Timothy A. Dickinson

Phylogeny and classification of Rosaceae

Phylogenetic relationships among 88 genera of Rosaceae were investigated using nucleotide sequence data from six nuclear (18S, gbssi1, gbssi2, ITS, pgip, and ppo) and four chloroplast (matK, ndhF, rbcL, and trnL-trnF) regions, separately and in various combinations, with parsimony and likelihood-based Bayesian approaches. The results were used to examine evolution of non-molecular characters and to develop a new phylogenetically based infrafamilial classification. As in previous molecular phylogenetic analyses of the family, we found strong support for monophyly of groups corresponding closely to many previously recognized tribes and subfamilies, but no previous classification was entirely supported, and relationships among the strongly supported clades were weakly resolved and/or conflicted between some data sets. We recognize three subfamilies in Rosaceae: Rosoideae, including Filipendula, Rubus, Rosa, and three tribes; Dryadoideae, comprising the four actinorhizal genera; and Spiraeoideae, comprising Lyonothamnus and seven tribes. All genera previously assigned to Amygdaloideae and Maloideae are included in Spiraeoideae. Three supertribes, one in Rosoideae and two in Spiraeoideae, are recognized.

Phylogeny of subtribe Pyrinae (formerly the Maloideae, Rosaceae): Limited resolution of a complex evolutionary history

Generic relationships in the Pyrinae (equivalent to subfamily Maloideae) were assessed with six chloroplast regions and five nuclear regions. We also plotted 12 non-molecular characters onto molecular phylogenies. Chloroplast DNA trees are incongruent with those from nuclear regions, as are most nuclear regions with one another. Some of this conflict may be the result of hybridization, which occurs between many genera of Pyrinae in the present and may have occurred in the past, and duplication of nuclear loci. Sequence divergence between genera of Pyrinae, which is significantly less than that between genera of another large clade in Rosaceae, the Rosoideae, is concentrated in terminal branches, with short internal branches. This pattern is consistent with an ancient, rapid radiation, which has also been hypothesized from the fossil record. Even with about 500,000 bp of sequence, our results resolve only several small groups of genera and leave much uncertainty about phylogenetic relationships within Pyrinae.

A review of the chemistry of the genus Crataegus.

Since the 1800s, natural health products that contain hawthorn (Crataegus spp.) have been used in North America for the treatment of heart problems such as hypertension, angina, arrhythmia, and congestive heart failure. Traditionally, Native American tribes used hawthorn (Crataegus spp.) to treat gastrointestinal ailments and heart problems, and consumed the fruit as food. Hawthorn also has a long history of use in Europe and China for food, and in traditional medicine. Investigations of Crataegus spp. typically focus on the identification and quantification of flavonoids and anthocyanins, which have been shown to have pharmacological activity. The main flavonoids found in Crataegus spp. are hyperoside, vitexin, and additional glycosylated derivatives of these compounds. Reviewed herein are the botany, ethnobotany, and traditional use of hawthorn while focusing on the phytochemicals that have been reported in Crataegus species, and the variation in the described chemistry between individual species.

Polyploidy, reproductive biology, and Rosaceae: understanding evolution and making classifications

The relationship between polyploidy and breeding system is of critical importance for understanding evolution and improving the taxonomy of large Rosaceous genera. Reviewing the data available for the family and for tribe Pyreae (formerly subfamily Maloideae) in particular, it appears that hybridization, pseudogamous gametophytic apomixis, polyploidy, and self-compatibility are closely linked. Studies of the evolutionary significance of any one or two of these factors need to consider the others as well. Taxonomic decisions likewise need to be informed by knowledge of how these factors affect patterns of phenetic and genetic variation.

