Phylogenomic inference of the African tribe Monodoreae (Annonaceae) and taxonomic revision of Dennettia, Uvariodendron and Uvariopsis.

Monodoreae (Annonaceae) is a tribe composed of 11 genera and 90 species restricted to the tropical African rain forests. All the genera are taxonomically well circumscribed except the species rich genera Uvariodendron and Uvariopsis which lack a recent taxonomic revision. Here, we used a robust phylogenomic approach, including all the 90 currently accepted species, with several specimens per species, and based on more than 300 Annonaceae-specific nuclear genes, to infer the phylogenetic tree of the Monodoreae and test the limits between the genera and species. We recover all the genera as monophyletic, except the genus Uvariopsis for which the species Uvariopsistripetala falls outside this clade. We thus reinstate the monotypic genus Dennettia for its single species Dennettiatripetala. We also erect a new tribe, Ophrypetaleae trib. nov., to accommodate the genera Ophrypetalum and Sanrafaelia, as we recover them excluded from the Monodoreae tribe with good support. Below the genus level, the genera Isolona, Monodora, Uvariastrum, Uvariodendron and Uvariopsis show weakly supported nodes and phylogenetic conflicts, suggesting that population level processes of evolution might occur in these clades. Our results also support, at the molecular level, the description of several new species of Uvariodendron and Uvariopsis, as well as several new synonymies. Finally, we present a taxonomic revision of the genera Dennettia, Uvariodendron and Uvariopsis, which contain one, 18 and 17 species respectively. We provide a key to the 11 genera of the Monodoraeae and describe four new species to science: Uvariodendronkimbozaense Dagallier & Couvreur, sp. nov., Uvariodendronmossambicense Robson ex Dagallier & Couvreur, sp. nov., Uvariodendronpilosicarpum Dagallier & Couvreur, sp. nov. and Uvariopsisoligocarpa Dagallier & Couvreur, sp. nov., and provide provisional descriptions of three putatively new species. We also present lectotypifications and nomenclatural changes implying synonymies and new combinations (Uvariodendroncitriodorum (Le Thomas) Dagallier & Couvreur, comb. et stat. nov., Uvariodendronfuscumvar.magnificum (Verdc.) Dagallier & Couvreur, comb. et stat. nov., Uvariopsiscongensisvar.angustifolia Dagallier & Couvreur, var. nov., Uvariopsisguineensisvar.globiflora (Keay) Dagallier & Couvreur, comb. et stat. nov., and Uvariopsissolheidiivar.letestui (Pellegr.) Dagallier & Couvreur, comb. et stat. nov.).

RésuméLa tribu des Monodoreae (Annonaceae) est composée de 11 genres et 90 espèces des forêts tropicales humides d'Afrique. Tout les genres sont taxonomiquement bien résolus, à part les genres Uvariodendron et Uvariopsis qui manquent d'une révision taxonomique récente. Ici, nous avons utilisé une approche phylogénomique robuste pour estimer l'arbre phylogénétique des Monodoreae, et tester les limites de genres et d'espèces. Pour cela, nous avons inclut les 90 espèces acceptées, et avons séquencé plus de 300 gènes. Tous les genres sont retrouvés monophylétiques, à part le genre Uvariopsis pour lequel l'espèce Uvariopsistripetala se retrouve exclue. Nous rétablissons donc le genre monotypique Dennettia et son unique espèce Dennettiatripetala. Nous érigeons une nouvelle tribu, les Ophrypetaleae trib. nov., pour accueillir les genres Ophrypetalum et Sanrafaelia, car nous les retrouvons exclus de la tribu des Monodoreae avec un bon support. Au niveau infra-générique, les genres Isolona, Monodora, Uvariastrum, Uvariodendron et Uvariopsis montrent de faibles supports de noeuds et des conflits phylogénétiques, ce qui suggère que des processus d'évolution se déroulent au niveau des populations. Nos résultats soutiennent également, sur un plan moléculaire, la description de plusieurs nouvelles espèces d'Uvariodendron et d'Uvariopsis, de même que plusieurs synonymies. Enfin, nous présentons une révision taxonomique des genres Dennettia, Uvariodendron et Uvariopsis, qui contiennent respectivement un, 18 et 17 espèces. Nous fournissons une clé des 11 genres de Monodoreae, et décrivons quatre nouvelles espèces pour la science: Uvariodendronkimbozaense Dagallier & Couvreur, sp. nov., Uvariodendronmossambicense Robson ex Dagallier & Couvreur, sp. nov., Uvariodendronpilosicarpum Dagallier & Couvreur, sp. nov. et Uvariopsisoligocarpa Dagallier & Couvreur, sp. nov., et fournissons une description provisoire de trois autres potentielles. Nous effectuons des lectotypifications et des changements nomenclaturaux tels que des synonymies et des nouvelles combinaisons (Uvariodendroncitriodorum (Le Thomas) Dagallier & Couvreur, comb. et stat. nov., Uvariodendronfuscumvar.magnificum (Verdc.) Dagallier & Couvreur, comb. et stat. nov., Uvariopsiscongensisvar.angustifolia Dagallier & Couvreur, var. nov., Uvariopsisguineensisvar.globiflora (Keay) Dagallier & Couvreur, comb. stat. nov., et Uvariopsissolheidiivar.letestui (Pellegr.) Dagallier & Couvreur, comb. stat. nov.).

