Ixora (Rubiaceae) on the Philippines - crossroad or cradle?

BACKGROUND: The Philippine archipelago is globally one of the most important model island systems for studying evolutionary processes. However, most plant species on this archipelago have not yet been studied in sufficient detail. The main aim of this study is to unravel the evolutionary history and biogeographic relationships of the Philippine members of the pantropical genus Ixora. RESULTS: The complex plastid and nuclear divergence patterns in Philippine Ixora, documented using tree and network approaches, reveal a highly dynamic evolution in Ixora, involving several phases of radiation and recolonization. Philippine Ixora comprises at least five lineages, of which one is most closely related to species from Wallacea, and the remaining four to species from Asia. CONCLUSIONS: Our study highlights the importance of Philippine species for understanding phytogeographic patterns in the Indomalayan-Australasian eco-region. The overall genetic differentiation, as well as the incongruence between genealogies based on the biparentally inherited nucleome and the maternally inherited plastome in Ixora, reflect the complex tectonic history of the Philippine archipelago. The Ixora lineage related to Wallacean species supports the delimitation of different ecozones along Huxley's line, because it is absent from Palawan. The remaining four lineages are all allied with Asian taxa, reflecting several waves of colonization. Close relationships between some widespread Philippine species and locally adapted narrow endemics suggest that the widespread, genetically diverse species act as pools for the formation of new species in a process of ongoing speciation. Our results suggest that the species concepts of some of the more widespread taxa need to be revised.

New Caledonian lineages of Psychotria (Rubiaceae) reveal different evolutionary histories and the largest documented plant radiation for the archipelago.

New Caledonia is a remote archipelago of the South-West Pacific, whose flora is rich, distinctive, and disharmonic. The interest of botanists has long been attracted by the spatio-temporal origin of this flora, but little attention has been paid to the modes of colonization and the diversification processes that have led to the archipelago's modern flora. To date, no explosive plant radiation has yet been highlighted for New Caledonia. A dated phylogenetic framework on the second richest New Caledonian genus--Psychotria s.l. and its allied genera (tribes Psychotrieae and Palicoureeae, Rubiaceae; ca. 85 species)--is provided in this study to explore its patterns of colonization and diversification in the archipelago. This study is based on a comprehensive species sampling, two nuclear and four plastid loci. Results show that New Caledonia was colonized four times by Psychotria and its allied genera during the Neogene long after its mid-Eocene re-emergence from the sea. The Pacific clade of Psychotrieae, one of the largest plant diversifications in the Pacific islands and the Indo-Pacific region, is absent from New Caledonia, possibly due to niche competition. Although the four lineages colonized New Caledonia relatively simultaneously during the Neogene, they express different evolutionary histories, as revealed by unevenness in species richness and net diversification rates. The genus Geophila has not diversified on New Caledonia, as a non-endemic single species has been documented in the archipelago. The genus Margaritopsis had a moderate level of diversification (four species) similar to that on other Pacific islands. The Psychotria clade NC1 appears to be a relictual lineage, which probably underwent a drastic extinction, with a narrow ecological habitat and dispersal limitations. The Psychotria clade NC2 is the largest and youngest New Caledonian plant radiation, and has undergone the fastest recorded diversification of any endemic lineage in the archipelago, and could be the result of a 'non-adaptive radiation', originating from Australian rainforests.

Chloroplast genomes of Rubiaceae: Comparative genomics and molecular phylogeny in subfamily Ixoroideae.

In Rubiaceae phylogenetics, the number of markers often proved a limitation with authors failing to provide well-supported trees at tribal and generic levels. A robust phylogeny is a prerequisite to study the evolutionary patterns of traits at different taxonomic levels. Advances in next-generation sequencing technologies have revolutionized biology by providing, at reduced cost, huge amounts of data for an increased number of species. Due to their highly conserved structure, generally recombination-free, and mostly uniparental inheritance, chloroplast DNA sequences have long been used as choice markers for plant phylogeny reconstruction. The main objectives of this study are: 1) to gain insight in chloroplast genome evolution in the Rubiaceae (Ixoroideae) through efficient methodology for de novo assembly of plastid genomes; and, 2) to test the efficiency of mining SNPs in the nuclear genome of Ixoroideae based on the use of a coffee reference genome to produce well-supported nuclear trees. We assembled whole chloroplast genome sequences for 27 species of the Rubiaceae subfamily Ixoroideae using next-generation sequences. Analysis of the plastid genome structure reveals a relatively good conservation of gene content and order. Generally, low variation was observed between taxa in the boundary regions with the exception of the inverted repeat at both the large and short single copy junctions for some taxa. An average of 79% of the SNP determined in the Coffea genus are transferable to Ixoroideae, with variation ranging from 35% to 96%. In general, the plastid and the nuclear genome phylogenies are congruent with each other. They are well-resolved with well-supported branches. Generally, the tribes form well-identified clades but the tribe Sherbournieae is shown to be polyphyletic. The results are discussed relative to the methodology used and the chloroplast genome features in Rubiaceae and compared to previous Rubiaceae phylogenies.

Evolution of Plant Architecture, Functional Diversification and Divergent Evolution in the Genus Atractocarpus (Rubiaceae) for New Caledonia.

