Genomic signatures of past megafrugivore-mediated dispersal in Malagasy palms

Seed dispersal affects gene flow and hence genetic differentiation of plant populations. During the Late Quaternary, most fruit-eating and seed-dispersing megafauna went extinct, but whether these animals have left signatures in the population genetics of their food plants, particularly those with large, ‘megafaunal’ fruits (i.e. &gt;4 cm—megafruits), remains unclear. Here, we assessed the population history, genetic differentiation and recent migration among populations of four animal-dispersed palm (Arecaceae) species with large (Borassus madagascariensis), medium-sized (Hyphaene coriacea, Bismarckia nobilis) and small (Chrysalidocarpus madagascariensis) fruits on Madagascar. We integrated double-digest restriction-site-associated DNA sequencing (ddRAD) of 167 individuals from 25 populations with (past) distribution ranges for extinct (e.g., giant lemurs and elephant birds) and extant seed-dispersing animals, landscape and human impact data, and applied linear mixed-effects models to explore the drivers of genetic variation in Malagasy palms. Palm populations that shared more megafrugivore species in the past had lower genetic differentiation than populations that shared fewer megafrugivore species. This suggests that megafrugivore-mediated seed dispersal in the past may have led to frequent gene flow among populations. In comparison, extant frugivore diversity only decreased genetic differentiation in the small-fruited palm. Furthermore, genetic differentiation of all palm species decreased with landscape connectivity (i.e. environmental suitability, forest cover and river density) and human impact (i.e. road density), while migration rates of the small-fruit palm increased with road density. Synthesis. Our results suggest that the legacy of megafrugivores regularly achieving long dispersal distances is still reflected in the population genetics of palms that were formerly dispersed by such animals. Furthermore, low genetic differentiation was possibly maintained after the megafauna extinctions through alternative dispersal (e.g. human- or river-mediated), long generation times and long lifespans of these megafruit palms. Our study illustrates how species interactions that happened &gt;1000 years ago can leave imprints in their population genetics.</p

A universal probe set for targeted sequencing of 353 nuclear genes from any flowering plant designed using k-medoids clustering

Sequencing of target-enriched libraries is an efficient and cost-effective method for obtaining DNA sequence data from hundreds of nuclear loci for phylogeny reconstruction. Much of the cost of developing targeted sequencing approaches is associated with the generation of preliminary data needed for the identification of orthologous loci for probe design. In plants, identifying orthologous loci has proven difficult due to a large number of whole-genome duplication events, especially in the angiosperms (flowering plants). We used multiple sequence alignments from over 600 angiosperms for 353 putatively single-copy protein-coding genes identified by the One Thousand Plant Transcriptomes Initiative to design a set of targeted sequencing probes for phylogenetic studies of any angiosperm group. To maximize the phylogenetic potential of the probes, while minimizing the cost of production, we introduce a k-medoids clustering approach to identify the minimum number of sequences necessary to represent each coding sequence in the final probe set. Using this method, 5-15 representative sequences were selected per orthologous locus, representing the sequence diversity of angiosperms more efficiently than if probes were designed using available sequenced genomes alone. To test our approximately 80,000 probes, we hybridized libraries from 42 species spanning all higher-order groups of angiosperms, with a focus on taxa not present in the sequence alignments used to design the probes. Out of a possible 353 coding sequences, we recovered an average of 283 per species and at least 100 in all species. Differences among taxa in sequence recovery could not be explained by relatedness to the representative taxa selected for probe design, suggesting that there is no phylogenetic bias in the probe set. Our probe set, which targeted 260 kbp of coding sequence, achieved a median recovery of 137 kbp per taxon in coding regions, a maximum recovery of 250 kbp, and an additional median of 212 kbp per taxon in flanking non-coding regions across all species. These results suggest that the Angiosperms353 probe set described here is effective for any group of flowering plants and would be useful for phylogenetic studies from the species level to higher-order groups, including the entire angiosperm clade itself

Phylogenomics and the rise of the angiosperms

Angiosperms are the cornerstone of most terrestrial ecosystems and human livelihoods1,2. A robust understanding of angiosperm evolution is required to explain their rise to ecological dominance. So far, the angiosperm tree of life has been determined primarily by means of analyses of the plastid genome3,4. Many studies have drawn on this foundational work, such as classification and first insights into angiosperm diversification since their Mesozoic origins5,6,7. However, the limited and biased sampling of both taxa and genomes undermines confidence in the tree and its implications. Here, we build the tree of life for almost 8,000 (about 60%) angiosperm genera using a standardized set of 353 nuclear genes8. This 15-fold increase in genus-level sampling relative to comparable nuclear studies9 provides a critical test of earlier results and brings notable change to key groups, especially in rosids, while substantiating many previously predicted relationships. Scaling this tree to time using 200 fossils, we discovered that early angiosperm evolution was characterized by high gene tree conflict and explosive diversification, giving rise to more than 80% of extant angiosperm orders. Steady diversification ensued through the remaining Mesozoic Era until rates resurged in the Cenozoic Era, concurrent with decreasing global temperatures and tightly linked with gene tree conflict. Taken together, our extensive sampling combined with advanced phylogenomic methods shows the deep history and full complexity in the evolution of a megadiverse clade

