Phylogeny ofCrataegus(Rosaceae) based on 257 nuclear loci and chloroplast genomes: evaluating the impact of hybridization

Abstract

Background Hawthorn species (Crataegus L.; Rosaceae tribe Maleae) form a well-defined clade comprising five subgeneric groups readily distinguished using either molecular or morphological data. While multiple subsidiary groups (taxonomic sections, series) are recognized within some subgenera, the number of and relationships among species in these groups are subject to disagreement. Gametophytic apomixis and polyploidy are prevalent in the genus, and disagreement concerns whether and how apomictic genotypes should be recognized taxonomically. Recent studies suggest that many polyploids arise from hybridization between members of different infrageneric groups. Methods We used target capture and high throughput sequencing to obtain nucleotide sequences for 257 nuclear loci and nearly complete chloroplast genomes from a sample of hawthorns representing all five currently recognized subgenera. Our sample is structured to include two examples of intersubgeneric hybrids and their putative diploid and tetraploid parents. We queried the alignment of nuclear loci directly for evidence of hybridization, and compared individual gene trees with each other, and with both the maximum likelihood plastome tree and the nuclear concatenated and multilocus coalescent-based trees. Tree comparisons provided a promising, if challenging (because of the number of comparisons involved) method for visualizing variation in tree topology. We found it useful to deploy comparisons based not only on tree-tree distances but also on a metric of tree-tree concordance that uses extrinsic information about the relatedness of the terminals in comparing tree topologies. Results We obtained well-supported phylogenies from plastome sequences and from a minimum of 244 low copy-number nuclear loci. These are consistent with a previous morphology-based subgeneric classification of the genus. Despite the high heterogeneity of individual gene trees, we corroborate earlier evidence for the importance of hybridization in the evolution of Crataegus. Hybridization between subgenus Americanae and subgenus Sanguineae was documented for the origin of Sanguineae tetraploids, but not for a tetraploid Americanae species. This is also the first application of target capture probes designed with apple genome sequence. We successfully assembled 95% of 257 loci in Crataegus, indicating their potential utility across the genera of the apple tribe.

Niche Shifts, Hybridization, Polyploidy and Geographic Parthenogenesis in Western North American Hawthorns (Crataegus subg. Sanguineae, Rosaceae)

“…Sequence data from plastomes and nuclear loci also support the distinctness of the taxa studied here and their cladistic relationships [4,37,43,121,122]. Although analyses of genetic data are not part of this study, in the context of establishing the extent to which the taxa studied here are genetically differentiated from each other it is worth noting results suggesting the extent to which morphological differentiation is associated with genetic differentiation.…”

“…Only since molecular data demonstrated the probable hybrid origin of western North American black-fruited (allo-) polyploids [4,37,43] has there been a rationale to include members of C. subg. Americanae in morphological comparisons aimed at investigating, in the case of the allopolyploids, their intermediacy with respect to putative parent taxa.…”

“…Americanae; Table 1) [41] that occur in partial sympatry with the Douglasianae and the Salignae (Figure 1A,B) [42]. One or both of these two species are implicated as the pollen parents of the Douglasianae and the Salignae allotetraploids (Table 1) [37,43]. Apart from naturalized C. monogyna Jacq.…”

“…Crataegus), leaving C. brachyacantha nested within a Salignae-Douglasianae clade. Re-rooting this tree using Mesquite 3.10 [115], with C. brachyacantha sister to all the other species as demonstrated by molecular data [4,37,43,103,116], made the Salignae clade sister to the Douglasianae, C. monogyna, and C. mollis. Nevertheless, until recently [44] C. saligna was retained in section Brevispinae with C. brachyacantha [3].…”

Comparative Genomic and Phylogenetic Analysis of Chloroplast Genomes of Hawthorn (Crataegus spp.) in Southwest China

“…In addition, we selected ten diploid species from five Crataegus subgenus, including C. subg. Americanae (C. crus-galli, C. (Phipps et al, 1990;Zarrei et al, 2015;Ufimov and Dickinson, 2020;Liston et al, 2021), and downloaded their intergenic regions sequences from NCBI (atpF-atpH, trnL-trnF, atpB-rbcL, rpl20-rps12 and rpl2-trnH). An outgroup (Amelanchier alnifolia (a)) was also downloaded from NCBI.…”