Phylogeographic pattern of Rhizophora (Rhizophoraceae) reveals the importance of both vicariance and long-distance oceanic dispersal to modern mangrove distribution.

BACKGROUND: Mangroves are key components of coastal ecosystems in tropical and subtropical regions worldwide. However, the patterns and mechanisms of modern distribution of mangroves are still not well understood. Historical vicariance and dispersal are two hypothetic biogeographic processes in shaping the patterns of present-day species distributions. Here we investigate evolutionary biogeography of mangroves in the Indo-West Pacific (IWP) and western Atlantic-East Pacific (AEP) regions using a large sample of populations of Rhizophora (the most representative mangrove genus) and a combination of chloroplast and nuclear DNA sequences and genome-wide ISSR markers. RESULTS: Our comparative analyses of biogeographic patterns amongst Rhizophora taxa worldwide support the hypothesis that ancient dispersals along the Tethys Seaway and subsequent vicariant events that divided the IWP and AEP lineages resulted in the major disjunctions. We dated the deep split between the Old and New World lineages to early Eocene based on fossil calibration and geological and tectonic changes. Our data also provide evidence for other vicariant processes within the Indo-West Pacific region in separating conspecific lineages of SE Asia and Australia-Pacific at the Oligocene-Miocene boundary. Close genetic affinities exist between extant Fijian and American lineages; East African and Australian lineages; and Australian and Pacific lineages; indicating relatively more recent oceanic long-distance dispersal events. CONCLUSIONS: Our study demonstrates that neither vicariance nor dispersal alone could explain the observed global occurrences of Rhizophora, but a combination of vicariant events and oceanic long-distance dispersals can account for historical diversification and present-day biogeographic patterns of mangroves.

Expanded phylogenetic and dating analyses of the apples and their relatives (Pyreae, Rosaceae).

Despite previous efforts to elucidate relationships within the Pyreae (Rosaceae), relationships among the major sub-lineages, generic limits, and divergence times have remained uncertain. The present study greatly expands phylogenetic analyses of the Pyreae by using a combination of 11 chloroplast regions plus nuclear ribosomal ITS sequences from 486 individuals representing 331 species and 27 genera. Maximum likelihood and bayesian analyses generally support existing generic boundary, although Sorbus, as previously circumscribed, is clearly non-monophyletic. Two significant conflicts were detected between the chloroplast and ITS phylogenies, suggesting that hybridization played a role in the origins of Micromeles and Pseudocydonia. In addition, we provide estimates of the divergence times of the major lineages. Our findings support the view that the major Pyreae lineages were established during the Eocene-Oligocene period, but that most of the modern diversity did not originate until the Miocene. At least five major, early Old World-New World disjunctions were detected and these vicariance events are generally most consistent with movement through the Beringia.

Genomic markers reveal introgressive hybridization in the Indo-West Pacific mangroves: a case study.

Biodiversity of mangrove ecosystems is difficult to assess, at least partly due to lack of genetic verification of morphology-based documentation of species. Natural hybridization, on the one hand, plays an important role in evolution as a source of novel gene combinations and a mechanism of speciation. However, on the other hand, recurrent introgression allows gene flow between species and could reverse the process of genetic differentiation among populations required for speciation. To understand the dynamic evolutionary consequences of hybridization, this study examines genomic structure of hybrids and parental species at the population level. In the Indo-West Pacific, Bruguiera is one of the dominant mangrove genera and species ranges overlap extensively with one another. Morphological intermediates between sympatric Bruguiera gymnorrhiza and Bruguiera sexangula have been reported as a variety of B. sexangula or a new hybrid species, B. × rhynchopetala. However, the direction of hybridization and extent of introgression are unclear. A large number of species-specific inter-simple sequence repeat (ISSR) markers were found in B. gymnorrhiza and B. sexangula, and the additive ISSR profiling of B. × rhynchopetala ascertained its hybrid status and identified its parental origin. The varying degree of scatterness among hybrid individuals in Principal Coordinate Analysis and results from NewHybrids analysis indicate that B. × rhynchopetala comprises different generations of introgressants in addition to F(1)s. High genetic relatedness between B. × rhynchopetala and B. gymnorrhiza based on nuclear and chloroplast sequences suggests preferential hybrid backcrosses to B. gymnorrhiza. We conclude that B. × rhynchopetala has not evolved into an incipient hybrid species, and its persistence can be explained by recurrent hybridization and introgression. Genomic data provide insights into the hybridization dynamics of mangrove plants. Such information can assist in biodiversity assessment by helping detect novel taxa and/or define species boundaries.

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.

Fine-scale comparisons of genetic variability in seed families of asexually and sexually reproducing Crataegus (hawthorn; Rosaceae).

The reproductive system is one of the key mechanisms that determine genetic diversity at different biological levels. However, few attempts have been made to assess the consequences of asexual reproduction by comparing genetic structure and fecundity of seed families in asexually and sexually reproducing individuals. We have examined two similar hawthorn species, Crataegus crus-galli and C. punctata, that differ in ploidy level and breeding system. Fecundity (per-fruit seed set) and microsatellite genotypes for five loci were determined in 18 and 26 seed families of C. crus-galli and C. punctata (totals of 83 and 118 embryos), respectively. Compared with the sexual diploid C. punctata, tetraploid C. crus-galli shows similar fecundity, but lower genotypic diversity within and between seed families. Reproduction in the tetraploid, while predominantly apomictic, is nevertheless accompanied by outcrossing and selfing. We conclude that in C. crus-galli pollen flow between conspecific individuals is limited, and the combination of pollen fertility, self-compatibility, and pseudogamous apomixis provides reproductive assurance in these tetraploids. Reproductive assurance, in turn, may explain the derived floral architecture seen in most North American tetraploid hawthorns. We also discuss analytical approaches for inferring mating-system parameters in tetraploids and for comparing microsatellite variation across ploidy levels.

Evidence for genetic association between East Asian and western North American Crataegus L. (Rosaceae) and rapid divergence of the eastern North American lineages based on multiple DNA sequences.

Phylogeographic relationships were constructed for 72 Old and New World Crataegus species using combinations of four chloroplast and up to five nuclear regions. Maximum parsimony, maximum likelihood, and Bayesian results yield consistent relationships among major lineages. The close associations of the East Asian and western North American species point toward ancient trans-Beringian migrations. Relationships among eastern North American species are poorly resolved and few groups are identified that are congruent with existing classifications. Scant variation and short internal branches among these species suggest rapid divergence associated with polyploidy and hybridization. Incongruence between the chloroplast and nuclear data, and morphology suggest hybrid origins of three species from an extinct European lineage (the male parent) and three different North American female parents. Europe and eastern North America are suggested as the most recent common areas for Crataegus; at least four dispersal events are inferred to explain the present distribution of the genus.

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.