Metapopulation Vicariance, Age of Island Taxa and Dispersal: A Case Study Using the Pacific Plant Genus Planchonella (Sapotaceae).

Oceanic islands originate from volcanism or tectonic activity without connections to continental landmasses, are colonized by organisms, and eventually vanish due to erosion and subsidence. Colonization of oceanic islands occurs through long-distance dispersals (LDDs) or metapopulation vicariance, the latter resulting in lineages being older than the islands they inhabit. If metapopulation vicariance is valid, island ages cannot be reliably used to provide maximum age constraints for molecular dating. We explore the relationships between the ages of members of a widespread plant genus (Planchonella, Sapotaceae) and their host islands across the Pacific to test various assumptions of dispersal and metapopulation vicariance. We sampled three nuclear DNA markers from 156 accessions representing some 100 Sapotaceae taxa, and analyzed these in BEAST with a relaxed clock to estimate divergence times and with a phylogeographic diffusion model to estimate range expansions over time. The phylogeny was calibrated with a secondary point (the root) and fossils from New Zealand. The dated phylogeny reveals that the ages of Planchonella species are, in most cases, consistent with the ages of the islands they inhabit. Planchonella is inferred to have originated in the Sahul Shelf region, to which it back-dispersed multiple times. Fiji has been an important source for range expansion in the Pacific for the past 23 myr. Our analyses reject metapopulation vicariance in all cases tested, including between oceanic islands, evolution of an endemic Fiji-Vanuatu flora, and westward rollback vicariance between Vanuatu and the Loyalty Islands. Repeated dispersal is the only mechanism able to explain the empirical data. The longest (8900 km) identified dispersal is between Palau in the Pacific and the Seychelles in the Indian Ocean, estimated at 2.2 Ma (0.4-4.8 Ma). The first split in a Hawaiian lineage (P. sandwicensis) matches the age of Necker Island (11.0 Ma), when its ancestor diverged into two species that are distinguished by purple and yellow fruits. Subsequent establishment across the Hawaiian archipelago supports, in part, progression rule colonization. In summary, we found no explanatory power in metapopulation vicariance and conclude that Planchonella has expanded its range across the Pacific by LDD. We contend that this will be seen in many other groups when analyzed in detail.

Species tree phylogeny and biogeography of the Neotropical genus Pradosia (Sapotaceae, Chrysophylloideae).

Recent phylogenetic studies in Sapotaceae have demonstrated that many genera need to be redefined to better correspond to natural groups. The Neotropical genus Pradosia is believed to be monophyletic and includes 26 recognized species. Here we reconstruct the generic phylogeny by a species-tree approach using (∗)BEAST, 21 recognized species (36 accessions), sequence data from three nuclear markers (ITS, ETS, and RPB2), a relaxed lognormal clock model, and a fossil calibration. We explore the evolution of five selected morphological characters, reconstruct the evolution of habitat (white-sand vs. clayish soils) preference, as well as space and time by using a recently developed continuous diffusion model in biogeography. We find Pradosia to be monophyletic in its current circumscription and to have originated in the Amazon basin at ∼47.5Ma. Selected morphological characters are useful to readily distinguish three clades. Preferences to white-sand and/or clay are somewhat important for the majority of species, but speciation has not been powered by habitat shifts. Pradosia brevipes is a relative young species (∼1.3Ma) that has evolved a unique geoxylic life strategy within Pradosia and is restricted to savannahs. Molecular dating and phylogenetic pattern indicate that Pradosia reached the Brazilian Atlantic coast at least three times: at 34.4Ma (P. longipedicellata), at 11.7Ma (P. kuhlmannii), and at 3.9Ma (weakly supported node within the red-flowered clade).

Phylogeny and generic limits in the Niemeyera complex of New Caledonian Sapotaceae: evidence of multiple origins of the anisomerous flower.