<i>Maesa brevipedicellata</i> (<i>Primulaceae</i>), a new species from Papua New Guinea

Maesa brevipedicellata, a new species of Maesa ( Primulaceae-Maesoideae) from Papua New Guinea, is described and illustrated based on herbarium specimen observations. The collections of this species resemble M. rufovillosa and were previously determined as that species. Maesa brevipedicellata is unique with its self- supporting habit, hispid hairs throughout and paniculate inflorescences with very short pedicels. This new species mainly differs from M. rufovillosa by the habit (tree/shrub in M. brevipedicellata vs climber in M. rufovillosa) and the inflorescence structure (panicles in M. brevipedicellata vs simple racemes in M. rufovillosa).</jats:p

Maesa brevipedicellata (Primulaceae), a new species from Papua New Guinea

Maesa brevipedicellata, a new species of Maesa (Primulaceae-Maesoideae) from Papua New Guinea, is described and illustrated based on herbarium specimen observations. The collections of this species resemble M. rufovillosa and were previously determined as that species. Maesa brevipedicellata is unique with its selfsupporting habit, hispid hairs throughout and paniculate inflorescences with very short pedicels. This new species mainly differs from M. rufovillosa by the habit (tree/shrub in M. brevipedicellata vs climber in M. rufovillosa) and the inflorescence structure (panicles in M. brevipedicellata vs simple racemes in M. rufovillosa)

Megafrugivores as fading shadows of the past: extant frugivores and the abiotic environment as the most important determinants of the distribution of palms in Madagascar

The extinction of all Madagascar's megafrugivores ca. 1000 years ago, may have left its signature on the current distribution of vertebrate-dispersed plants across the island, due to the loss of effective seed dispersal. In this study, we dissect the roles of extinct and extant frugivore distributions, abiotic variables, human impact and spatial predictors on the compositional turnover, or beta-diversity, of palm (Arecaceae) species and their fruit sizes across 40 assemblages on Madagascar. Variation partitioning showed that palm beta-diversity is mostly shaped by the distribution of extant frugivores (8 lemur, 3 bird, 2 rodent and 1 bat species) and the abiotic environment (e.g., forest cover, slope and temperature), and to a lesser extent by the distribution of extinct frugivores (5 giant lemur and 3 elephant bird species). However, the contribution of these variables differed between dry western assemblages and wet eastern assemblages, with a more prominent role, albeit still small, of extinct megafrugivores in the west. These results suggest that palm distributions in the dry west of Madagascar, where megafrugivores were probably most abundant in the past, still show signatures of past interactions. With a fourth-corner analysis we observed that the distribution of palm species with relatively large fruits and seeds was negatively associated with home range of extant mammalian frugivores and frugivore richness of both past and extant communities, and positively associated with the hand-wing index (HWI) – a proxy for dispersal ability - of extant bird communities. This suggests that palm species with relatively large fruits tend to occur in places with fewer, small-ranged mammalian frugivores, which may indicate dysfunctional seed dispersal, although a few wide-ranging bird species may compensate this loss by dispersing the seeds of small-to medium-sized palm fruits. Our results shed new light on anachronisms in Madagascar, and how defaunation and past interactions may underlie current plant distributions.This data repository consists of the following folders and files: Main folder Word document containing information on each file and instructions for use (ReadMe.docx) Excel document with 4 different sheets, containing supplementary tables S1, S2 and S3 and their references (TableS1_S2_S3.xlsx) Supporting information for the manuscript (SupportingInformation.pdf) "data" folder Palm presence-absence data for each of the forty 0.3x0.3 grid cells (Palms_in_grid03.csv) Palm dispersal-related trait data (maximum stem height in meters, average fruit length in millimeters, average fruit width in millimeters, average seed length in millimeters and average seed width in millimeters) for the 165 palm species appearing in the 40 grid cells (PalmTraits.csv) Average climatic, soil and human variables per grid cell (Environment_grid03.csv): Extant and extinct frugivore presence-absence data for each of the forty 0.3x0.3 grid cell (frugivore_extant_extinct_in_grid03.csv) Extant and extinct frugivore dispersal-related trait data (frugivore_traits.csv): Body mass in kilograms, hand-wing index (HWI) and home range in hectares. Geographic coordinates in Latitude and Longitude decimal degrees for the centroids of each of the forty 0.3x0.3 grid cell (centroids_grid03.csv) Shapefile of the forty 0.3x0.3 grid cell created in QGIS 3.10.7 used to extract all the other values (0.3grid_20records) Metadata Average climatic, soil and human variables per grid cell (Environment_grid03.csv) BIO1: Annual mean temperature (°C x 10) BIO4: Temperature seasonality (standard deviation ×100) BIO6: Minimum temperature of the coldest month (°C x 10) BIO12: Annual mean precipitation (mm x month-1) pet: Annual potential evapotranspiration from the Thornthwaite equation (mm) cwd: Annual climatic water deficit (mm) alt: Altitude (in m) slop: Slope in degrees solar: Solar radiation (in Wh.m-2.day-1) percfor2010: Madagascar's forest in 2010 was derived from the 30 m resolution 2000 forest map by Harper et al. (2007). Clay: Soil clay content (0-2 micrometre) in g/100g (w%) CationEC: Cation exchange capacity (CEC measured in 1 M NH4OAc buffered at pH 7) in cmolc/kg (fine earth) Extractable_Aluminum: Extractable aluminium content (Al measured by Mehlich 3) in mg/kg (fine earth) Total_Nitrogen: Total nitrogen (N) content in g/kg of the fine earth fraction Total_Phosphorus: Total Phosphorus (P) content of the soil fine earth fraction in mg/kg (ppm) Popdensity2010: "For all locations with more than 1000 people per km−2, we assigned a pressure score of 10. For more sparsely populated areas with densities lower than 1000 people·km−2, we logarithmically scaled the pressure score using: Pressure score = 3.333 × log(populationdensity+1)" (Venter et al. 2016). HFP2009: Human footprint for 2009, calculated as a summary value from other several human-related variables such as built environments, population density, night-time lights, croplands, pasture, roads, railways, navigable waterways. Roads: "We mapped the direct and indirect influence of roads by assigning a pressure score of 8 for 0.5 km out for either side of roads, and access pressures were awarded a score of 4 at 0.5 km and decaying exponentially out to 15 km either side of the road" (Venter et al. 2016) Funding provided by: Deutsche ForschungsgemeinschaftCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001659Award Number: DFG–FZT 118Funding provided by: Deutsche ForschungsgemeinschaftCrossref Funder Registry ID: http://dx.doi.org/10.13039/501100001659Award Number: 202548816Please refer to the Methods section and Supplementary Information of the published article

