Diversity, phylogeny and evolution of the rapidly evolving genus Psidium L. (Myrtaceae, Myrteae).

BACKGROUND AND AIMS: Psidium is the fourthth largest genus of Myrtaceae in the Neotropics. Psidium guajava is widely cultivated in the tropics for its edible fruit. It is commercially under threat due to the disease guava decline. Psidium cattleyanum is one of the 100 most invasive organisms in the world. Knowledge of the phylogenetic relationships within Psidium is poor. We aim to provide a review of the biology, morphology and ecology of Psidium, a phylogenetic tree, an infrageneric classification and a list of species. METHODS: Morphological and geographic data were obtained by studying Psidium in herbaria and in the field between 1988 and 2020. Forty-six herbaria were visited personally. A database of approx. 6000 specimens was constructed, and the literature was reviewed. Thirty species (about a third of the species in the genus) were sampled for molecular phylogenetic inference. Two chloroplast (psbA-trnH and ndhF) and two nuclear (external transcribed spacer and internal transcribed spacer) regions were targeted. Phylogenetic trees were constructed using maximum likelihood (ML; RaxML) and Bayesian inference (BI; MrBayes). KEY RESULTS: Psidium is a monophyletic genus with four major clades recognized as sections. Section Psidium (ten species), to which P. guajava belongs, is sister to the rest of the genus; it is widespread across the Neotropics. Section Obversifolia (six species; restricted to the Brazilian Atlantic Forest), which includes P. cattleyanum, is sister to the innermost clade composed of sister sections Apertiflora (31 species; widespread but most diverse in the Brazilian Atlantic Forest) + Mitranthes (26 species; widespread in dry forests and probably diverse in the Caribbean). Characters associated with diversification within Psidium are discussed. CONCLUSIONS: Research on pre-foliation, colleters, leaf anatomy, leaf physiology, staminal development, placentation and germination associated with the anatomy of the opercular plug is desirable. Studies are biased towards sections Psidium and Obversifolia, with other sections poorly known.

Phylogeny and biogeography of Myrcia sect. Aguava (Myrtaceae, Myrteae) based on phylogenomic and Sanger data provide evidence for a Cerrado origin and geographically structured clades.

Myrcia is one of the largest exclusively Neotropical angiosperm genera, including ca. 800 species divided into nine sections. Myrcia sect. Aguava is one of most complex sections of Myrcia due to high morphological variation and wide distribution range of some species, including M. guianensis, with distribution throughout South America and a complex taxonomic history. We used complete plastid DNA sequences data generated using next-generation sequencing of 45 terminals, mostly from Myrcia sect. Aguava. These data were combined with five target DNA regions (ITS, psbA-trnH, trnL-trnF, trnQ-rps16, ndhF) of additional terminals to increase taxonomic coverage. Phylogenetic analyses were conducted using a maximum likelihood approach, and divergence times and ancestral range distributions were estimated. Myrcia sect. Aguava is monophyletic and exclusively comprises species with trilocular ovaries but has no relationship with other groups within Myrcia that possess trilocular ovaries. Three main lineages that correspond to geographical distribution are recognized within Myrcia sect. Aguava. Multiple accessions reveal a non-monophyletic Myrcia guianensis and stress the biogeographical structure inside the group. Myrcia sect. Aguava had a probable mid-Miocene origin in the Cerrado, but lineages that persisted there diversified only more recently, when the present-day vegetation started to stabilize. Posterior migrations to Atlantic Forest, Amazon and Caribbean occurred at the end of Miocene, evidencing transitions from open and dry to forested and more humid areas that are less frequent in the Neotropics. Overall, it is observed that related lineages remained in ecologically similar environments. Future perspectives on Myrcia and Myrteae in the phylogenomic era are also discussed.

Harnessing the potential of integrated systematics for conservation of taxonomically complex, megadiverse plant groups.