Traditional generic limits within the "Niemeyera complex" (Sapotaceae: Chrysophylloideae) in Australia and New Caledonia do not correspond to natural groups. We analyzed nuclear (ETS, ITS) and chloroplast (trnH-psbA, trnS-G) sequence data, and 42 morphological characters, using a near-complete taxon sampling. The resulting phylogeny provides a new generic framework where Leptostylis and Sebertia are monophyletic, Niemeyera is recognized as a small genus confined to Australia, and the circumscriptions of Achradotypus and Pycnandra require significant modification. This framework allows about 20 recently discovered species to be described in appropriate genera and assessed for their conservation status. Evolutionary changes in two widely used characters, anisomerous flowers and the number of stamens inserted opposite each corolla lobe, have occurred multiple times. There is no evidence that anisomery originated through hybridization as suggested in other groups. Instead, the two characters are closely coupled and often mutually exclusive. The diagnostic value of morphological characters varies considerably; for example, the presence, absence, and type of malpighiaceous hairs convey more phylogenetic information than many traditionally used features. Criteria and options for a new generic classification are discussed, and a reconstruction of the hypothesized ancestor that likely colonized New Caledonia in the Oligocene is presented.

Multi-gene phylogeny of the pantropical subfamily Chrysophylloideae (Sapotaceae): evidence of generic polyphyly and extensive morphological homoplasy.

We present a molecular phylogeny of 26 out of the 28 currently accepted genera in the subfamily Chrysophylloideae (Sapotaceae) using parsimony, parsimony jackknifing, and Bayesian inference. A data matrix of 8984 characters was obtained from DNA sequences of seven chloroplast loci, two nuclear loci, indels coded as binary characters, and morphology. Our phylogenetic reconstruction suggests that Chrysophyllum, Pouteria, and Pradosia, as well as some sections within Chrysophyllum and Pouteria, are all polyphyletic. These taxa were previously described largely on the basis of unique combinations of states for a set of morphological characters. Mapping some of these characters onto one of the most parsimonious trees indicates that the symplesiomorphic flower in the subfamily was probably 5-merous, had stamens inserted in the tube orifice, staminodes, seeds with foliaceous cotyledons, exserted radicle, and endosperm. These characters have subsequently been lost multiple times and cannot be used as synapomorphies to support broad generic concepts. Despite the high degree of homoplasy some well-defined clades can be described on the basis of alternative character state combinations. Also, many of these well-supported clades appear to be restricted to particular geographical areas (e.g. all taxa in Australasia form a monophyletic group). Hence, we suggest that the segregate genera Aningeria, Malacantha, and Martiusella may ultimately be resurrected, and probably also Donella and Gambeya, but their circumscriptions are still unclear. One species, Chrysophyllum cuneifolium, may have originated from a hybridization event between continents where the maternal genome (cpDNA) comes from South America and the nuclear genome comes from Africa. © The Willi Hennig Society 2008.

Phylogeny, diagnostic characters and generic limitation of Australasian Chrysophylloideae (Sapotaceae, Ericales): evidence from ITS sequence data and morphology.

Current generic limits in Chrysophylloideae (Sapotaceae) from Australia, New Caledonia and the Pacific islands have been shown not to correspond to monophyletic groups. In particular, revisions of generic boundaries are necessary for Pouteria and Niemeyera. We present the first cladistic study of a large representative sample from these areas based on (i) nuclear ribosomal DNA (nrDNA) sequence data, and (ii) combined data of nrDNA and morphology. The data were analyzed with parsimony jackknifing using equal weights and gaps coded as binary characters. Our results from the two data sets are highly congruent and morphological data often increase support as well as tree resolution. A basal polytomy prevents hypotheses of intergeneric relationships, but several groups receive strong support, and hence, four segregates of Pouteria (Beccariella, Planchonella, Sersalisia and Van-royena) are resurrected. Four others, Albertisiella, Bureavella, Iteiluma and Pyriluma are rejected. Niemeyera is redefined as a small genus confined to Australia. Generic limits within the sister group to Niemeyera are still unclear, a group that includes Leptostylis and Pycnandra. Furthermore, Van-royena may have originated from an intergeneric hybridization event. Traditionally used and newly identified morphological characters are scrutinized for their diagnostic value. For instance, the position of stamen insertion within the corolla tube is a strong indication of generic relationship. Unique synapomorphies are rare and genera must be distinguished on character state combinations. Following the results, several taxonomic combinations are necessary (Beccariella brownlessiana, B. macrocarpa, B. singuliflora, B. vieillardii, Pichonia daenikeri, Planchonella asterocarpon, P. dothioense, P. myrsinifolia, P. myrsinodendron and P. xylocarpa).

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.

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.

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.