What explains the high island endemicity of Philippine Rafflesia? A species distribution modeling analysis of three threatened parasitic plant species and their hosts.

PREMISE: Rafflesia are rare holoparasitic plants. In the Philippines, all but one species are found only on single islands. This study aimed to better understand the factors contributing to this distributional pattern. Specifically, we sought to determine whether narrow environmental tolerances of host and/or parasite species might explain their island endemicity. METHODS: We used Maxent species distribution modeling to identify areas with suitable habitat for R. lagascae, R. lobata, and R. speciosa and their Tetrastigma host species. These analyses were carried out for current climate conditions and two future climate change scenarios. RESULTS: Although species distribution models indicated suitable environmental conditions for the Tetrastigma host species in many parts of the Philippines, considerably fewer areas were inferred to have suitable conditions for the three Rafflesia species. Some of these areas are on islands from which they have not been reported. All three species will face significant threats as a result of climate change. CONCLUSIONS: Our results suggest that limited inter-island dispersibility and/or specific environmental requirements are likely responsible for the current pattern of island endemicity of the three Rafflesia species, rather than environmental requirements of their Tetrastigma host species.

Global models and predictions of plant diversity based on advanced machine learning techniques.

Despite the paramount role of plant diversity for ecosystem functioning, biogeochemical cycles, and human welfare, knowledge of its global distribution is still incomplete, hampering basic research and biodiversity conservation. Here, we used machine learning (random forests, extreme gradient boosting, and neural networks) and conventional statistical methods (generalized linear models and generalized additive models) to test environment-related hypotheses of broad-scale vascular plant diversity gradients and to model and predict species richness and phylogenetic richness worldwide. To this end, we used 830 regional plant inventories including c. 300 000 species and predictors of past and present environmental conditions. Machine learning showed a superior performance, explaining up to 80.9% of species richness and 83.3% of phylogenetic richness, illustrating the great potential of such techniques for disentangling complex and interacting associations between the environment and plant diversity. Current climate and environmental heterogeneity emerged as the primary drivers, while past environmental conditions left only small but detectable imprints on plant diversity. Finally, we combined predictions from multiple modeling techniques (ensemble predictions) to reveal global patterns and centers of plant diversity at multiple resolutions down to 7774 km2 . Our predictive maps provide accurate estimates of global plant diversity available at grain sizes relevant for conservation and macroecology.

Global exchange and accumulation of non-native plants.

All around the globe, humans have greatly altered the abiotic and biotic environment with ever-increasing speed. One defining feature of the Anthropocene epoch is the erosion of biogeographical barriers by human-mediated dispersal of species into new regions, where they can naturalize and cause ecological, economic and social damage. So far, no comprehensive analysis of the global accumulation and exchange of alien plant species between continents has been performed, primarily because of a lack of data. Here we bridge this knowledge gap by using a unique global database on the occurrences of naturalized alien plant species in 481 mainland and 362 island regions. In total, 13,168 plant species, corresponding to 3.9% of the extant global vascular flora, or approximately the size of the native European flora, have become naturalized somewhere on the globe as a result of human activity. North America has accumulated the largest number of naturalized species, whereas the Pacific Islands show the fastest increase in species numbers with respect to their land area. Continents in the Northern Hemisphere have been the major donors of naturalized alien species to all other continents. Our results quantify for the first time the extent of plant naturalizations worldwide, and illustrate the urgent need for globally integrated efforts to control, manage and understand the spread of alien species.

A phylogenetic and biogeographic study of Rafflesia (Rafflesiaceae) in the Philippines: Limited dispersal and high island endemism.

Rafflesia (Rafflesiaceae) is a small endo-holoparasitic Asian plant genus known for its exceptionally large flowers, rare species, and high island endemism. In this study, phylogenetic (parsimony and Bayesian inference) and biogeographic (BioGeoBEARS) analyses of DNA sequence data (atp6 and matR genes, and nad1 B-C intron from the mitochondrial genome, and the nuclear ribosomal internal transcribed spacer) were used to reconstruct the phylogenetic relationships among 12 of the 13 known Philippine Rafflesia species and to determine the timing and pathways of their diversification. The results of these analyses confirm those of previous Rafflesia studies (which were largely focused on non-Philippine species) in finding pronounced biogeographic patterns. They suggest that dispersal between islands has been relatively uncommon, and indicate that the high island endemism of Rafflesia is a result of poor inter-island dispersal abilities. The results further suggest that its ancestral range might have been in Borneo, and that its lineages and species evolved earlier and more gradually than previously assumed.

