Rapid in situ diversification rates in Rhamnaceae explain the parallel evolution of high diversity in temperate biomes from global to local scales.

The macroevolutionary processes that have shaped biodiversity across the temperate realm remain poorly understood and may have resulted from evolutionary dynamics related to diversification rates, dispersal rates, and colonization times, closely coupled with Cenozoic climate change. We integrated phylogenomic, environmental ordination, and macroevolutionary analyses for the cosmopolitan angiosperm family Rhamnaceae to disentangle the evolutionary processes that have contributed to high species diversity within and across temperate biomes. Our results show independent colonization of environmentally similar but geographically separated temperate regions mainly during the Oligocene, consistent with the global expansion of temperate biomes. High global, regional, and local temperate diversity was the result of high in situ diversification rates, rather than high immigration rates or accumulation time, except for Southern China, which was colonized much earlier than the other regions. The relatively common lineage dispersals out of temperate hotspots highlight strong source-sink dynamics across the cosmopolitan distribution of Rhamnaceae. The proliferation of temperate environments since the Oligocene may have provided the ecological opportunity for rapid in situ diversification of Rhamnaceae across the temperate realm. Our study illustrates the importance of high in situ diversification rates for the establishment of modern temperate biomes and biodiversity hotspots across spatial scales.

Dispersal from Africa to the Neotropics was followed by multiple transitions across Neotropical biomes facilitated by frugivores.

BACKGROUND AND AIM: Plant disjunctions have fascinated biogeographers and ecologists for a long time. We use tribe Bocageeae (Annonaceae), a predominantly Neotropical plant group distributed across several present-day Neotropical biomes and with an African-American disjunction, to investigate long-distance dispersal mediated by frugivorous animals at both intercontinental and intracontinental scales. METHODS: We reconstructed a species-level phylogeny of tribe Bocageeae with a dataset composed of 116 nuclear markers. We sampled 70% of Bocageeae species, covering its geographic range and representing all eight genera. We estimated divergence times using BEAST, inferred ancestral range distributions and reconstructed ancestral states for fruit traits related to long-distance dispersal in a Bayesian framework. KEY RESULTS: The ancestral Bocageeae date to the Early Eocene and were inferred to occur in Africa and proto-Amazonia. Its ancestral fruits were large and dehiscent. The first lineage split gave rise to an exclusively Neotropical clade during the Middle Eocene, in proto-Amazonia. Range exchange between the Amazon and the Atlantic Forest occurred at least once during the Miocene, and from Amazonia to Central America and Mexico, during the Early Miocene. Transitions in different sets of fruit morphologies were inferred to be related to dispersal events across South American regions/biomes. CONCLUSIONS: In Bocageeae mammals may have been responsible for long-distance dispersal through the Boreotropics. In the Neotropics, proto-Amazonia is proposed to be the source for dispersal to other tropical American biomes. Long-distance dispersal may have happened via a wide range of dispersal guilds, depending on frugivore radiations, diversity, and abundance at particular time periods and places. Hence, inter- and intracontinental dispersal may not rely on a single dispersal syndrome or guild, but more on the availability of frugivorous lineages for seed dispersal.

Desmopsisterriflora, an extraordinary new species of Annonaceae with flagelliflory.

Flagelliflory refers to the production of inflorescences exclusively on long, whip-like branches which emerge from the main trunk and extend along the ground or below it. It is the rarest type of cauliflory and only a few cases have been reported in the world. Here, a new species of Annonaceae with flagelliflory is described and illustrated. The phylogenetic relationships of the new species were inferred using a hybrid-capture phylogenomic approach and we present some notes on its reproductive ecology and pollen characteristics. The new species, namely Desmopsisterriflorasp. nov., is part of a clade composed of Mexican species of Stenanona with long, awned petals. Desmopsisterriflora is distinguished by its flageliflorous inflorescences, basely fused sepals, thick red petals, reduced number of ovules per carpel, pollen grains with a weakly rugulate to fossulate exine ornamentation, and its globose, apiculate fruits with a woody testa. The morphological characteristics of the flagella suggest that these are specialized branches rather than inflorescences, and the absence of ramiflory implies an exclusively reproductive function. The flowers are infrequently visited by insects, their potential pollinators being flies and ants.