A sequential diversification with Miocene extinction and Pliocene speciation linked to mountain uplift explains the diversity of the African rain forest clade Monodoreae (Annonaceae).

BACKGROUND AND AIMS: Throughout the Cenozoic, Africa underwent several climatic and geological changes impacting the evolution of tropical rain forests (TRF). African TRF are thought to have extended from East to West in a 'pan-African' TRF, followed by several events of fragmentation during drier climate periods. During the Miocene, climate cooling and mountain uplift led to the aridification of tropical Africa and open habitats expanded at the expense of TRF, which likely experienced local extinctions. However, in plants, these drivers were previously inferred using limited taxonomic and molecular data. Here, we tested the impact of climate and geological changes on diversification within the diverse clade Monodoreae (Annonaceae) composed of 90 tree species restricted to African TRF. METHODS: We reconstructed a near complete phylogenetic tree, based on 32 nuclear genes, and dated using relaxed clocks and fossil calibrations in a Bayesian framework. We inferred the biogeographic history and the diversification dynamics of the clade using multiple birth-death models. KEY RESULTS: Monodoreae originated in East African TRF ca. 25 million years ago (Ma) and expanded toward Central Africa during the Miocene. We inferred range contractions during the middle Miocene and document important connections between East and West African TRF after 15-13 Ma. Our results indicated a sudden extinction event during the late Miocene, followed by an increase in speciation rates. Birth-death models suggested that African elevation change (orogeny) is positively linked to speciation in this clade. CONCLUSION: East Africa is inferred as an important source of Monodoreae species, and possibly for African plant diversity in general. Our results support a "sequential scenario of diversification" where increased aridification triggered extinction of TRF species in Monodoreae. This was quickly followed by rain forests fragmentation, subsequently enhancing lagged speciation resulting from vicariance and improved climate conditions. In contrast to previous ideas, the uplift of East Africa is shown to have played a positive role in Monodoreae diversification.

Population structure in Neotropical plants: Integrating pollination biology, topography and climatic niches.

Animal pollinators mediate gene flow among plant populations, but in contrast to well-studied topographic and (Pleistocene) environmental isolating barriers, their impact on population genetic differentiation remains largely unexplored. Comparing how these multifarious factors drive microevolutionary histories is, however, crucial for better resolving macroevolutionary patterns of plant diversification. Here we combined genomic analyses with landscape genetics and niche modelling across six related Neotropical plant species (424 individuals across 33 localities) differing in pollination strategy to test the hypothesis that highly mobile (vertebrate) pollinators more effectively link isolated localities than less mobile (bee) pollinators. We found consistently higher genetic differentiation (FST ) among localities of bee- than vertebrate-pollinated species with increasing geographical distance, topographic barriers and historical climatic instability. High admixture among montane populations further suggested relative climatic stability of Neotropical montane forests during the Pleistocene. Overall, our results indicate that pollinators may differentially impact the potential for allopatric speciation, thereby critically influencing diversification histories at macroevolutionary scales.

Individualistic evolutionary responses of Central African rain forest plants to Pleistocene climatic fluctuations.

Understanding the evolutionary dynamics of genetic diversity is fundamental for species conservation in the face of climate change, particularly in hyper-diverse biomes. Species in a region may respond similarly to climate change, leading to comparable evolutionary dynamics, or individualistically, resulting in dissimilar patterns. The second-largest expanse of continuous tropical rain forest (TRF) in the world is found in Central Africa. Here, present-day patterns of genetic structure are thought to be dictated by repeated expansion and contraction of TRFs into and out of refugia during Pleistocene climatic fluctuations. This refugia model implies a common response to past climate change. However, given the unrivalled diversity of TRFs, species could respond differently because of distinct environmental requirements or ecological characteristics. To test this, we generated genome-wide sequence data for >700 individuals of seven codistributed plants from Lower Guinea in Central Africa. We inferred species' evolutionary and demographic histories within a comparative phylogeographic framework. Levels of genetic structure varied among species and emerged primarily during the Pleistocene, but divergence events were rarely concordant. Demographic trends ranged from repeated contraction and expansion to continuous growth. Furthermore, patterns in genetic variation were linked to disparate environmental factors, including climate, soil, and habitat stability. Using a strict refugia model to explain past TRF dynamics is too simplistic. Instead, individualistic evolutionary responses to Pleistocene climatic fluctuations have shaped patterns in genetic diversity. Predicting the future dynamics of TRFs under climate change will be challenging, and more emphasis is needed on species ecology to better conserve TRFs worldwide.