Species diversity and growth forms in tropical american palm communities

To advance our understanding of the processes that govern the assembly of palm communities and the local coexistence of numerous palm species, we here synthesize available information in the literature on species diversity and growth-form composition in palm communities across the Americas. American palm communities surveyed had 4-48 (median 16) species in study plots covering 0.09-7.2 ha. Climate, soils, hydrology, and topography are the main factors determining palm community species richness. Tropical lowland terra firme rain forests are the most species-rich whereas forests that are inundated or grow on sandy soils or in areas with seasonal climate have much fewer species. Palm communities in the central-western Amazon and in Central America are significantly richer than the average region and those in the Caribbean significantly poorer in species. As for branching, the 789 species of tropical American palms belong to Corner's model (solitary, 268 species, 33%), Tomlinsons model (cespitose, 521 species, 66%) and Schoute's model (dichotomous branching, three species, < 1%). We assigned the species to eight different growth forms: (i) Large tall-stemmed Palms (102 spp), (ii) Large-leaved medium-short-stemmed Palms (31 spp), (iii) Medium-sized Palms (95 spp), (iv) Medium/Small Palms with Stout Stem (42 spp), (v) Small Palms (423 spp), (vi) Large acaulescent Palms (28 spp), (vii) Small acaulescent Palms (56 spp), and (viii) Climbing Palms (12 spp). The eight growth forms are differently represented in the palm communities, and the categories Small Palms and Large tall-stemmed Palms dominate the communities both in terms of species richness and in number of individuals

Ecological traits influence the phylogenetic structure of bird species co-occurrences worldwide

The extent to which species’ ecological and phylogenetic relatedness shape their co-occurrence patterns at large spatial scales remains poorly understood. By quantifying phylogenetic assemblage structure within geographic ranges of >8000 bird species, we show that global co-occurrence patterns are linked - after accounting for regional effects - to key ecological traits reflecting diet, mobility, body size and climatic preference. We found that co-occurrences of carnivorous, migratory and cold-climate species are phylogenetically clustered, whereas nectarivores, herbivores, frugivores and invertebrate eaters tend to be more phylogenetically overdispersed. Preference for open or forested habitats appeared to be independent from the level of phylogenetic clustering. Our results advocate for an extension of the tropical niche conservatism hypothesis to incorporate ecological and life-history traits beyond the climatic niche. They further offer a novel species-oriented perspective on how biogeographic and evolutionary legacies interact with ecological traits to shape global patterns of species coexistence in birds