What explains high plant richness in East Asia? Time and diversification in the tribe Lysimachieae (Primulaceae).

What causes the disparity in biodiversity among regions is a fundamental question in biogeography, ecology, and evolutionary biology. Evolutionary and biogeographic processes (speciation, extinction, dispersal) directly determine species richness patterns, and can be studied using integrative phylogenetic approaches. However, the strikingly high richness of East Asia relative to other Northern Hemisphere regions remains poorly understood from this perspective. Here, for the first time, we test two general hypotheses (older colonization time, faster diversification rate) to explain this pattern, using the plant tribe Lysimachieae (Primulaceae) as a model system. We generated a new time-calibrated phylogeny for Lysimachieae (13 genes, 126 species), to estimate colonization times and diversification rates for each region and to test the relative importance of these two factors for explaining regional richness patterns. We find that neither time nor diversification rates alone explain richness patterns among regions in Lysimachieae. Instead, a new index that combines both factors explains global richness patterns in the group and their high East Asian biodiversity. Based on our results from Lysimachieae, we suggest that the high richness of plants in East Asia may be explained by a combination of older colonization times and faster diversification rates in this region.

On the biogeography of Centipeda: a species-tree diffusion approach.

Reconstructing the biogeographic history of groups present in continuous arid landscapes is challenging due to the difficulties in defining discrete areas for analyses, and even more so when species largely overlap both in terms of geography and habitat preference. In this study, we use a novel approach to estimate ancestral areas for the small plant genus Centipeda. We apply continuous diffusion of geography by a relaxed random walk where each species is sampled from its extant distribution on an empirical distribution of time-calibrated species-trees. Using a distribution of previously published substitution rates of the internal transcribed spacer (ITS) for Asteraceae, we show how the evolution of Centipeda correlates with the temporal increase of aridity in the arid zone since the Pliocene. Geographic estimates of ancestral species show a consistent pattern of speciation of early lineages in the Lake Eyre region, with a division in more northerly and southerly groups since ∼840 ka. Summarizing the geographic slices of species-trees at the time of the latest speciation event (∼20 ka), indicates no presence of the genus in Australia west of the combined desert belt of the Nullabor Plain, the Great Victoria Desert, the Gibson Desert, and the Great Sandy Desert, or beyond the main continental shelf of Australia. The result indicates all western occurrences of the genus to be a result of recent dispersal rather than ancient vicariance. This study contributes to our understanding of the spatiotemporal processes shaping the flora of the arid zone, and offers a significant improvement in inference of ancestral areas for any organismal group distributed where it remains difficult to describe geography in terms of discrete areas.

Species tree phylogeny and character evolution in the genus Centipeda (Asteraceae): evidence from DNA sequences from coding and non-coding loci from the plastid and nuclear genomes.

A species tree phylogeny of the Australian/New Zealand genus Centipeda (Asteraceae) is estimated based on nucleotide sequence data. We analysed sequences of nuclear ribosomal DNA (ETS, ITS) and three plasmid loci (ndhF, psbA-trnH, and trnL-F) using the multi-species coalescent module in BEAST. A total of 129 individuals from all 10 recognised species of Centipeda were sampled throughout the species distribution ranges, including two subspecies. We conclude that the inferred species tree topology largely conform previous assumptions on species relationships. Centipeda racemosa (Snuffweed) is the sister to remaining species, which is also the only consistently perennial representative in the genus. Centipeda pleiocephala (Tall Sneezeweed) and C. nidiformis (Cotton Sneezeweed) constitute a species pair, as does C. borealis and C. minima (Spreading Sneezeweed), all sharing the symplesiomorphic characters of spherical capitulum and convex receptacle with C. racemosa. Another species group comprising C. thespidioides (Desert Sneezeweed), C. cunninghamii (Old man weed, or Common sneeze-weed), C. crateriformis is well-supported but then include the morphologically aberrant C. aotearoana, all sharing the character of having capitula that mature more slowly relative the subtending shoot. Centipeda elatinoides takes on a weakly supported intermediate position between the two mentioned groups, and is difficult to relate to any of the former groups based on morphological characters.

Phylogenetic relationships and generic delimitation in Inuleae subtribe Inulinae (Asteraceae) based on ITS and cpDNA sequence data.