The value of natural history collections for conservation science research is increasingly recognized, despite their well-documented limitations in terms of taxonomic, geographic, and temporal coverage. Specimen-based analyses are particularly important for tropical plant groups for which field observations are scarce and potentially unreliable due to high levels of diversity-amplifying identification challenges. Specimen databases curated by specialists are rich sources of authoritatively identified, georeferenced occurrence data, and such data are urgently needed for large genera. We compared entries in a monographic database for the large Neotropical genus Myrcia in 2007 and 2017. We classified and quantified differences in specimen records over this decade and determined the potential impact of these changes on conservation assessments. We distinguished misidentifications from changes due to taxonomic remodeling and considered the effects of adding specimens and georeferences. We calculated the potential impact of each change on estimates of extent of occurrence (EOO), the most frequently used metric in extinction-risk assessments of tropical plants. We examined whether particular specimen changes were associated with species for which changes in EOO over the decade were large enough to change their conservation category. Corrections to specimens previously misidentified or lacking georeferences were overrepresented in such species, whereas changes associated with taxonomic remodeling (lumping and splitting) were underrepresented. Among species present in both years, transitions to less threatened status outnumbered those to more threatened (8% vs 3%, respectively). Species previously deemed data deficient transitioned to threatened status more often than to not threatened (10% vs 7%, respectively). Conservation scientists risk reaching unreliable conclusions if they use specimen databases that are not actively curated to reflect changing knowledge.

Empleo del Potencial de la Sistemática Integrada para la Conservación de Grupos Botánicos Complejos y Megadiversos Resumen Cada vez se reconoce más el valor que tienen las colecciones de historia natural para la investigación dentro de la ciencia de la conservación, a pesar de las limitaciones en la documentación adecuada de la cobertura taxonómica, geográfica y temporal. Los análisis con base en especímenes son de particular importancia en los grupos de plantas tropicales, para los cuales las observaciones en el campo son escasas y potencialmente de poca confianza debido la gran cantidad de retos de identificación que amplifican la diversidad. Las bases de datos de especímenes que son curadas por especialistas son fuentes abundantes de datos identificados autoritativamente y de distribución georeferenciada, por lo que es urgente la necesidad de dichos datos para géneros extensos. Comparamos las entradas en una base de datos monográfica para el género neotropical extenso Myrcia en 2007 y en 2017. Clasificamos y cuantificamos las diferencias en los registros de especímenes durante esta década y determinamos el impacto potencial de estos cambios sobre las evaluaciones de conservación. Separamos las identificaciones erróneas de los cambios causados por la remodelación taxonómica y consideramos los efectos de la adición de especímenes y de georeferencias. Calculamos el impacto potencial de cada cambio sobre las estimaciones de la extensión de la distribución (EOO, en inglés), la medida que se utiliza con mayor frecuencia en las valoraciones del riesgo de extinción de las plantas tropicales. Examinamos si los cambios en un espécimen particular estuvieron asociados con especies para las cuales los cambios en la EOO durante la década fueron lo suficientemente amplios para cambiarles la categoría de conservación. Las correcciones hechas a especímenes previamente mal identificados o carentes de georeferencias estuvieron sobre-representadas en dichas especies, mientras que los cambios asociados con la remodelación taxonómica (agrupamiento y separación) estuvieron sub-representados. Entre las especies presentes en ambos años, las transiciones hacia un estado de conservación con menor amenaza superaron en cantidad a aquellas hacia un estado de mayor amenaza (8% vs 3%, respectivamente). Las especies que con anterioridad se clasificaban como deficientes de datos tuvieron más transiciones hacia el estado de amenazadas que hacia el estado de no amenazadas (10% vs 7%, respectivamente). Los científicos de la conservación corren el riesgo de llegar a conclusiones poco confiables si utilizan bases de datos de especímenes que no sean actualizadas para reflejar el conocimiento cambiante.

Floral heterochrony promotes flexibility of reproductive strategies in the morphologically homogeneous genus Eugenia (Myrtaceae).