Phylogenomics and continental biogeographic disjunctions: insight from the Australian starflowers (Calytrix).

PREMISE: Continental-scale disjunctions and associated drivers are core research interests in biogeographic studies. Here, we selected a species-rich Australian plant genus (Calytrix; Myrtaceae) as a case study to investigate these patterns. Species of this endemic Australian starflower genus have a disjunct distribution across the mesic fringes of the continent and are largely absent from the arid center. METHODS: We used high-throughput sequencing to generate unprecedented resolution and near complete species-level nuclear and plastid phylogenies for Calytrix. BioGeoBEARS and biogeographic stochastic mapping were used to infer ancestral areas, the relative contributions of vicariance and dispersal events, and directionality of dispersal. RESULTS: Present-day disjunctions in Calytrix are explained by a combination of scenarios: (1) retreat of multiple lineages from the continental center to the more mesic fringes as Australia became progressively more arid, with subsequent extinction in the center as well as (2) origination of ancestral lineages in southwestern Australia (SWA) for species-rich clades. The SWA biodiversity hotspot is a major diversification center and the most common source area of dispersals, with multiple lineages originating in SWA and subsequently spreading to the adjacent arid Eremaean region. CONCLUSIONS: Our results suggest that major extinction, as a result of cooling and drying of the Australian continent in the Eocene-Miocene, shaped the present-day biogeography of Calytrix. We hypothesize that this peripheral vicariance pattern, which is similar to the African Rand flora, may explain the disjunctions of many other Australian plant groups. Further studies with densely sampled phylogenies are required to test this hypothesis.

Historical biogeography of Pomaderris (Rhamnaceae): Continental vicariance in Australia and repeated independent dispersals to New Zealand.

AIM: Gondwanan biogeographic patterns include a combination of old vicariance events following the breakup of the supercontinent, and more recent long-distance dispersals across the southern landmasses. Floristic relationships between Australia and New Zealand have mostly been attributed to recent dispersal events rather than vicariance. We assessed the biogeographic history of Pomaderris (Rhamnaceae), which occurs in both Australia and New Zealand, by constructing a time-calibrated molecular phylogeny to infer (1) phylogenetic relationships and (2) the relative contributions of vicariance and dispersal events in the biogeographic history of the genus. LOCATION: Australia and New Zealand. METHODS: Using hybrid capture and high throughput sequencing, we generated nuclear and plastid data sets to estimate phylogenetic relationships and fossil calibrated divergence time estimates for Pomaderris. BioGeoBEARS and biogeographical stochastic mapping (BSM) were used to assess the ancestral area of the genus and the relative contributions of vicariance vs dispersal, and the directionality of dispersal events. RESULTS: Our analyses indicate that Pomaderris originated in the Oligocene and had a widespread Australian distribution. Vicariance of western and eastern Australian clades coincides with the uplift of the Nullarbor Plain c. 14 Ma, followed by subsequent in-situ and within-biome diversification with little exchange across regions. A rapid radiation of southeastern Australian taxa beginning c. 10 Ma was the source for at least six independent long-distance dispersal events to New Zealand during the Pliocene-Pleistocene. MAIN CONCLUSIONS: Our study demonstrates the importance of dispersal in explaining not only the current cross-Tasman distributions of Pomaderris, but for the New Zealand flora more broadly. The pattern of multiple independent long-distance dispersal events for Pomaderris, without significant radiation within New Zealand, is congruent with other lowland plant groups, suggesting that this biome has a different evolutionary history compared with the younger alpine flora of New Zealand, which exhibits extensive radiations often following single long distance dispersal events.

Extinction pulse at Eocene-Oligocene boundary drives diversification dynamics of two Australian temperate floras.

