The enigmatic tropical alpine flora on the African sky islands is young, disturbed, and unsaturated.

Tropical alpine floras are renowned for high endemism, spectacular giant rosette plants testifying to convergent adaptation to harsh climates with nightly frosts, and recruitment dominated by long-distance dispersal from remote areas. In contrast to the larger, more recent (late Miocene onward) and contiguous expanses of tropical alpine habitat in South America, the tropical alpine flora in Africa is extremely fragmented across small patches on distant mountains of variable age (Oligocene onward). How this has affected the colonization and diversification history of the highly endemic but species-poor afroalpine flora is not well known. Here we infer phylogenetic relationships of ∼20% of its species using novel genome skimming data and published matrices and infer a timeframe for species origins in the afroalpine region using fossil-calibrated molecular clocks. Although some of the mountains are old, and although stem node ages may substantially predate colonization, most lineages appear to have colonized the afroalpine during the last 5 or 10 My. The accumulation of species increased exponentially toward the present. Taken together with recent reports of extremely low intrapopulation genetic diversity and recent intermountain population divergence, this points to a young, unsaturated, and dynamic island scenario. Habitat disturbance caused by the Pleistocene climate oscillations likely induced cycles of colonization, speciation, extinction, and recolonization. This study contributes to our understanding of differences in the histories of recruitment on different tropical sky islands and on oceanic islands, providing insight into the general processes shaping their remarkable floras.

Structural adaptations in plants from the humid equatorial Andes indicate a trade-off between hydraulic transport efficiency and safety.

PREMISE: Environmental gradients of mountains are reflected in traits that are common to high-elevation plants worldwide. Closely related species of Senecio from the equatorial Andes grow as broad-leaved climbers in montane forests, basal broad-leaved rosette herbs in azonal marshy habitats, and ascending, narrow-leaved subshrubs in high-elevation páramo. Habitat variation along the elevational gradient enables testing whether modifications in leaf and stem functional traits among species were driven by contrasting environmental conditions. METHODS: We used quantitative analyses to describe changes in morphological and anatomical traits of leaves and stems in 10 species from various habitats. We applied univariate (linear regression, hierarchical ANOVA) and multivariate (NMDS ordination, permutational MANOVA) techniques to examine the correlation of traits with the species' habitats and elevation. RESULTS: Species from the humid and frost-free montane forest develop xylem optimized for transport efficiency by increasing the internal diameter and length of the conduits. In contrast, páramo species are optimized toward hydraulic safety by producing narrower conduits and are more likely to prevent the risk of frost-induced cavitation. Moreover, species from the high-elevation páramo habitats present a set of water-transport-related anatomical traits of leaf lamina, allowing for efficient regulation of transpiration losses. CONCLUSIONS: Morphological and anatomical traits of leaves and stems in species of Senecio inhabiting montane forests and high-elevation páramo in the equatorial Andes demonstrate a trade-off between hydraulic safety and efficiency of water transport.

Island woodiness underpins accelerated disparification in plant radiations.

The evolution of secondary (insular) woodiness and the rapid disparification of plant growth forms associated with island radiations show intriguing parallels between oceanic islands and tropical alpine sky islands. However, the evolutionary significance of these phenomena remains poorly understood and the focus of debate. We explore the evolutionary dynamics of species diversification and trait disparification across evolutionary radiations in contrasting island systems compared with their nonisland relatives. We estimate rates of species diversification, growth form evolution and phenotypic space saturation for the classical oceanic island plant radiations - the Hawaiian silverswords and Macaronesian Echium - and the well-studied sky island radiations of Lupinus and Hypericum in the Andes. We show that secondary woodiness is associated with dispersal to islands and with accelerated rates of species diversification, accelerated disparification of plant growth forms and occupancy of greater phenotypic trait space for island clades than their nonisland relatives, on both oceanic and sky islands. We conclude that secondary woodiness is a prerequisite that could act as a key innovation, manifest as the potential to occupy greater trait space, for plant radiations on island systems in general, further emphasizing the importance of combinations of clade-specific traits and ecological opportunities in driving adaptive radiations.

Sweet vernal grasses (Anthoxanthum) colonized African mountains along two fronts in the Late Pliocene, followed by secondary contact, polyploidization and local extinction in the Pleistocene.