Background and Aims: Comparative floral ontogeny represents a valuable tool to understand angiosperm evolution. Such an approach may elucidate subtle changes in development that discretely modify floral architecture and underlie reproductive lability in groups with superficial homogeneous morphology. This study presents a comparative survey of floral development in Eugenia (Myrtaceae), one of the largest genera of angiosperms, and shows how previously undocumented ontogenetic trends help to explain the evolution of its megadiversity in contrast to its apparent flower uniformity. Methods: Using scanning electron microscopy, selected steps of the floral ontogeny of a model species (Eugenia punicifolia) are described and compared with 20 further species representing all ten major clades in the Eugenia phylogenetic tree. Additional floral trait data are contrasted for correlation analysis and character reconstructions performed against the Myrtaceae phylogenetic tree. Key results: Eugenia flowers show similar organ arrangement patterns: radially symmetrical, (most commonly) tetramerous flowers with variable numbers of stamens and ovules. Despite a similar general organization, heterochrony is evident from size differences between tissues and structures at similar developmental stages. These differences underlie variable levels of investment in protection, subtle modifications to symmetry, herkogamic effects and independent androecium and gynoecium variation, producing a wide spectrum of floral display and contributing to fluctuations in fitness. During Eugenia's bud development, the hypanthium (as defined here) is completely covered by stamen primordia, unusual in other Myrtaceae. This is the likely plesiomorphic state for Myrteae and may have represented a key evolutionary novelty in the tribe. Conclusions: Floral evolution in Eugenia depends on heterochronic patterns rather than changes in complexity to promote flexibility in floral strategies. The successful early establishment of Myrteae, previously mainly linked to the key innovation of fleshy fruit, may also have benefitted from changes in flower structure.

Myrteae phylogeny, calibration, biogeography and diversification patterns: Increased understanding in the most species rich tribe of Myrtaceae.

Myrteae (c. 2500 species; 51 genera) is the largest tribe of Myrtaceae and an ecologically important groups of angiosperms in the Neotropics. Systematic relationships in Myrteae are complex, hindering conservation initiatives and jeopardizing evolutionary modelling. A well-supported and robust phylogenetic hypothesis was here targeted towards a comprehensive understanding of the relationships within the tribe. The resultant topology was used as a base for key evolutionary analyses such as age estimation, historical biogeography and diversification rate patterns. One nuclear (ITS) and seven chloroplast (psbA-trnH, matK, ndhF, trnl-trnF, trnQ-rps16, rpl16 and rpl32-trnL) DNA regions for 115 taxa representing 46 out of the 51 genera in the tribe were accessed and analysed using maximum likelihood and Bayesian inference tools for phylogenetic reconstruction. Dates of diversification events were estimated and contrasted using two distinct fossil sets (macro and pollen) in BEAST. The subsequent dated phylogenies were compared and analysed for biogeographical patterns using BioGeoBEARS and diversification rates using BAMM. Myrteae phylogeny presents strong statistical support for three major clades within the tribe: Australasian group, Myrtus group and Main Neotropical Lineage. Dating results from calibration using macrofossil are an average of 20 million years older and show an early Paleocene origin of Myrteae, against a mid-Eocene one from the pollen fossil calibration. Biogeographic analysis shows the origin of Myrteae in Zealandia in both calibration approaches, followed by a widespread distribution throughout the still-linked Gondwana continents and diversification of Neotropical endemic lineages by later vicariance. Best configuration shift indicates three points of acceleration in diversification rates, all of them occurring in the Main Neotropical Lineage. Based on the reconstructed topology, several new taxonomic placements were recovered, including: the relative position of Myrtus communis, the placement of the Blepharocalyx group, the absence of generic endemism in the Caribbean, and the paraphyletism of the former Pimenta group. Distinct calibration approaches affect biogeography interpretation, increasing the number of necessary long distance dispersal events in the topology with older nodes. It is hypothesised that biological intrinsic factors such as modifications of embryo type and polyploidy might have played a role in accelerating shifts of diversification rates in Neotropical lineages. Future perspectives include formal subtribal classification, standardization of fossil calibration approaches and better links between diversification shifts and trait evolution.

The evolutionary history of Eugenia sect. Phyllocalyx (Myrtaceae) corroborates historically stable areas in the southern Atlantic forests.