Population genetic structure of diploid sexual and polyploid apomictic hawthorns (Crataegus; Rosaceae) in the Pacific Northwest

Polyploidy and gametophytic apomixis are two important and associated processes in plants. Many hawthorn species are polyploids and can reproduce both sexually and apomictically. However, the population genetic structure of these species is poorly understood. Crataegus douglasii is represented exclusively by self‐compatible tetraploid pseudogamous apomicts across North America, whereas Crataegus suksdorfii found in the Pacific Northwest is known to include self‐incompatible diploid sexuals as well as polyploid apomicts. We compare population structure and genetic variability in these two closely related taxa using microsatellite and chloroplast sequence markers. Using 13 microsatellite loci located on four linkage groups, 251 alleles were detected in 239 individuals sampled from 15 localities. Within‐population multilocus genotypic variation and molecular diversity are greatest in diploid sexuals and lowest in triploid apomicts. Apart from the isolation of eastern North American populations of C. douglasii, there is little evidence of isolation by distance in this taxon. Genetic diversity in western populations of C. douglasii suggests that gene flow is frequent, and that colonization and establishment are often successful. In contrast, local populations of C. suksdorfii are more markedly differentiated. Gene flow appears to be limited primarily by distance in diploids and by apomixis and self‐compatibility in polyploids. We infer that apomixis and reproductive barriers between cytotypes are factors that reduce the frequency of gene flow among populations, and may ultimately lead to allopatric speciation in C. suksdorfii. Our findings shed light on evolution in woody plants that show heterogeneous ploidy levels and reproductive systems.

Polyploidy and Diversification: A Phylogenetic Investigation in Rosaceae

Polyploidy has been described both as an evolutionary dead end and as a major engine of diversification for angiosperms. Two recent studies have found that genera with higher proportions of polyploid species are more species rich. Here, we investigate patterns of diversification and polyploidy by performing traditional and phylogenetically corrected analyses within the Rosaceae. We find that polyploidy is associated with increased species richness and then differentiate between three alternative hypotheses for this pattern: (1) that polyploidy is associated with herbaceous growth habit, a trait that is in turn associated with increased species richness; (2) that polyploid clades are more evolutionarily successful (i.e., experience increased speciation and/or fewer extinction events) than diploid clades, perhaps because of the increase in genomic content or the increase in plant/flower size that often accompanies polyploidization; and (3) that the polyploidization events themselves, along with the reproductive isolation from the parental clade(s) that follows polyploidization, are responsible for the increased species richness observed in clades with a high proportion of polyploids. There is no evidence that polyploidy and herbaceous growth habit were correlated or that polyploid clades are more species rich than their diploid sister groups. We posit that the third hypothesis has the greatest potential for explaining the pattern of higher species richness of polyploid clades.

Reproductive Biology in Subfam. Maloideae (Rosaceae)

Maloids are versatile in reproductive mode-vegetative spreading, self-incompati- bility, self-compatibility, and apomixis all occur-and they engage in extensive hybridization and polyploidy. Naturally occurring gametophytic apomixis has been reported from almost 100 taxa in six genera-Aronia, Amelanchier, Cotoneaster, Crataegus, Malus, and Sorbus s.l. Generally in maloids apomixis is facultative, aposporous, pseudogamous, and characterized by a distinctive multiplicity of megagametophytes per ovule. Unlike their sexual relatives apomicts are almost always triploid or tetraploid and self-compatible. Maloid polyploids that have been studied express some apomixis. Reported evidence for apomixis includes ploidy level and mode of development of megagameto- phytes, presence of multiple megagametophytes in one ovule, polyembryony, progeny of maternal phenotype, complete pollen sterility, and seed set in the absence of pollination. Crosses between apomictic and sexual taxa yield apomictic offspring in most cases, indicating, along with other studies, that apomixis is genetically dominant over sexuality in the Maloideae. Hybridization at generic and specific levels is remarkably frequent. Smaller genera tend to be diploid; larger genera also contain triploids and tetraploids; and higher ploidy levels and aneuploidy are rare. Hybrid- ization, often coupled with polyploidy and uniparental reproduction, leads to new, more or less reproductively isolated forms in the Maloideae.