The diversification of ecological roles and related adaptations in closely related species within a lineage is one of the most important processes linking plant evolution and ecology. Plant architecture offers a robust framework to study these processes as it can highlight how plant structure influences plant diversification and ecological strategies. We investigated a case of gradual evolution of branching architecture in Atractocarpus spp. (Rubiaceae), forming a monophyletic group in New Caledonia that has diversified rapidly, predominantly in rainforest understory habitats. We used a transdisciplinary approach to depict architectural variations and revealed multiple evolutionary transitions from a branched (Stone's architectural model) to a monocaulous habit (Corner's architectural model), which involved the functional reduction of branches into inflorescences. We propose an integrative functional index that assesses branching incidence on functional traits influencing both assimilation and exploration functions. We showed that architectural transitions correlate with ecologically important functional traits. Variation in ecologically important traits among closely relatives, as supported by the architectural analysis, is suggestive of intense competition that favored divergence among locally coexisting species. We propose that Pleistocene climatic fluctuations causing expansion and contraction of rainforest could also have offered ecological opportunities for colonizers in addition to the process of divergent evolution.

Multiple Assembly Rules Drive the Co-occurrence of Orthopteran and Plant Species in Grasslands: Combining Network, Functional and Phylogenetic Approaches.

Understanding the factors underlying the co-occurrence of multiple species remains a challenge in ecology. Biotic interactions, environmental filtering and neutral processes are among the main mechanisms evoked to explain species co-occurrence. However, they are most often studied separately or even considered as mutually exclusive. This likely hampers a more global understanding of species assembly. Here, we investigate the general hypothesis that the structure of co-occurrence networks results from multiple assembly rules and its potential implications for grassland ecosystems. We surveyed orthopteran and plant communities in 48 permanent grasslands of the French Jura Mountains and gathered functional and phylogenetic data for all species. We constructed a network of plant and orthopteran species co-occurrences and verified whether its structure was modular or nested. We investigated the role of all species in the structure of the network (modularity and nestedness). We also investigated the assembly rules driving the structure of the plant-orthopteran co-occurrence network by using null models on species functional traits, phylogenetic relatedness and environmental conditions. We finally compared our results to abundance-based approaches. We found that the plant-orthopteran co-occurrence network had a modular organization. Community assembly rules differed among modules for plants while interactions with plants best explained the distribution of orthopterans into modules. Few species had a disproportionately high positive contribution to this modular organization and are likely to have a key importance to modulate future changes. The impact of agricultural practices was restricted to some modules (3 out of 5) suggesting that shifts in agricultural practices might not impact the entire plant-orthopteran co-occurrence network. These findings support our hypothesis that multiple assembly rules drive the modular structure of the plant-orthopteran network. This modular structure is likely to play a key role in the response of grassland ecosystems to future changes by limiting the impact of changes in agricultural practices such as intensification to some modules leaving species from other modules poorly impacted. The next step is to understand the importance of this modular structure for the long-term maintenance of grassland ecosystem structure and functions as well as to develop tools to integrate network structure into models to improve their capacity to predict future changes.

Recent changes in mountain grasslands: a vegetation resampling study.

Understanding how land-use changes affect different facets of plant biodiversity in seminatural European grasslands is of particular importance for biodiversity conservation. As conclusions of previous experimental or synchronic observational studies did not converge toward a general agreement, assessing the recent trends in vegetation change in various grassland systems using a diachronic approach is needed. In this resurvey study, we investigated the recent changes in grassland vegetation of the French Jura Mountains, a region with a long tradition of pastoralism. We compared the floristic composition of 150 grassland plots recorded between 1990 and 2000 with new relevés made in 2012 on the same plots. We considered taxonomic, phylogenetic and functional diversity as well as ecological characteristics of the plant communities derived from ecological indicator values and life strategies of the species. PCA of the floristic composition revealed a significant general trend linked to the sampling year. Wilcoxon paired tests showed that contemporary communities were generally more dominated by grass species and presented a higher tolerance to defoliation, a higher pastoral value, and a higher nutrient indicator value. Comparisons revealed a decrease in phylogenetic and functional diversity. By contrast, local species richness has slightly increased. The intensity of change in species composition, measured by Hellinger distance between pairs of relevés, was dependent on neither the time lag between the two surveys, the author of the first relevé nor its location or elevation. The most important changes were observed in grasslands that previously presented low pastoral value, low grass cover, low tolerance to defoliation, and high proportion of stress-tolerant species. This trend was likely linked to the intensification of grassland management reported in the region, with a parallel increase in mowing frequency, grazing pressure, and fertilization level. More restrictive specifications should be applied to agricultural practices to avoid overexploitation of mountain species-rich grasslands and its negative consequences on their biodiversity and resilience.

Phylogeny and classification of the species-rich pantropical showy genus Ixora (Rubiaceae-Ixoreae) with indications of geographical monophyletic units and hybrids.

Species-rich genera often have various conflicting circumscriptions from independent regional flora treatments. Testing the monophyly of these groups of plants is an important step toward the establishment of a phylogenetic classification. The genus Ixora of the tribe Ixoreae in the subfamily Ixoroideae (coffee family or Rubiaceae) is a species-rich pantropical genus of ca. 500 species. Phylogenetic analyses of Ixoreae based on combined sequence data from one nuclear (nrETS) and two chloroplast (rps16 and trnT-F) markers reveal the paraphyly of Ixora as presently delimited and also show that the tribe can be subdivided into three major clades: the Mascarene/neotropical/Malagasy/African clade, the Pacific clade, and the Asian clade. Given the lack of morphological synapomorphies supporting the different Ixora clades and the morphological consistency of the ingroup taxa, we propose a broad circumscription of Ixora including all its satellite genera: Captaincookia, Doricera, Hitoa, Myonima, Sideroxyloides, Thouarsiora, and Versteegia. The current infrageneric classification of Ixora is not supported. The different Ixora subclades represent geographical units. Nuclear and chloroplast tree topologies were partially incongruent, indicating at least four potential natural hybridization events. Other conflicting positions for the cultivated species are most likely due to anthropogenic hybridization.