Use of RNA and DNA to Identify Mechanisms of Bacterial Community Homogenization.

Biotic homogenization, i.e., the increase in community similarity through time or space, is a commonly observed response following conversion of native ecosystems to agriculture, but our understanding of the ecological mechanisms underlying this process is limited for bacterial communities. Identifying mechanisms of bacterial community homogenization following rapid environmental change may be complicated by the fact only a minority of taxa is active at any time. Here we used RNA- and DNA-based metabarcoding to distinguish putatively active taxa in the bacterial community from inactive taxa. We asked how soil bacterial communities respond to land use change following a rapid transition from rainforest to agriculture in the Congo Basin using a chronosequence that spans from roughly 1 week following slash-and-burn to an active plantation roughly 1.5 years post-conversion. Our results indicate that the magnitude of community homogenization is larger in the RNA-inferred community than the DNA-inferred perspective. We show that as the soil environment changes, the RNA-inferred community structure tracks environmental variation and loses spatial structure. The DNA-inferred community does not respond to environmental variability to the same degree, and is instead homogenized by a subset of taxa that is shared between forest and conversion sites. Our results suggest that complementing DNA-based surveys with RNA can provide insights into the way bacterial communities respond to environmental change.

Tracking of Host Defenses and Phylogeny During the Radiation of Neotropical Inga-Feeding Sawflies (Hymenoptera; Argidae).

Coevolutionary theory has long predicted that the arms race between plants and herbivores is a major driver of host selection and diversification. At a local scale, plant defenses contribute significantly to the structure of herbivore assemblages and the high alpha diversity of plants in tropical rain forests. However, the general importance of plant defenses in host associations and divergence at regional scales remains unclear. Here, we examine the role of plant defensive traits and phylogeny in the evolution of host range and species divergence in leaf-feeding sawflies of the family Argidae associated with Neotropical trees in the genus Inga throughout the Amazon, the Guiana Shield and Panama. Our analyses show that the phylogenies of both the sawfly herbivores and their Inga hosts are congruent, and that sawflies radiated at approximately the same time, or more recently than their Inga hosts. Analyses controlling for phylogenetic effects show that the evolution of host use in the sawflies associated with Inga is better correlated with Inga chemistry than with Inga phylogeny, suggesting a pattern of delayed host tracking closely tied to host chemistry. Finally, phylogenetic analyses show that sister species of Inga-sawflies are dispersed across the Neotropics, suggesting a role for allopatric divergence and vicariance in Inga diversification. These results are consistent with the idea that host defensive traits play a key role not only in structuring the herbivore assemblages at a single site, but also in the processes shaping host association and species divergence at a regional scale.

Transformaciones espacio-temporales de la cobertura vegetal en el Parque Nacional Corcovado, 1960-2014 / Space-time transformations of vegetation coverage in Corcovado National Park, 1960-2014

Resumen Los estudios a nivel regional que evalúan las dinámicas espacio-temporales de la vegetación en Costa Rica, especialmente, dentro de los Parques Nacionales son escasos. Así, considerando aportar en este vacío de conocimiento, este artículo analiza la distribución espacio-temporal de la vegetación dentro del periodo 1960-1976, 1992, 1997 y 2012 en Parque Nacional Corcovado, localizado en la Península de Osa y catalogado como el bosque tropical lluvioso más septentrional en la costa pacífica de América. Además, esta área contiene una riqueza de biodiversidad, fundamentada en su antigüedad geológica, el aislamiento que presentó durante largos periodos; así como las condiciones climáticas particulares que generan ecosistemas únicos como bosques nubosos relacionados con brisa marina a alturas de más de 500 msnm. Este estudio evalúa la distribución espacial de la vegetación a partir de mapas resultantes del proceso de fotointerpretación de imágenes del 1960, 1976, 1997 y 2012, así como del análisis del índice de paisaje. Se concluye que las transformaciones espacio-temporales de la vegetación durante el periodo de estudio han sido mínimas, y el hecho de que hayan sido escasas las áreas impactadas por la actividad antrópica, generó una restauración ecológica importante durante las últimas décadas. Se encontró una relación de expansión y contracción entre el bosque nuboso y bosque, así como este último y el bosque inundado, en función de la recuperación de la cobertura boscosa dentro del Parque Nacional y de la Península de Osa, y el volumen y distribución de la precipitación. Asimismo, este estudio propone la necesidad de establecer el monitoreo permanente de la vegetación para esclarecer las relaciones que se establecen entre estos tipos de vegetación.

