Phylogenomics of the Andean Tetraploid Clade of the American Amaryllidaceae (Subfamily Amaryllidoideae): Unlocking a Polyploid Generic Radiation Abetted by Continental Geodynamics

Abstract

One of the two major clades of the endemic American Amaryllidaceae subfam. Amaryllidoideae constitutes the tetraploid-derived (n = 23) Andean-centered tribes, most of which have 46 chromosomes. Despite progress in resolving phylogenetic relationships of the group with plastid and nrDNA, certain subclades were poorly resolved or weakly supported in those previous studies. Sequence capture using anchored hybrid enrichment was employed across 95 species of the clade along with five outgroups and generated sequences of 524 nuclear genes and a partial plastome. Maximum likelihood phylogenetic analyses were conducted on concatenated supermatrices, and coalescent-based species tree analyses were run on the gene trees, followed by hybridization network, age diversification and biogeographic analyses. The four tribes Clinantheae, Eucharideae, Eustephieae, and Hymenocallideae (sister to Clinantheae) are resolved in all analyses with > 90 and mostly 100% support, as are almost all genera within them. Nuclear gene supermatrix and species tree results were largely in concordance; however, some instances of cytonuclear discordance were evident. Hybridization network analysis identified significant reticulation in Clinanthus, Hymenocallis, Stenomesson and the subclade of Eucharideae comprising Eucharis, Caliphruria, and Urceolina. Our data support a previous treatment of the latter as a single genus, Urceolina, with the addition of Eucrosia dodsonii. Biogeographic analysis and penalized likelihood age estimation suggests an origin in the Cauca, Desert and Puna Neotropical bioprovinces for the complex in the mid-Oligocene, with more dispersals than vicariances in its history, but no extinctions. Hymenocallis represents the only instance of long-distance vicariance from the tropical Andean origin of its tribe Hymenocallideae. The absence of extinctions correlates with the lack of diversification rate shifts within the clade. The Eucharideae experienced a sudden lineage radiation ca. 10 Mya. We tie much of the divergences in the Andean-centered lineages to the rise of

Comparative plastomics of Amaryllidaceae: inverted repeat expansion and the degradation of the ndh genes in Strumaria truncata Jacq.

“…Amaryllidaceae J. St.-Hil. ( Saint-Hilaire, 1805 ) is a cosmopolitan family of bulbous geophytes and rhizomatous perennials in Asparagales ( Meerow, 2000 ) comprising approximately 90 genera, and over 1,700 species ( Meerow, Gardner & Nakamura, 2020 ), in three subfamilies: Amaryllidoideae, Allioideae, and Agapanthoideae, all of which share an umbellate inflorescence. This family of petaloid monocots contains many horticulturally important genera, including: Agapanthus, Allium, Amaryllis, Clivia, Galanthus, Hippeastrum, Narcissus, and Nerine ( Heywood et al, 2007 ).…”

“…This family of petaloid monocots contains many horticulturally important genera, including: Agapanthus, Allium, Amaryllis, Clivia, Galanthus, Hippeastrum, Narcissus, and Nerine ( Heywood et al, 2007 ). Amaryllidoideae, the most diverse subfamily with c. 75 genera ( Meerow, Gardner & Nakamura, 2020 ), has a complex evolutionary history, including hybridisation ( García et al., 2017 ; Marques et al, 2017 ; Meerow, Gardner & Nakamura, 2020 ), and morphological convergence ( Meerow, 2010 ). Arising from our research, in horticulturally important Amaryllidaceae genera ( Könyves et al., 2018 ; Könyves et al., 2019a ; David & Könyves, 2019 ), here we report the sequencing and assembly of five Amaryllidoideae species and compare our assemblies with available Amaryllidaceae plastomes from GenBank.…”

Comparative plastomics of Amaryllidaceae: Inverted repeat expansion and the degradation of the ndh genes in Strumaria truncata Jacq

“…Apart from plant lineages less reliant on photosynthesis, multiple ndh gene losses have also been reported in fully photosynthetic lineages for example in aquatic/semi-aquatic plants (Iles, Smith & Graham, 2013;Peredo, King & Les, 2013;Folk et al, 2020), gymnosperms (Wakasugi et al, 1994;McCoy et al, 2008), Orchidaceae (Kim et al, 2015;Roma et al, 2018), and Cactaceae (Sanderson et al, 2015;Köhler et al, 2020) Amaryllidaceae J. St.-Hil. (Saint-Hilaire, 1805), is a cosmopolitan family of bulbous geophytes and rhizomatous perennials in Asparagales (Meerow, 2000), comprising approximately 90 genera and over 1,700 species (Meerow, Gardner & Nakamura, 2020) in three subfamilies: Amaryllidoideae, Allioideae, and Agapanthoideae, all of which share an umbellate inflorescence. This family of petaloid monocots contains many horticulturally important genera, including: Agapanthus, Allium, Amaryllis, Clivia, Galanthus, Hippeastrum, Narcissus, Nerine (Heywood et al, 2007).…”

“…This family of petaloid monocots contains many horticulturally important genera, including: Agapanthus, Allium, Amaryllis, Clivia, Galanthus, Hippeastrum, Narcissus, Nerine (Heywood et al, 2007). Amaryllidoideae, the most diverse subfamily with c. 75 genera (Meerow, Gardner & Nakamura, 2020), has a complex evolutionary history including hybridisation (García et al, 2017;Marques et al, 2017;Meerow, Gardner & Nakamura, 2020) and morphological convergence (Meerow, 2010). Arising from our research in horticulturally important Amaryllidaceae genera (Könyves et al, 2018(Könyves et al, , 2019aDavid & Könyves, 2019) here we report the sequencing and assembly of five Amaryllidoideae species and compare our assemblies with available Amaryllidaceae plastomes from GenBank.…”

The complete plastome of the South African species, Amaryllis belladonna L. (Amaryllidaceae)

“…(13 genera with 795 species) and Amaryllidoideae (75 genera with ∼900 species; Meerow et al. 2020 ). The family has a cosmopolitan distribution, with centers of diversity for the Amaryllidoideae in the Mediterranean Basin, South Africa, and South America (Rønsted et al.…”