BACKGROUND AND AIMS: Eugenia sect. Phyllocalyx Nied. includes 14 species endemic to the Neotropics, mostly distributed in the Atlantic coastal forests of Brazil. Here the first comprehensive phylogenetic study of this group is presented, and this phylogeny is used as the basis to evaluate the recent infrageneric classification in Eugenia sensu lato (s.l.) to test the history of the evolution of traits in the group and test hypotheses associated with the history of this clade. METHODS: A total of 42 taxa were sampled, of which 14 were Eugenia sect. Phyllocalyx for one nuclear (ribosomal internal transcribed spacer) and four plastid markers (psbA-trnH, rpl16, trnL-rpl32 and trnQ-rps16). The relationships were reconstructed based on Bayesian analysis and maximum likelihood. Additionally, ancestral area analysis and modelling methods were used to estimate species dispersal, comparing historically climatic stable (refuges) and unstable areas. KEY RESULTS: Maximum likelihood and Bayesian inferences indicate that Eugenia sect. Phyllocalyx is paraphyletic and the two clades recovered are characterized by combinations of morphological characters. Phylogenetic relationships support a link between Cerrado and south-eastern species and a difference in the composition of species from north-eastern and south-eastern Atlantic forest. Refugia and stable areas identified within unstable areas suggest that these areas were important to maintain diversity in the Atlantic forest biodiversity hotspot. CONCLUSION: This study provides a robust phylogenetic framework to address important historical questions for Eugenia s.l. within an evolutionary context, supporting the need for better taxonomic study of one of the largest genera in the Neotropics. Furthermore, valuable insight is offered into diversification and biome shifts of plant species in the highly environmentally impacted Atlantic forest of South America. Evidence is presented that climate stability in the south-eastern Atlantic forest during the Quaternary contributed to the highest levels of plant diversity in this region that acted as a refugium.

Botanical Monography in the Anthropocene.

Unprecedented changes in the Earth's biota are prompting urgent efforts to describe and conserve plant diversity. For centuries, botanical monographs - comprehensive systematic treatments of a family or genus - have been the gold standard for disseminating scientific information to accelerate research. The lack of a monograph compounds the risk that undiscovered species become extinct before they can be studied and conserved. Progress towards estimating the Tree of Life and digital information resources now bring even the most ambitious monographs within reach. Here, we recommend best practices to complete monographs urgently, especially for tropical plant groups under imminent threat or with expected socioeconomic benefits. We also highlight the renewed relevance and potential impact of monographies for the understanding, sustainable use, and conservation of biodiversity.

Evolution of exceptional species richness among lineages of fleshy-fruited Myrtaceae.

BACKGROUND AND AIMS: The angiosperm family Myrtaceae comprises 17 tribes with more than half of the estimated 5500 species being referred to the fleshy-fruited and predominantly rainforest associated Syzygieae and Myrteae. Previous studies suggest that fleshy fruits have evolved separately in these lineages, whereas generally shifts in fruit morphology have been variously implicated in diversification rate shifts among angiosperms. A phylogenetic hypothesis and estimate divergence times for Myrtaceae is developed as a basis to explore the evidence for, and drivers of, elevated diversification rates among the fleshy-fruited tribes of Myrtaceae. METHODS: Bayesian phylogenetic analyses of plastid and nuclear DNA sequences were used to estimate intertribal relationships and lineage divergence times in Myrtaceae. Focusing on the fleshy-fruited tribes, a variety of statistical approaches were used to assess diversification rates and diversification rate shifts across the family. KEY RESULTS: Analyses of the sequence data provide a strongly supported phylogenetic hypothesis for Myrtaceae. Relative to previous studies, substantially younger ages for many of the clades are reported, and it is argued that the use of flexible calibrations to incorporate fossil data provides more realistic divergence estimates than the use of errorless point calibrations. It is found that Syzygieae and Myrteae have experienced elevated diversification rates relative to other lineages of Myrtaceae. Positive shifts in diversification rate have occurred separately in each lineage, associated with a shift from dry to fleshy fruit. CONCLUSIONS: Fleshy fruits have evolved independently in Syzygieae and Myrteae, and this is accompanied by exceptional diversification rate shifts in both instances, suggesting that the evolution of fleshy fruits is a key innovation for rainforest Myrtaceae. Noting the scale dependency of this hypothesis, more complex explanations may be required to explain diversification rate shifts occurring within the fleshy-fruited tribes, and the suggested phylogenetic hypothesis provides an appropriate framework for this undertaking.