Phylogenetic relationships in Inuleae subtribe Inulinae (Asteraceae) were investigated. DNA sequence data from three chloroplast regions (ndhF, trnL-F and psbA-trnH) and the nuclear ribosomal internal transcribed spacer (ITS) region were analysed separately and in combination using parsimony and Bayesian inference. A total of 163 ingroup taxa were included, of which 60 were sampled for all four markers. Conflicts between chloroplast and nuclear data were assessed using partitioned Bremer support (PBS). Rather than averaging PBS over several trees from constrained searches, individual trees were considered by evaluating PBS ranges. Criteria to be used in the detection of a significant conflict between data partitions are proposed. Three nodes in the total data tree were found to encompass significant conflict that could result from ancient hybridization. Neither of the large, heterogeneous and widespread genera Inula and Pulicaria is monophyletic. A monophyletic group ("the Inula complex") that comprises all species of Inula includes also Telekia, Carpesium, Chrysophthalmum, Rhanteriopsis, Amblyocarpum, and Pentanema sensu stricto. Two species of Pentanema were found to be closer to Blumea (including Blumeopsis and Merrittia) and Caesulia. The monophyletic "Pulicaria complex" includes all taxa with heteromorphic pappus. Within this group, Francoeuria is distinct from Pulicaria and merits recognition as a separate genus. © The Willi Hennig Society 2009.

Phylogeny, character evolution, and classification of Sapotaceae (Ericales).

We present the first cladistic study of the largely tropical family Sapotaceae based on both morphological and molecular data. The data were analyzed with standard parsimony and parsimony jackknife algorithms using equally and successive weighted characters. Sapotaceae are confirmed to constitute two main evolutionary lineages corresponding to the tribes Isonandreae-Mimusopeae-Sideroxyleae and Chrysophylleae-Omphalocarpeae. The Sideroxyleae are monophyletic, Isonandreae are polyphyletic as presently circumscribed, and as suggested by the analyses, the subtribe Mimusopeae-Mimusopinae has evolved within the Mimusopeae-Manilkarinae, which hence is also paraphyletic. Generic limits must be altered within Sideroxyleae with the current members Argania, Nesoluma and Sideroxylon. Argania cannot be maintained at a generic level unless a narrower generic concept is adopted for Sideroxylon. Nesoluma cannot be upheld in a narrow or broad generic concept of Sideroxylon. The large tribe Chrysophylleae circumscribes genera such as Chrysophyllum, Pouteria, Synsepalum, and Xantolis, but the tribe is monophyletic only if the taxa from Omphalocarpeae are also included. Neither Chrysophyllum nor Pouteria are monophyletic in their current definitions. The results indicate that the African taxa of Pouteria are monophyletic and distinguishable from the South American taxa. Resurrection of Planchonella, corresponding to Pouteria section Oligotheca, is proposed. The African genera Synsepalum and Englerophytum form a monophyletic group, but their generic limits are uncertain. Classification of the Asian genus Xantolis is particularly interesting. Morphology alone is indecisive regarding Xantolis relationships, the combined unweighted data of molecules and morphology indicates a sister position to Isonandreae-Mimusopeae-Sideroxyleae, whereas molecular data alone, as well as successive weighted combined data point to a sister position to Chrysophylleae-Omphalocarpeae. An amended subfamily classification is proposed corresponding to the monophyletic groups: Sarcospermatoideae (Sarcosperma), Sapotoideae (Isonandreae-Mimusopeae-Sideroxyleae) and Chrysophylloideae (Chrysophylleae-Omphalocarpeae), where Sapotoideae circumscribes the tribes Sapoteae and Sideroxyleae as well as two or three as yet unnamed lineages. Morphological characters are often highly homoplasious and unambiguous synapomorphies cannot be identified for subfamilies or tribes, which we believe are the reason for the variations seen between different classifications of Sapotaceae.

Corrigendum: Patterns of diversification amongst tropical regions compared: a case study in Sapotaceae.

[This corrects the article on p. 362 in vol. 5, PMID: 25520736.].

Patterns of diversification amongst tropical regions compared: a case study in Sapotaceae.