The diversification dynamics of the Australian temperate flora remains poorly understood. Here, we investigate whether differences in plant richness in the southwest Australian (SWA) biodiversity hotspot and southeast Australian (SEA) regions of the Australian continent can be attributed to higher net diversification, more time for species accumulation, or both. We assembled dated molecular phylogenies for the 21 most species-rich flowering plant families found across mesic temperate Australia, encompassing both SWA and SEA regions, and applied a series of diversification models to investigate responses across different groups and timescales. We show that the high richness in SWA can be attributed to a higher net rate of lineage diversification and more time for species accumulation. Different pulses of diversification were retrieved in each region. A decrease in diversification rate across major flowering plant lineages at the Eocene-Oligocene boundary (ca 34 Ma) was witnessed in SEA but not in SWA. Our study demonstrates the importance of historical diversification pulses and differential responses to global events as drivers of present-day diversity. More broadly, we show that diversity within the SWA biodiversity hotspot is not only the result of recent radiations, but also reflects older events over the history of this planet.

Floral micromorphology and nectar composition of the early evolutionary lineage Utricularia (subgenus Polypompholyx, Lentibulariaceae).

Utricularia (Lentibulariaceae) is a genus comprising around 240 species of herbaceous, carnivorous plants. Utricularia is usually viewed as an insect-pollinated genus, with the exception of a few bird-pollinated species. The bladderworts Utricularia multifida and U. tenella are interesting species because they represent an early evolutionary Utricularia branch and have some unusual morphological characters in their traps and calyx. Thus, our aims were to (i) determine whether the nectar sugar concentrations and composition in U. multifida and U. tenella are similar to those of other Utricularia species from the subgenera Polypompholyx and Utricularia, (ii) compare the nectary structure of U. multifida and U. tenella with those of other Utricularia species, and (iii) determine whether U. multifida and U. tenella use some of their floral trichomes as an alternative food reward for pollinators. We used light microscopy, histochemistry, and scanning and transmission electron microscopy to address those aims. The concentration and composition of nectar sugars were analysed using high-performance liquid chromatography. In all of the examined species, the floral nectary consisted of a spur bearing glandular trichomes. The spur produced and stored the nectar. We detected hexose-dominated (fructose + glucose) nectar in U. multifida and U. tenella as well as in U. violacea. In both U. multifida and U. tenella, there were trichomes that blocked the entrance into the throat and spur. Because these trichomes were rich in chromoplasts and contained lipid droplets, they may form an additional visual attractant. Bearing in mind the phylogenetic hypothesis for the genus, we suggest that an early ancestor of Utricularia had a nectariferous spur flower with a lower lip that formed a wide landing platform for bee pollinators.

Floral micromorphology of the bird-pollinated carnivorous plant species Utricularia menziesii R.Br. (Lentibulariaceae).

Background and Aims: Bird pollination is rare among species in the genus Utricularia, and has evolved independently in two lineages of this genus. In Western Australia, the Western Spinebill, Acanthorhynchus superciliosus, visits flowers of Utricularia menziesii (section Pleiochasia: subgenus Polypompholyx). This study aimed to examine the micromorphology of U. menziesii flowers to assess traits that might be linked to its pollination strategy. Methods: Light microscopy, histochemistry and scanning electron microscopy were used. Nectar sugar composition was analysed using high-performance liquid chromatography. Key Results: The flowers of U. menziesii fulfil many criteria that characterize bird-pollinated flowers: red colour, a large, tough nectary spur that can withstand contact with a hard beak, lack of visual nectar guides and fragrance. Trichomes at the palate and throat may act as tactile signals. Spur nectary trichomes did not form clearly visible patches, but were more frequently distributed along vascular bundles, and were small and sessile. Each trichome comprised a single basal cell, a unicellular short pedestal cell (barrier cell) and a multicelled head. These trichomes were much smaller than those of the U. vulgaris allies. Hexose-dominated nectar was detected in flower spurs. Fructose and glucose were present in equal quantities (43 ± 3.6 and 42 ± 3.6 g L-1). Sucrose was only detected in one sample, essentially at the limit of detection for the method used. This type of nectar is common in flowers pollinated by passerine perching birds. Conclusions: The architecture of nectary trichomes in U. menziesii was similar to that of capitate trichomes of insect-pollinated species in this genus; thus, the most important specializations to bird pollination were flower colour (red), and both spur shape and size modification. Bird pollination is probably a recent innovation in the genus Utricularia, subgenus Polypompholyx, and is likely to have evolved from bee-pollinated ancestors.