of polyploidy and the geographic expansion in Europe and North America. Tulbaghieae presented x = 6, but with numerical stability (2n = 12). In contrast, the tribe Gilliesieae (x = 6) varied considerably in genome size (associated with Robertsonian translocations), rDNA sites distribution and chromosome number. Our data indicate that evolutionary history of Allioideae tribes is linked to distinct trends of karyotype evolution.

Keywords: Amaryllidaceae; BioGeoBEARS; biogeography; cytogenetics; genome size; phylogenetic comparative methods (PCMs); rDNA sites.

FIGURE 1

Geographic distribution and diversification patterns of the three tribes of the subfamily Allioideae (Amaryllidaceae). Geographic distribution was obtained from http://www.gbif.org.

FIGURE 2

Mitotic cells showing the distribution of 5S (red) and 35S (green) rDNA sites in Chilean Gilliesieae species. (A,B) Individuals of Miersia chilensis com 2n = 20 (2SM + 18A) (A) and 2n = 12 (8M + 2SM + 2A) (B). (C) Speea humilis 2n = 12 (8M + 2SM + 2A). (D–F) Species with 2n = 14 (4M + 4SM + 6A): Gilliesia graminea (D), Gethyum atropurpureum (E), and Solaria miersioides (F). Scale bar in (F) = 10 μm.

FIGURE 3

Ancestral chromosome number reconstruction inferred with ChromEvol of Amaryllidaceae species. Numbers at nodes represent the most probable ancestral chromosome number (n). Dispersion plots at the right of the phylogeny represent the chromosome numbers and genome sizes (1C_x values) of the different Allioideae groups.

FIGURE 4

Evolution of rDNA sites across Amaryllidaceae phylogeny. (A) Ancestral number of 35S rDNA sites reconstruction on a pruned phylogeny of Amaryllidaceae. Hot branch colors indicate higher number of sites while cold colors represent lower number of sites. (B) Schematic idiograms showing the position of 5S (red) and 35S (green) rDNA sites on the chromosomes of species of the subfamily Allioideae. Darker regions represent the centromere.

FIGURE 5

Ancestral range reconstruction for Amaryllidaceae (under the DEC + J model) focusing on subfamily Allioideae. Pie charts at the nodes represent the probability of ancestral range. Colored slices represent the most probable ancestral range while white slices represent other possible ranges. Panels (A–D) are paleomaps representing the geological state of the Earth at 120, 65, 40, and 20 Mya, respectively.

FIGURE 6

Rate of diversification through time on the subfamily Allioideae. On the left, the dated phylogeny of the subfamily, with colored branches indicating the rate of diversification. Colder colors represent low rates, while hot colors represent high rates. On the right, plots of diversification rate through time for each Allioideae lineage. Strong red lines represent the consensus correlation, while purple shade represents the uncertainty of the analysis.