Abstract
Plant biologists have debated the evolutionary origin of the apple tribe (Maleae; Rosaceae) for over a century. The “wide-hybridization hypothesis” posits that the pome-bearing members of Maleae (base chromosome number x = 17) resulted from a hybridization and/or allopolyploid event between progenitors of other tribes in the subfamily Amygdaloideae with x = 8 and x = 9, respectively. An alternative “spiraeoid hypothesis” proposed that the x = 17 of Maleae arose via the genome doubling of x = 9 ancestors to x = 18, and subsequent aneuploidy resulting in x = 17. We use publicly available genomic data—448 nuclear genes and complete plastomes—from 27 species representing all major tribes within the Amygdaloideae to investigate evolutionary relationships within the subfamily containing the apple tribe. Specifically, we use network analyses and multi-labeled trees to test the competing wide-hybridization and spiraeoid hypotheses. Hybridization occurred between an ancestor of the tribe Spiraeeae (x = 9) and an ancestor of the clade Sorbarieae (x = 9) + Exochordeae (x = 8) + Kerrieae (x = 9), giving rise to the clade Gillenieae (x = 9) + Maleae (x = 17). The ancestor of the Maleae + Gillenieae arose via hybridization between distantly related tribes in the Amygdaloideae (i.e., supporting the wide hybridization hypothesis). However, some evidence supports an aspect of the spiraeoid hypothesis—the ancestors involved in the hybridization event were likely both x = 9, so genome doubling was followed by aneuploidy to result in x = 17 observed in Maleae. By synthesizing existing genomic data with novel analyses, we resolve the nearly century-old mystery regarding the origin of the apple tribe. Our results also indicate that nuclear gene tree-species tree conflict and/or cytonuclear conflict are pervasive at several other nodes in subfamily Amygdaloideae of Rosaceae.
Highlights
Throughout the Rosaceae, there is pervasive conflict between phylogenetic relationships inferred using the nuclear vs. chloroplast genomes
The Exochordeae (Prinsepia utilis Royle. and Oemleria cerasiformis (Torr. & Gray ex Hook. & Arn.) J.W.Landon), Kerrieae [Kerria japonica (L.) DC. and Rhodotypos scandens (Thunb.) Makino], and Sorbarieae [Adenostoma fasciculatum Hook. & Arn. and Sorbaria sorbifolia (L.) A.Braun] formed a clade that is sister to the clade comprised of Gillenieae [Gillenia stipulata (Muhl. ex Willd.) Nutt.] and Maleae [Cydonia oblonga Mill., Sorbus torminalis (L.) Crantz, Malus domestica, Rhaphiolepis indica (L.) Lindl. ex Ker Gawl., Amelanchier alnifolia (Nutt.) Nutt., Vauquelinia californica (Torr.) Sarg., and Kageneckia oblonga Ruiz & Pav.]
We present multiple lines of evidence indicating that an ancestor of the Spiraeeae was likely the maternal participant in an ancient hybridization event and an ancestor of the clade Sorbarieae + Exochordeae + Kerrieae was likely the paternal participant, there was some minor variation in analyses regarding the identity of the paternal parent (Figures 3, 5)
Summary
Throughout the Rosaceae, there is pervasive conflict between phylogenetic relationships inferred using the nuclear vs. chloroplast genomes. Many lineages of the Rosaceae contain economically important species; the Maleae, with over 1,000 species, includes commercially important fruit crops, such as apples and pears, as well as many ornamentals. Nuclear data indicate that the Dryadoideae are sister to the Amygdaloideae + Rosoideae (Xiang et al, 2017), whereas phylogenetic relationships reconstructed using plastome data have still not conclusively resolved the branching order. In the Amygdaloideae, the relationships between many tribes conflict when the nuclear and chloroplast topologies are compared (Figure 1; Xiang et al, 2017; Zhang et al, 2017). Within the Rosaceae, many relationships between tribes were inconsistent between the nuclear and chloroplast genomes, such as the placement of all tribes within the Rosoideae except for Ulmarieae (Xiang et al, 2017; Zhang et al, 2017). Cytonuclear conflict exists within the Rosaceae at shallower systematic scales (e.g., within the tribe Maleae; Liu et al, 2019, 2020a,b, 2021)
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