Abstract Regional studies evaluating spatial-temporal transformations of vegetation in Costa Rica, especially within National Parks, are scarce. Therefore, this paper analyses the vegetation distribution during 1960, 1976, 1997 and 2014 in Corcovado National Park. This protected area is located in the Osa Peninsula, Costa Rica, and represents the Northern most tropical rain forest on the Pacific coast of America. This area offers a great wealth of biodiversity due to its geological formation, isolation for long time periods, and its particular climatic conditions that generate unique ecosystems such as cloud forests associated with ocean situated close to hill breezes located over 500 masl, as well as dense tropical forest. This study evaluates the spatial distribution of vegetation based on maps that resulted from the process of photo-interpretation of 1960, 1976, 1997 and 2012, as well as from the landscape index analysis. It concludes that during the study period, the vegetation changes have been minimal. Instead, in the few areas impacted by human activity (small-scale agriculture and pasture lands) an ecological restoration has occurred during recent decades. In addition, this research suggests that the recovering forest cover within the park and even within the Osa Peninsula has been expanding the cloud forest. An increase and contraction relationship between the different categories (Cloud forest and forests as well of flooded forest and forest in flat zones) was found. Furthermore, this study suggests the need of permanent plots in order to monitor vegetation and identify the factors that explain this previous process. Rev. Biol. Trop. 66(1): 352-367. Epub 2018 March 01.

Controls on foliar nutrient and aluminium concentrations in a tropical tree flora: phylogeny, soil chemistry and interactions among elements.

Foliar elemental concentrations are predictors of life-history variation and contribute to spatial patterns in biogeochemical cycling. We examined the contributions of habitat association, local soil environment, and elemental interactions to variation in foliar elemental concentrations in tropical trees using methods that account for phylogeny. We sampled top-soils and leaves of 58 tropical trees in heath forest (HF) on nutrient-poor sand and mixed dipterocarp forest (MDF) on nutrient-rich clay soils. A phylogenetic generalized least squares method was used to determine how foliar nutrient and aluminium (Al) concentrations varied in response to habitat distribution, soil chemistry and other elemental concentrations. Foliar nitrogen (N) and Al concentrations were greater for specialists of MDF than for specialists of HF, while foliar calcium (Ca) concentrations showed the opposite trend. Foliar magnesium (Mg) concentrations were lower for generalists than for MDF specialists. Foliar element concentrations were correlated with fine-scale variation in soil chemistry in phylogenetically controlled analyses across species, but there was limited within-species plasticity in foliar elemental concentrations. Among Al accumulators, foliar Al concentration was positively associated with foliar Ca and Mg concentrations, and negatively associated with foliar phosphorus (P) concentrations. The Al-accumulation trait and relationships between foliar elemental and Al concentrations may contribute to species habitat partitioning and ecosystem-level differences in biogeochemical cycles.

The temperature acclimation potential of tropical bryophytes.

Bryophyte biomass and diversity in tropical moist forests decrease dramatically from higher altitudes towards the lowlands. High respiratory carbon losses at high temperatures may partly explain this pattern, if montane species are unable to acclimatise their metabolic rates to lowland temperatures. We transplanted ten bryophyte species from two altitudes (1200 and 500 m a.s.l.) to lower (warmer) altitudes (500 m and sea level) in Panama. We studied short-term temperature acclimation of CO2 exchange for 2.5 months, and survival and growth for 21 months following transplantation. Short-term acclimation did not occur, and on a longer time scale mortality was highest and growth lowest in the transplanted samples. A few transplanted samples of most species, however, survived the whole experiment and finished with growth rates similar to controls. This recovery of growth rate suggests temperature acclimation, in spite of no measurable metabolic changes in smaller random samples. This acclimation even compensated for shorter periods of CO2 uptake due to more rapid drying. Nevertheless, these species are not abundant in lowland forests, perhaps due to dispersal or establishment limitation. The apparent heterogeneity of the acclimation potential within species may allow populations to adapt locally and avoid being forced uphill under climatic warming.

Relationship between photosynthetic phosphorus-use efficiency and foliar phosphorus fractions in tropical tree species.