High tropical mountains harbour remarkable and fragmented biodiversity thought to a large degree to have been shaped by multiple dispersals of cold-adapted lineages from remote areas. Few dated phylogenetic/phylogeographic analyses are however available. Here, we address the hypotheses that the sub-Saharan African sweet vernal grasses have a dual colonization history and that lineages of independent origins have established secondary contact. We carried out rangewide sampling across the eastern African high mountains, inferred dated phylogenies from nuclear ribosomal and plastid DNA using Bayesian methods, and performed flow cytometry and AFLP (amplified fragment length polymorphism) analyses. We inferred a single Late Pliocene western Eurasian origin of the eastern African taxa, whose high-ploid populations in one mountain group formed a distinct phylogeographic group and carried plastids that diverged from those of the currently allopatric southern African lineage in the Mid- to Late Pleistocene. We show that Anthoxanthum has an intriguing history in sub-Saharan Africa, including Late Pliocene colonization from southeast and north, followed by secondary contact, hybridization, allopolyploidization and local extinction during one of the last glacial cycles. Our results add to a growing body of evidence showing that isolated tropical high mountain habitats have a dynamic recent history involving niche conservatism and recruitment from remote sources, repeated dispersals, diversification, hybridization and local extinction.

Frequent colonization and little in situ speciation in Senecio in the tropical alpine-like islands of eastern Africa.

PREMISE OF THE STUDY: Floras of continental habitat islands, like those of islands, originate mostly through colonization, which can be followed by in situ speciation. We here address the question of the relative importance of colonization and in situ diversification in the high-altitude areas of the eastern African high mountains, the tropical Afroalpine Region, using the most species-rich genus in the region, Senecio, as an example. METHODS: We expanded earlier Senecioneae phylogenies by adding more tropical African species and analyzed our phylogenetic tree biogeographically. KEY RESULTS: Senecio contains at least five clades with tropical African species, all of them containing tropical afroalpine species. Between four to 14 independent colonization events into the tropical Afroalpine most likely from montane regions in southern Africa were found. Additionally, relationships of tropical afroalpine species to Palearctic and South American taxa were identified. Although some in situ diversification occurred in Senecio in the tropical Afroalpine, the resulting number of species per clade is never higher than seven. CONCLUSION: Like other genera, Senecio colonized the tropical Afroalpine several times independently. Comparison with Mt. Kinabalu, a small tropical alpine-like region in Southeast Asia, and alpine-like regions in the Andes implies that rates of in situ speciation might be linked to area size.

Good-bye to tropical alpine plant giants under warmer climates? Loss of range and genetic diversity in Lobelia rhynchopetalum.

The main aim of this paper is to address consequences of climate warming on loss of habitat and genetic diversity in the enigmatic tropical alpine giant rosette plants using the Ethiopian endemic Lobelia rhynchopetalum as a model. We modeled the habitat suitability of L. rhynchopetalum and assessed how its range is affected under two climate models and four emission scenarios. We used three statistical algorithms calibrated to represent two different complexity levels of the response. We analyzed genetic diversity using amplified fragment length polymorphisms and assessed the impact of the projected range loss. Under all model and scenario combinations and consistent across algorithms and complexity levels, this afro-alpine flagship species faces massive range reduction. Only 3.4% of its habitat seems to remain suitable on average by 2,080, resulting in loss of 82% (CI 75%-87%) of its genetic diversity. The remaining suitable habitat is projected to be fragmented among and reduced to four mountain peaks, further deteriorating the probability of long-term sustainability of viable populations. Because of the similar morphological and physiological traits developed through convergent evolution by tropical alpine giant rosette plants in response to diurnal freeze-thaw cycles, they most likely respond to climate change in a similar way as our study species. We conclude that specialized high-alpine giant rosette plants, such as L. rhynchopetalum, are likely to face very high risk of extinction following climate warming.

Photosynthesis and photoinhibition in a tropical alpine giant rosette plant, Lobelia rhynchopetalum.