The Global Naturalized Alien Flora (GloNAF) database.

This dataset provides the Global Naturalized Alien Flora (GloNAF) database, version 1.2. GloNAF represents a data compendium on the occurrence and identity of naturalized alien vascular plant taxa across geographic regions (e.g. countries, states, provinces, districts, islands) around the globe. The dataset includes 13,939 taxa and covers 1,029 regions (including 381 islands). The dataset is based on 210 data sources. For each taxon-by-region combination, we provide information on whether the taxon is considered to be naturalized in the specific region (i.e. has established self-sustaining populations in the wild). Non-native taxa are marked as "alien", when it is not clear whether they are naturalized. To facilitate alignment with other plant databases, we provide for each taxon the name as given in the original data source and the standardized taxon and family names used by The Plant List Version 1.1 (http://www.theplantlist.org/). We provide an ESRI shapefile including polygons for each region and information on whether it is an island or a mainland region, the country and the Taxonomic Databases Working Group (TDWG) regions it is part of (TDWG levels 1-4). We also provide several variables that can be used to filter the data according to quality and completeness of alien taxon lists, which vary among the combinations of regions and data sources. A previous version of the GloNAF dataset (version 1.1) has already been used in several studies on, for example, historical spatial flows of taxa between continents and geographical patterns and determinants of naturalization across different taxonomic groups. We intend the updated and expanded GloNAF version presented here to be a global resource useful for studying plant invasions and changes in biodiversity from regional to global scales. We release these data into the public domain under a Creative Commons Zero license waiver (https://creativecommons.org/share-your-work/public-domain/cc0/). When you use the data in your publication, we request that you cite this data paper. If GloNAF is a major part of the data analyzed in your study, you should consider inviting the GloNAF core team (see Metadata S1: Originators in the Overall project description) as collaborators. If you plan to use the GloNAF dataset, we encourage you to contact the GloNAF core team to check whether there have been recent updates of the dataset, and whether similar analyses are already ongoing.

Possible loss of the chloroplast genome in the parasitic flowering plant Rafflesia lagascae (Rafflesiaceae).

Rafflesia is a genus of holoparasitic plants endemic to Southeast Asia that has lost the ability to undertake photosynthesis. With short-read sequencing technology, we assembled a draft sequence of the mitochondrial genome of Rafflesia lagascae Blanco, a species endemic to the Philippine island of Luzon, with ∼350× sequencing depth coverage. Using multiple approaches, however, we were only able to identify small fragments of plastid sequences at low coverage depth (<2×) and could not recover any substantial portion of a chloroplast genome. The gene fragments we identified included photosynthesis and energy production genes (atp, ndh, pet, psa, psb, rbcL), ribosomal RNA genes (rrn16, rrn23), ribosomal protein genes (rps7, rps11, rps16), transfer RNA genes, as well as matK, accD, ycf2, and multiple nongenic regions from the inverted repeats. None of the identified plastid gene sequences had intact reading frames. Phylogenetic analysis suggests that ∼33% of these remnant plastid genes may have been horizontally transferred from the host plant genus Tetrastigma with the rest having ambiguous phylogenetic positions (<50% bootstrap support), except for psaB that was strongly allied with the plastid homolog in Nicotiana. Our inability to identify substantial plastid genome sequences from R. lagascae using multiple approaches--despite success in identifying and developing a draft assembly of the much larger mitochondrial genome--suggests that the parasitic plant genus Rafflesia may be the first plant group for which there is no recognizable plastid genome, or if present is found in cryptic form at very low levels.

Genomic evidence for the parallel evolution of coastal forms in the Senecio lautus complex.

Instances of parallel ecotypic divergence where adaptation to similar conditions repeatedly cause similar phenotypic changes in closely related organisms are useful for studying the role of ecological selection in speciation. Here we used a combination of traditional and next generation genotyping techniques to test for the parallel divergence of plants from the Senecio lautus complex, a phenotypically variable groundsel that has adapted to disparate environments in the South Pacific. Phylogenetic analysis of a broad selection of Senecio species showed that members of the S. lautus complex form a distinct lineage that has diversified recently in Australasia. An inspection of thousands of polymorphisms in the genome of 27 natural populations from the S. lautus complex in Australia revealed a signal of strong genetic structure independent of habitat and phenotype. Additionally, genetic differentiation between populations was correlated with the geographical distance separating them, and the genetic diversity of populations strongly depended on geographical location. Importantly, coastal forms appeared in several independent phylogenetic clades, a pattern that is consistent with the parallel evolution of these forms. Analyses of the patterns of genomic differentiation between populations further revealed that adjacent populations displayed greater genomic heterogeneity than allopatric populations and are differentiated according to variation in soil composition. These results are consistent with a process of parallel ecotypic divergence in face of gene flow.