Molecular Reappraisal of Relationships Between Crataegus and Mespilus (Rosaceae, Pyreae)—Two Genera or One?

Abstract Mespilus and Crataegus are sister genera in Rosaceae tribe Pyreae. Mespilus has been seen to comprise not only the medlar, Mespilus germanica, of western Eurasia but also the Arkansas, U.S.A. endemic, Mespilus canescens. Crataegus, on the other hand, consists of 140–200 species found throughout the northern hemisphere. Diagnoses of these two genera rely on morphological features of leaves, flowers and fruits. However, character states supposed to be diagnostic of Mespilus occur in species of Crataegus. We used two nuclear (ribosomal ITS and LEAFY intron2) and four intergenic chloroplast DNA regions (trnS-trnG, psbA-trnH, trnH-rpl2, and rpl20-rps12) to estimate the phylogeny of Mespilus and Crataegus. Maximum parsimony, maximum likelihood, and Bayesian analyses all corroborate the sister group relationship between Crataegus and Mespilus, and Crataegus brachyacantha sister to the rest of Crataegus. However, incongruence between chloroplast and nuclear data supports the hypothesis of a hybrid origin for Mespilus canescens, with Crataegus brachyacantha or its ancestor as the maternal parent. Accordingly, we (1) restrict Crataegus section Brevispinae to Crataegus brachyacantha (2) distinguish the Arkansas endemic as a nothospecies; (3) describe a new section and a new nothosection within Crataegus to contain the former species of Mespilus and Crataemespilus; and (4) make two new combinations under Crataegus.

Reconstructing reticulation history in a phylogenetic framework and the potential of allopatric speciation driven by polyploidy in an agamic complex in Crataegus (Rosaceae).

Polyploidy plays a prominent role in the speciation process in plants. Many species are known to be part of agamic complexes comprising sexual diploids and more or less exclusively asexual polyploids. However, polyploid formation has been studied in very few cases, primarily because of the challenges in examining these cases phylogenetically. In this study, we demonstrate the use of a variety of phylogenetic approaches to unravel origins and infer reticulation history in a diploid–polyploid complex of black‐fruited Crataegus. The tree approaches are shown to be useful in testing alternative hypotheses and in revealing genealogies of nuclear genes, particularly in polyploid organisms that may contain multiple copies. Compared to trees, network approaches provide a better indication of reticulate relationships among recently diverged taxa. Taken together, our data point to both the autopolyploid and allopolyploid origins of triploids in natural populations of Crataegus suksdorfii, whereas tetraploids are formed via a triploid bridge, involving the backcross of allotriploid offspring with their diploid C. suksdorfii parent, followed by gene introgression from sympatric C. douglasii. Our findings provide empirical evidence for different pathways of polyploid formation that are all likely to occur within natural populations and the allopatric establishment of neopolyploids subsequent to their formation.

Population Structure and Reproductive Ecology in the Maloideae (Rosaceae)

The available data suggest that the population structure of maloid species may be affected dramatically by features of their breeding system, and by their reproductive ecology in general. Morphometric data from Amelanchier, Crataegus, and Sorbus demonstrate associations be- tween the occurrence of uniparental reproduction (apomixis and selfing) and polyploidy with topodeme phenotypic variability. These associations appear to be modified by factors such as fe- cundity, propagule size, and differences in shade tolerance between and within genera. Uniparental reproduction, abundant seed production, and the short time available in which to colonize recently disturbed sites decrease the number of genotypes in maloid topodemes. At present, however, genetic data with which to test this assertion are lacking. Rigorous evaluation is necessary in view of the possibility that much of the taxonomic complexity of genera such as Amelanchier, Crataegus, and Sorbus is due at least in part to naive assumptions about population structure in these genera on the part of earlier taxonomists. Their ignorance of the roles played by hybridization, uniparental reproduction, and polyploidy may have led them to recognize as species individual genotypes.