Species diversity is unequally distributed across the globe, with the greatest concentration occurring in the tropics. Even within the tropics, there are significant differences in the numbers of taxa found in each continental region. Manilkara is a pantropical genus of trees in the Sapotaceae comprising c. 78 species. Its distribution allows for biogeographic investigation and testing of whether rates of diversification differ amongst tropical regions. The age and geographical origin of Manilkara are inferred to determine whether Gondwanan break-up, boreotropical migration or long distance dispersal have shaped its current disjunct distribution. Diversification rates through time are also analyzed to determine whether the timing and tempo of speciation on each continent coincides with geoclimatic events. Bayesian analyses of nuclear (ITS) and plastid (rpl32-trnL, rps16-trnK, and trnS-trnFM) sequences were used to reconstruct a species level phylogeny of Manilkara and related genera in the tribe Mimusopeae. Analyses of the nuclear data using a fossil-calibrated relaxed molecular clock indicate that Manilkara evolved 32-29 million years ago (Mya) in Africa. Lineages within the genus dispersed to the Neotropics 26-18 Mya and to Asia 28-15 Mya. Higher speciation rates are found in the Neotropical Manilkara clade than in either African or Asian clades. Dating of regional diversification correlates with known palaeoclimatic events. In South America, the divergence between Atlantic coastal forest and Amazonian clades coincides with the formation of drier Cerrado and Caatinga habitats between them. In Africa diversification coincides with Tertiary cycles of aridification and uplift of the east African plateaux. In Southeast Asia dispersal may have been limited by the relatively recent emergence of land in New Guinea and islands further east c. 10 Mya.

Phylogenetic analysis of sexual systems in Inuleae (Asteraceae).

From an ancestor with bisexual flowers, plants with unisexual flowers, or even unisexual individuals have evolved in different lineages of angiosperms. The Asteraceae tribe Inuleae includes hermaphroditic, monoecious, dioecious, and gynomonoecious species. Gynomonoecy, the sexual system in which female and bisexual flowers occur on the same plant, is prevalent in the Asteraceae. We inferred one large gene phylogeny (ndhF) and two supertrees to investigate whether gynomonoecy was a stage in the evolution from hermaphroditism to monoecy. We identified transitions in sexual system evolution using the stochastic character mapping method. From gynomonoecious ancestors, both hermaphroditic and monoecious descendants have evolved. Gynomonoecy was not restricted to a stage in the evolution toward monoecy because the number of transitions and the rate of change from monoecy to gynomonoecy were much higher than the opposite. We also investigated one hypothesized association among female flowers and the development of a petaloid ray as an explanation of gynomonoecy maintenance in Asteraceae. We found that peripheral female flowers and petaloid rays were phylogenetically correlated. However, empirical evidence shows that a causal relationship between these traits is not clear.

Relationships of Anagallis foemina and A. arvensis (Myrsinaceae): new insights inferred from DNA sequence data.

We investigated the relationship between Anagallis arvensis and A. foemina using nuclear and plastid molecular data. Information from the nuclear rDNA internal transcribed spacer (ITS) region and four different chloroplast loci; ndhF, trnL-F, rpl16, and rps16 was analysed using both parsimony and Bayesian inference. Anagallis foemina was found to be most closely related to the perennial A. monelli, and not to A. arvensis. The existence of two different cpDNA haplotypes was revealed; one shared by Anagallis foemina, A. monelli, A. platyphylla, and one A. arvensis individual, while all other investigated A. arvensis individuals shared the second haplotype. Ancestral cpDNA polymorphism within Anagallis arvensis or hybridization are possible explanations, however, information in ITS data is too scarce to falsify any of these hypotheses.

Boreotropical migration explains hybridization between geographically distant lineages in the pantropical clade Sideroxyleae (Sapotaceae).

To determine whether the fragmented pantropical distribution of present day Sideroxyleae primarily is the result of long-distance dispersals or represents the remnants of a once continuous distribution in the northern hemisphere, the boreotropical flora, we used phylogenetic analyses of chloroplast and nuclear ribosomal DNA data, Bayesian molecular dating, and Bayesian estimation of ancestral areas. Incongruence between the two data sets was examined with a nuclear low copy gene phylogeny to discover any occurrences of reticulate evolution. The Pacific clade Nesoluma was shown to have two distinct copies of the nuclear low copy gene AAT, one from an African and one from an American ancestral lineage, indicating that it is of allopolyploid origin. We conclude that Sideroxyleae, including the ancestral lineages of Nesoluma, were part of the boreotropical flora and entered the New World via the north Atlantic land bridge. We also suggest that the distribution of extant species resulted from the cooling climate at the end of the Eocene. Sideroxylon oxyacanthum is shown not to belong in the group, but in Chrysophylloideae. A classification reflecting phylogenetic relationships, as well as new combinations for the species in Nesoluma under Sideroxylon, is presented.

