Phylogenomics of the andean tetraploid clade of the american amaryllidaceae (sbfamily amaryllidioideae): unlocking a polyploid generic radiation abetted by continental geodynamics

Authors: MEEROW, ALAN - Retired ARS Employee; GARDNER, ELLIOT - Case Western Reserve University (CWRU); Nakamura, Kyoko

Submitted to: Frontiers in Plant Science
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 10/12/2020
Publication Date: 11/5/2020
Citation: Meerow, A.W., Gardner, E., Nakamura, K. 2020. Phylogenomics of the andean tetraploid clade of the american amaryllidaceae (sbfamily amaryllidioideae): unlocking a polyploid generic radiation abetted by continental geodynamics. Frontiers in Plant Science. 11: 582422. https://doi.org/10.3389/fpls.2020.582422.
DOI: https://doi.org/10.3389/fpls.2020.582422

Interpretive Summary: The second large group of the highly ornamental American Amaryllidaceae subfamily Amaryllidoideae constitutes four Andean-centered tribes, most of which have 46 chromosomes. Despite progress in resolving evolutionary relationships of the group with one or two genes, many were poorly resolved or weakly supported in those previous studies. We applied a next generation sequencing technique across 100 species that yielded data from 524 nuclear genes and 2/3 of the chloroplast genome, analyses of which produced fully resolved trees. The four tribes Clinantheae, Eucharideae, Eustephieae (the first branch), and Hymenocallideae (sister to Clinanthus) are resolved in all analyses with 100% support in our tree-of-life for the group. Various family tree building methodologies were largely in concordance; however there was discordance between the trees based on nuclear gene sequences and those from the chloroplast sequences. We determined that this was due to hybridization among species in the genera Clinanthus, Hymenocallis, Stenomesson and between the genera 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 and age estimation analyses suggest an origin in the central Andean region (north and central Peru) for the complex in the mid-Oligocene, with no extinctions in its history. We correlate most of the divergence in the Andean-centered lineages of Amaryllidaceae to the rise of the Andes, directly and indirectly. This is the largest DNA sequence data set to be applied within Amaryllidaceae to date and should help for breeding or marker assisted research in the future.

Technical Abstract: The second large clade 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 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 species tree analyses were run on the gene trees, followed by hybridization network, age diversification and biogeographic analyses. The four tribes Clinantheae, Eucharideae, Eustephieae (the first branch), and Hymenocallideae (sister to Clinanthus) are resolved in all analyses with 100% support. Nuclear gene supermatrix and species tree results were largely in concordance; however cytonuclear discordance was 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 central Andean region (north and central Peru) for the complex in the mid-Oligocene, with more dispersals than vicariances in its history, but no extinctions. 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 the Andes, directly and indirectly, and suggest that the Amotape-Huancabamba Zone functioned as both a corrider (dispersal) and a barrier to migration (vicariance). Several taxonomic changes are made. This is the largest DNA sequence data set to be applied within Amaryllidaceae to date.