Carbodioxide uptake, oxygen evolution and chlorophyll fluorescence of leaves of Lobelia Lobelia rhynchopetalum Hemsl., a giant rosette plant of the tropical alpine regions of Ethiopia, were studied under field conditions at 4000 m above sea level. Our objective was to investigate the photosynthetic adaptation to the combination of wide fluctuation in diurnal temperature, high photon flux densities (PFD) and low CO2 partial pressure encountered in these regions. At an ambient CO2 partial pressure of c. 17 Pa, maximal rates of CO2 uptake were low, ranging between 4 and 6 µmol m-2 s-1 . Such rates, however, required high PFDs and were observed only at levels of 1500 µmol photons m-2 s-2 . Carbon dioxide uptake was significantly inhibited when PFD was ≤ 2000 µmol photons m-2 s-1 . On the other hand, at saturating CO2 levels, maximal photosynthetic oxygen evolution was higher (30 µmol C2 m-2 s-1 ). saturating at the same PFD as CO2 uptake. Quantum efficiency of CO2 uptake (0.006 mol CO2 mol photons-1 , at high altitude and a low CO, partial pressure of 17 Pa) and even of oxygen evolution under CO2 -saturating conditions in the leaf O2 electrode (0.05 mol O2 mo) photons-1 ) indicated reduced photosynthetic efficiency. Electron transport rate (ETR) was strongly correlated with the leaf temperature. Non-photochemical quenching (NPQ) responded inversely to leaf temperature and stomatal conductance. The results indicated that in the morning, when the sun irradiates the partly frozen leaves with closed stomata, NPQ is the principal mechanism by which Lobelia leaves protect their photosynthetic apparatus. However, during the day, the predominant upright inclination of the leaves significantly contributes to protecting the leaves from excess light absorption. A comparison of the chlorophyll fluorescence of young and old leaves revealed that the former had high ETR and quantum efficiency of photosynthetic electron transport but a lower capacity for NPQ. Extremely high NPQ values but low ETR and low quantum efficiency were recorded for the old leaves. Thus, in the course of maturation the leaves apparently lose photosynthetic efficiency but increase their capability for protective non-photochemical quenching.

Pubescence, floral temperature and fecundity in species of Puya (Bromeliaceae) in the Ecuadorian Andes.

The effects of inflorescence pubescence on floral temperatures and fecundity were examined in four species of Puya in the Ecuadorian Andes. These species span an elevational range from 1,980-4,000 m and comparisons among these species showed that pubescence production increases significantly with elevation. Flower temperatures of glabrous or slightly pubescent species of Puya from lower elevations closely tracked air temperature, while those of the pubescent páramo species did not. Pubescence removal experiments on Puya hamata, a páramo species, demonstrated that pubescence is an effective insulator, maintaining elevated flower temperatures. In Puya clava-herculis (also a páramo species) elevated flower temperatures were associated with higher seed set. Thus, the greater production of inflorescence pubescence in páramo species of Puya may be an important factor contributing to reproductive success in these higher elevation species.

Fire adaptation in Neblinaria celiae (Theaceae), a high-elevation rosette shrub endemic to a wet equatorial tepui.

Neblinaria celiae (Theaceae), a rosette shrub endemic to the exceedingly rainy summit of remote Cerro de la Neblina in southern Venezuela, has a previously undescribed set of adaptations to fire. Its growth form entails sparse branching, massive terminal leaf rosettes, and thick bark. It is highly fire-tolerant, with a survival rate of 93% in a stand recently ignited by lightning, vs. 0% in seven co-occurring woody species. Survival increases sharply with rosette height, favoring a sparsely branched habit that would maximize the rate of upward growth through the sparse fuel layer supported by a sterile substrate. Thick bark and massive rosettes help protect cambial and foliar meristems from brief exposure to high temperatures. Rosettes on shorter plants are exposed to greater damage from fire near the ground and, as expected, are bigger and impound more rainwater; the greater number of leaves nearly balances the greater leaf mortality caused by fire. We relate Neblinaria's growth form to its dominance atop Neblina, to a general model for the evolution of sparse branching, and to the evolution of growth form in other tepui plants.

Microclimate and ecophysiological significance of the tree-like life-form of Lobelia rhynchopetalum in a tropical alpine environment.

The microclimate and the adaptive significance of the tree-like plant life-form for growth in a tropical alpine environment was investigated with the pachycaul arborescent giant rosette plant, Lobelia rhynchopetalum (Hochst. A. Rich.) Hemsl. in the Bale and Simen Mountains, Ethiopia. The microclimate of plants of three height classes was examined with respect to temperature, relative humidity and the effect of wind. Although the total heat gains were rather similar, leaves of young, still stemless (acaulescent) individuals of Lobelia were subjected to a high diurnal temperature fluctuation of up to 29 K compared to a 14-K fluctuation for the leaves of an individual 3.5 m in height. During the cold nights, temperatures of the inner rosette leaves and inside leaf buds of caulescent plants were 4-5 K above air temperature, while corresponding temperatures of acaulescent individuals were 1-2 K below air temperature. The inner temperature of the stem tissue was higher than the surface temperature of the stem by about 5 K for most of the cold night. The annual rates of increment in whole plant, stem and rosette height, and stem diameter of L. rhynchopetalum showed that the young, still acaulescent individuals, with an annual increment of 5.6 cm in plant height, had the lowest growth rate, compared to 12.1 and 22.1 cm for caulescent life-forms. The results show that the most important advantage gained by the tree-like life-form of adult L. rhynchopetalum is probably a more favourable microclimate in which the strong diurnal temperature fluctuations at the ground are mitigated and nocturnal temperatures do not drop below freezing point.