Evolution of Lecythidaceae with an emphasis on the circumscription of neotropical genera: information from combined ndhF and trnL-F sequence data.

The Lecythidaceae comprise a pantropical family best known for the edible seeds of the Brazil nut (Bertholletia excelsa) and the cannon-ball tree (Couroupita guianensis), which is planted as a botanical curiosity in subtropical and tropical gardens. In addition, species of the family are often among the most common in neotropical forests, especially in the Amazon Basin. The Brazil nut family is diverse and abundant in the Amazon and is considered to be an indicator of undisturbed or scarcely disturbed lowland forests; thus, what is learned about its evolution, ecology, and biogeography may suggest similar patterns for other Amazonian tree families. We used combined data sets derived from the ndhF and trnL-F genes to elucidate relationships of genera in both the Old and New Worlds that have been associated with Lecythidaceae. Our molecular tree agrees with the recognition of Napoleonaeaceae and Scytopetalaceae. Within the Lecythidaceae, there is molecular support for recognizing three subfamilies: Foetidioideae, Planchonioideae, and Lecythidoideae. We then focused on genera of the Lecythidoideae and found support for recognizing Allantoma (when the actinomorphic-flowered species of Cariniana are included in it), Grias, Gustavia, Corythophora, Couratari, and Couroupita, but conclude that Cariniana, Lecythis, and Eschweilera are not monoyphyletic. Because the position of the monotypic Bertholletia excelsa in relation to the other zygomorphic-flowered genera is not resolved, we are not able to comment on its generic relationships.

Accounting for variation of substitution rates through time in Bayesian phylogeny reconstruction of Sapotoideae (Sapotaceae).

We used Bayesian phylogenetic analysis of 5 kb of chloroplast DNA data from 68 Sapotaceae species to clarify phylogenetic relationships within Sapotoideae, one of the two major clades within Sapotaceae. Variation in substitution rates through time was shown to be a very important aspect of molecular evolution for this data set. Relative rates tests indicated that changes in overall rate have taken place in several lineages during the history of the group and Bayes factors strongly supported a covarion model, which allows the rate of a site to vary over time, over commonly used models that only allow rates to vary across sites. Rate variation over time was actually found to be a more important model component than rate variation across sites. The covarion model was originally developed for coding gene sequences and has so far only been tested for this type of data. The fact that it performed so well with the present data set, consisting mainly of data from noncoding spacer regions, suggests that it deserves a wider consideration in model based phylogenetic inference. Repeatability of phylogenetic results was very difficult to obtain with the more parameter rich models, and analyses with identical settings often supported different topologies. Overparameterization may be the reason why the MCMC did not sample from the posterior distribution in these cases. The problem could, however, be overcome by using less parameter rich evolutionary models, and adjusting the MCMC settings. The phylogenetic results showed that two taxa, previously thought to belong in Sapotoideae, are not part of this group. Eberhardtia aurata is the sister of the two major Sapotaceae clades, Chrysophylloideae and Sapotoideae, and Neohemsleya usambarensis belongs in Chrysophylloideae. Within Sapotoideae two clades, Sideroxyleae and Sapoteae, were strongly supported. Bayesian analysis of the character history of some floral morphological traits showed that the ancestral type of flower in Sapotoideae may have been characterized by floral parts (sepals, petals, stamens, and staminodes) in single whorls of five, entire corolla lobes, and seeds with an adaxial hilum.

Phylogenetic relationships among New Caledonian Sapotaceae (Ericales): molecular evidence for generic polyphyly and repeated dispersal.