The genetic ghost of an invasion past: colonization and extinction revealed by historical hybridization in Senecio.

Hybridization is an important evolutionary factor in the diversification of many plant and animal species. Of particular interest is that historical hybridization resulting in the origin of new species or introgressants has occurred between species now geographically separated by great distances. Here, we report that Senecio massaicus, a tetraploid species native to Morocco and the Canary Islands, contains genetic material of two distinct, geographically separated lineages: a Mediterranean lineage and a mainly southern African lineage. A time-calibrated internal transcribed spacer phylogeny indicates that the hybridization event took place up to 6.18 Ma. Because the southern African lineage has never been recorded from Morocco or the Canary Islands, we hypothesize that it reached this area in the distant past, but never became permanently established. Interestingly, the southern African lineage includes S. inaequidens, a highly invasive species that has recently become widespread throughout Europe and was introduced at the end of the 19th century as a 'wool alien'. Our results suggest that this more recent invasion of Europe by S. inaequidens represents the second arrival of this lineage into the region.

Can plant resistance to specialist herbivores be explained by plant chemistry or resource use strategy?

At both a macro- and micro-evolutionary level, selection of and performance on host plants by specialist herbivores are thought to be governed partially by host plant chemistry. Thus far, there is little evidence to suggest that specialists can detect small structural differences in secondary metabolites of their hosts, or that such differences affect host choice or performance of specialists. We tested whether phytochemical differences between closely related plant species are correlated with specialist host choice. We conducted no-choice feeding trials using 17 plant species of three genera of tribe Senecioneae (Jacobaea, Packera, and Senecio; Asteraceae) and a more distantly related species (Cynoglossum officinale; Boraginaceae) containing pyrrolizidine alkaloids (PAs), and four PA-sequestering specialist herbivores of the genus Longitarsus (Chrysomelidae). We also assessed whether variation in feeding by specialist herbivores is attributable to different resource use strategies of the tested plant species. Plant resource use strategy was quantified by measuring leaf dry matter content, which is related to both plant nutritive value and to plant investment in quantitative defences. We found no evidence that intra-generic differences in PA profiles affect feeding by specialist herbivores. Instead, our results indicate that decisions to begin feeding are related to plant resource use strategy, while decisions to continue feeding are not based on any plant characteristics measured in this study. These findings imply that PA composition does not significantly affect host choice by these specialist herbivores. Leaf dry matter content is somewhat phylogenetically conserved, indicating that plants may have difficulty altering resource use strategy in response to selection pressure by herbivores and other environmental factors on an evolutionary time scale.

Frequent gain and loss of pyrrolizidine alkaloids in the evolution of Senecio section Jacobaea (Asteraceae).

Pyrrolizidine alkaloids (PAs) of the macrocyclic senecionine type are secondary metabolites characteristic for most species of the genus Senecio (Asteraceae). These PAs are deterrent and toxic to most vertebrates and insects and provide plants with a chemical defense against herbivores. We studied the PA composition of 24 out of 26 species of Senecio section Jacobaea using GC-MS. The PA profiles of eight of these species have not been studied before and additional PAs were identified for most other species that were included in previous studies. With one exception (senecivernine) all 26 PAs identified in sect. Jacobaea can be regarded as derivatives of the biosynthetic backbone structure senecionine. Based on the PA profiles of the species of sect. Jacobaea and the results of previous tracer studies, we constructed two hypothetical biosynthetic scenarios of senecionine diversification. Both scenarios contain two major reactions: the conversion of the necine base moiety retronecine into the otonecine moiety and site-specific epoxidations within the necic acid moiety. Further reactions are site-specific hydroxylations, sometimes followed by O-acetylations, site-specific dehydrogenations, E, Z-isomerizations, and epoxide hydrolysis and chlorolysis. The GC-MS data and both biosynthetic scenarios were subsequently used to study the evolution of PA formation in sect. Jacobaea by reconstructing the evolutionary history of qualitative PA variation in this section. This was achieved by optimizing additive presence/absence data of PAs and types of enzymatic conversions on a maximum parsimony cladogram of section Jacobaea inferred from DNA sequence and morphological data. Besides showing large intra- and interspecific variation, PA distribution appears to be largely incidental within the whole clade. These results together with the finding that all but one of the PAs identified in sect. Jacobaea are also present in species of other sections of Senecio indicate that differences in PA profiles in Senecio can not be explained by the gain and loss of PA specific genes, but rather by a transient switch-off and switch-on of the expression of genes encoding PA pathway-specific enzymes.