How plants develop adaptive strategies to efficiently use nutrients on infertile soils is an important topic in plant ecology. It has been suggested that, with decreasing phosphorus (P) availability, plants increase photosynthetic P-use efficiency (PPUE) (i.e., the ratio of instantaneous photosynthetic carbon assimilation rate per unit foliar P). However, the mechanism to increase PPUE remains unclear. In this study, we tested whether high PPUE is explained by an optimized allocation of P in cells among P-containing biochemical compounds (i.e., foliar P fractions). We investigated the relationships among mass-based photosynthetic carbon assimilation rate (A mass), PPUE, total foliar P concentration, and foliar P fractions in 10 tree species in two tropical montane rain forests with differing soil P availability (five species on sedimentary soils and five species on P-poorer ultrabasic serpentine soils) on Mount Kinabalu, Borneo. We chemically fractionated foliar P into the following four fractions: metabolic P, lipid P, nucleic acid P, and residual P. A mass was positively correlated with the concentrations of total foliar P and of metabolic P across 10 tree species. Mean A mass and mean concentrations of total foliar P and of each foliar P fraction were lower on the P-poorer ultrabasic serpentine soils than on the sedimentary soils. There was a negative relationship between the proportion of metabolic P per total P and the proportion of lipid P per total P. PPUE was positively correlated with the ratio of metabolic P to lipid P. High PPUE is explained by the net effect of a relatively greater investment of P into P-containing metabolites and a relatively lesser investment into phospholipids in addition to generally reduced concentrations of all P fractions. We conclude that plants optimize the allocation of P among foliar P fractions for maintaining their productivity and growth and for reducing demand for P as their adaptation to P-poor soils.

Growth, biomass allocation and photosynthesis of invasive and native Hawaiian rainforest species.

Growth, biomass allocation, and photosynthetic characteristics of seedlings of five invasive non-indigenous and four native species grown under different light regimes were studied to help explain the success of invasive species in Hawaiian rainforests. Plants were grown under three greenhouse light levels representative of those found in the center and edge of gaps and in the understory of Hawaiian rainforests, and under an additional treatment with unaltered shade. Relative growth rates (RGRs) of invasive species grown in sun and partial shade were significantly higher than those for native species, averaging 0.25 and 0.17 g g-1 week-1, respectively, while native species averaged only 0.09 and 0.06 g g-1 week-1, respectively. The RGR of invasive species under the shade treatment was 40% higher than that of native species. Leaf area ratios (LARs) of sun and partial-shade-grown invasive and native species were similar but the LAR of invasive species in the shade was, on average, 20% higher than that of native species. There were no differences between invasive and native species in biomass allocation to shoots and roots, or in leaf mass per area across light environments. Light-saturated photosynthetic rates (Pmax) were higher for invasive species than for native species in all light treatments. Pmax of invasive species grown in the sun treatment, for example, ranged from 5.5 to 11.9 µmol m-2 s-1 as compared with 3.0-4.5 µmol m-2 s-1 for native species grown under similar light conditions. The slope of the linear relationship between Pmax and dark respiration was steeper for invasive than for native species, indicating that invasive species assimilate more CO2 at a lower respiratory cost than native species. These results suggest that the invasive species may have higher growth rates than the native species as a consequence of higher photosynthetic capacities under sun and partial shade, lower dark respiration under all light treatments, and higher LARs when growing under shade conditions. Overall, invasive species appear to be better suited than native species to capturing and utilizing light resources, particularly in high-light environments such as those characterized by relatively high levels of disturbance.

Variation in seed and seedling traits in Pithecellobium pedicellare, a tropical rain forest tree.

Pithecellobium pedicellare, a mimosoid legume, is a large canopy tree in the tropical rain forests of Costa Rica. We examined the pattern of variation in seed weight, germination date, hypocotyl length (stem), and rachis length (the first leaf) of the seedlings in this species. Seeds collected from widely dispersed individual trees at the La Selva Biological Station, Costa Rica, were randomly planted in blocks, and grown under controlled, indoor conditions for about 2 weeks. There-fore, we were able to quantify the effects of maternal family on mean seed weight and the effects of maternal family and microenvironment on the remaining traits examined. A significant effect of maternal family was detected for all traits. In particular, the maternal effects on germination date and seedling size traits which were consistently significant even after controlling the initial seed weight may indicate that the maternal effects reflect, at least to some extent, maternal genetic control over these traits. Despite overall strong maternal effects, the performance of maternal siblings, such as the rachis length, differed among blocks. The sensitivity of maternal siblings to the local environments may contribute to the maintenance of genetic variability in this highly outcrossing tropical species.