The phylogeny of a representative group of genera and species from the Sapotaceae tribe Chrysophylleae, mainly from Australia and New Caledonia, was studied by jackknife analyses of sequences of nuclear ribosomal DNA. The phylogeny conflicts with current opinions on generic delimitation in Sapotaceae. Pouteria and Niemeyera, as presently circumscribed, are both shown to be nonmonophyletic. In contrast, all species currently assigned to these and other segregate genera confined to Australia, New Caledonia, or neighboring islands, form a supported clade. Earlier classifications in which more genera are recognized may better reflect relationships among New Caledonian taxa. Hence, there is need for a revision of generic boundaries in Chrysophylleae, and particularly within the Pouteria complex, including Leptostylis, Niemeyera, Pichonia, Pouteria pro parte (the main part of section Oligotheca), and Pycnandra. Section Oligotheca have been recognized as the separate genus Planchonella, a monophyletic group that needs to be resurrected. Three clades with strong support in our jackknife analysis have one Australian species that is sister to a relatively large group of New Caledonian endemics, suggesting multiple dispersal events between this small and isolated tropical island and Australia. The phylogeny also suggests an interesting case of a relatively recent and rapid radiation of several lineages of Sapotaceae within New Caledonia.

Phylogenetic relationships in the order Ericales s.l.: analyses of molecular data from five genes from the plastid and mitochondrial genomes.

Phylogenetic interrelationships in the enlarged order Ericales were investigated by jackknife analysis of a combination of DNA sequences from the plastid genes rbcL, ndhF, atpB, and the mitochondrial genes atp1 and matR. Several well-supported groups were identified, but neither a combination of all gene sequences nor any one alone fully resolved the relationships between all major clades in Ericales. All investigated families except Theaceae were found to be monophyletic. Four families, Marcgraviaceae, Balsaminaceae, Pellicieraceae, and Tetrameristaceae form a monophyletic group that is the sister of the remaining families. On the next higher level, Fouquieriaceae and Polemoniaceae form a clade that is sister to the majority of families that form a group with eight supported clades between which the interrelationships are unresolved: Theaceae-Ternstroemioideae with Ficalhoa, Sladenia, and Pentaphylacaceae; Theaceae-Theoideae; Ebenaceae and Lissocarpaceae; Symplocaceae; Maesaceae, Theophrastaceae, Primulaceae, and Myrsinaceae; Styracaceae and Diapensiaceae; Lecythidaceae and Sapotaceae; Actinidiaceae, Roridulaceae, Sarraceniaceae, Clethraceae, Cyrillaceae, and Ericaceae.

Phylogenetics of asterids based on 3 coding and 3 non-coding chloroplast DNA markers and the utility of non-coding DNA at higher taxonomic levels.

Asterids comprise 1/4-1/3 of all flowering plants and are classified in 10 orders and >100 families. The phylogeny of asterids is here explored with jackknife parsimony analysis of chloroplast DNA from 132 genera representing 103 families and all higher groups of asterids. Six different markers were used, three of the markers represent protein coding genes, rbcL, ndhF, and matK, and three other represent non-coding DNA; a region including trnL exons and the intron and intergenic spacers between trnT (UGU) to trnF (GAA); another region including trnV exons and intron, trnM and intergenic spacers between trnV (UAC) and atpE, and the rps16 intron. The three non-coding markers proved almost equally useful as the three coding genes in phylogenetic reconstruction at the high level of orders and families in asterids, and in relation to the number of aligned positions the non-coding markers were even more effective. Basal interrelationships among Cornales, Ericales, lamiids (new name replacing euasterids I), and campanulids (new name replacing euasterids II) are resolved with strong support. Family interrelationships are fully or almost fully resolved with medium to strong support in Cornales, Garryales, Gentianales, Solanales, Aquifoliales, Apiales, and Dipsacales. Within the three large orders Ericales, Lamiales, and Asterales, family interrelationships remain partly unclear. The analysis has contributed to reclassification of several families, e.g., Tetrameristaceae, Ebenaceae, Styracaceae, Montiniaceae, Orobanchaceae, and Scrophulariaceae (by inclusion of Pellicieraceae, Lissocarpaceae, Halesiaceae, Kaliphoraceae, Cyclocheilaceae, and Myoporaceae+Buddlejaceae, respectively), and to the placement of families that were unplaced in the APG-system, e.g., Sladeniaceae, Pentaphylacaceae, Plocospermataceae, Cardiopteridaceae, and Adoxaceae (in Ericales, Ericales, Lamiales, Aquifoliales, and Dipsacales, respectively), and Paracryphiaceae among campanulids. Several families of euasterids remain unclassified to order.