Patterns and causes of incongruence between plastid and nuclear Senecioneae (Asteraceae) phylogenies.

One of the longstanding questions in phylogenetic systematics is how to address incongruence among phylogenies obtained from multiple markers and how to determine the causes. This study presents a detailed analysis of incongruent patterns between plastid and ITS/ETS phylogenies of Tribe Senecioneae (Asteraceae). This approach revealed widespread and strongly supported incongruence, which complicates conclusions about evolutionary relationships at all taxonomic levels. The patterns of incongruence that were resolved suggest that incomplete lineage sorting (ILS) and/or ancient hybridization are the most likely explanations. These phenomena are, however, extremely difficult to distinguish because they may result in similar phylogenetic patterns. We present a novel approach to evaluate whether ILS can be excluded as an explanation for incongruent patterns. This coalescence-based method uses molecular dating estimates of the duration of the putative ILS events to determine if invoking ILS as an explanation for incongruence would require unrealistically high effective population sizes. For four of the incongruent patterns identified within the Senecioneae, this approach indicates that ILS cannot be invoked to explain the observed incongruence. Alternatively, these patterns are more realistically explained by ancient hybridization events.

Tackling speciose genera: species composition and phylogenetic position of Senecio sect. Jacobaea (Asteraceae) based onplastid and nrDNA sequences.

The molecular phylogeny of Senecio sect. Jacobaea (Asteraceae; Senecioneae) was studied to clarify species composition and interspecific relationships of Senecio sect. Jacobaea. This information is necessary for studies seeking explanations of the evolutionary success of Senecio, in terms of high species numbers and the evolution of chemical defense mechanisms. Parsimony analyses with 60 species of the tribe Senecioneae, representing 23 genera and 11 sections of Senecio, based on DNA sequence data of the plastid genome (the trnT-L intergenic spacer, the trnL intron, and two parts of the trnK intron, flanking both sides of the matK gene) and nuclear genome (ITS1, 5.8S, and ITS2 gene and spacers) show that sect. Jacobaea is a strongly supported monophyletic group. Fifteen species have been identified as members of section Jacobaea, including three species that have been consistently ascribed to this section in taxonomic literature and 12 species that were either placed in other sections of Senecio or not exclusively ascribed to sect. Jacobaea. This section was traditionally circumscribed as a group of European, biennial, or perennial herbs with pinnately incised leaves, but the results of this study show that one annual species, a species from northeastern Asia, and a species growing in the Himalayas are members of sect. Jacobaea as well. Furthermore, not all species in the section have pinnately incised leaves. The genera Emilia, Packera, and Pseudogynoxys form the sister clade of sect. Jacobaea, but this relationship lacks strong bootstrap support and thus remains provisional.

Phylogeny reconstruction in the gap between too little and too much divergence: the closest relatives of Senecio jacobaea (Asteraceae) according to DNA sequences and AFLPs.

The species composition and molecular phylogeny of Senecio sect. Jacobaea (Asteraceae; Senecioneae) were studied to identify the closest relatives of Senecio jacobaea. Maximum parsimony and Bayesian inference analyses of DNA sequence data of the plastid (the trnT-L igs, the trnL intron, two parts of the trnK intron, and the psbA-trnH igs) and nuclear genome (ITS1, 5.8S, and ITS2) showed these markers to be suitable to assess the species composition of sect. Jacobaea, identifying 24 species as members of this section. Of these, nine species were not previously assigned to the section. The selected DNA sequence regions, however, showed too little sequence divergence to be optimal for phylogenetic inference within sect. Jacobaea. In contrast, AFLPs proved to be too variable to be used to study relationships between the basal lineages in sect. Jacobaea. Nonetheless, these markers are very useful to study the phylogeny of S. jacobaea and its closest relatives. The combined use of DNA sequence data and AFLPs allowed us to take a major step towards resolving phylogenetic relationships in sect. Jacobaea, identifying Senecio alpinus, Senecio pancicii and Senecio subalpinus (using DNA sequence data) or Senecio chrysanthemoides (using AFLPs) as the closest relatives of S. jacobaea.