Nomenclatural and taxonomic updates in Rourea subgen. Rourea sect. Multifoliolatae (Connaraceae).

The pantropical genus Rourea Aubl. (Connaraceae) is composed of ca. 70 species, most of which occur in the Neotropics. Rourea is currently subdivided into three subgenera, with the American taxa included in Rourea subgen. Rourea. Forero (1976) recognised six sections for the species of the New World, with Rourea subgen. R. sect. Multifoliolatae being exclusive to Brazil, characterised by multifoliolate leaves, relatively small leaflets and the staminal tube (0.8-)1-1.5 mm long. Following Forero's (1976) treatment, additional botanical collections have become available in Brazilian herbaria, allowing re-evaluation of species concepts. This work recognises and revises 12 species in this section, mainly restricted to southeastern Brazil and southern Bahia. A nomenclatural and taxonomic study of these species is here presented, including an identification key, morphological descriptions, illustrations and geographic distribution maps. A new species is also described.

Plant diversity hotspots in the Atlantic coastal forests of Brazil.

Plant-diversity hotspots on a global scale are well established, but smaller local hotspots within these must be identified for effective conservation of plants at the global and local scales. We used the distributions of endemic and endemic-threatened species of Myrtaceae to indicate areas of plant diversity and conservation importance within the Atlantic coastal forests (Mata Atlântica) of Brazil. We applied 3 simple, inexpensive geographic information system (GIS) techniques to a herbarium specimen database: predictive species-distribution modeling (Maxent); complementarity analysis (DIVA-GIS); and mapping of herbarium specimen collection locations. We also considered collecting intensity, which is an inherent limitation of use of natural history records for biodiversity studies. Two separate areas of endemism were evident: the Serra do Mar mountain range from Paraná to Rio de Janeiro and the coastal forests of northern Espírito Santo and southern Bahia. We identified 12 areas of approximately 35 km(2) each as priority areas for conservation. These areas had the highest species richness and were highly threatened by urban and agricultural expansion. Observed species occurrences, species occurrences predicted from the model, and results of our complementarity analysis were congruent in identifying those areas with the most endemic species. These areas were then prioritized for conservation importance by comparing ecological data for each.

The use and misuse of herbarium specimens in evaluating plant extinction risks.

Herbarium specimens provide verifiable and citable evidence of the occurrence of particular plants at particular points in space and time, and are vital resources for assessing extinction risk in the tropics, where plant diversity and threats to plants are greatest. We reviewed approaches to assessing extinction risk in response to the Convention on Biological Diversity's Global Strategy for Plant Conservation Target 2: an assessment of the conservation status of all known plant species by 2020. We tested five alternative approaches, using herbarium-derived data for trees, shrubs and herbs in five different plant groups from temperate and tropical regions. All species were previously fully assessed for the IUCN Red List. We found significant variation in the accuracy with which different approaches classified species as threatened or not threatened. Accuracy was highest for the machine learning model (90%) but the least data-intensive approach also performed well (82%). Despite concerns about spatial, temporal and taxonomic biases and uncertainties in herbarium data, when specimens represent the best available evidence for particular species, their use as a basis for extinction risk assessment is appropriate, necessary and urgent. Resourcing herbaria to maintain, increase and disseminate their specimen data is essential to guide and focus conservation action.This article is part of the theme issue 'Biological collections for understanding biodiversity in the Anthropocene'.

Circumscription and synopsis of Eugenia section Speciosae Bünger & Mazine (Myrtaceae).

A new section of Eugenia (Myrtaceae) is described, segregate from Eugenia sect. Phyllocalyx. Phylogenetic studies suggest that Eugenia sect. Phyllocalyx as traditionally delimited is paraphyletic. To maintain the monophyly of each of the sections in Eugenia s.l., we herein opt to circumscribe a new section and recognize six taxa in sect. Speciosae, which has a distribution mostly in southeastern Brazil and northern South America. Nomenclatural notes are made and a taxonomic key is provided for the species of the section.