From genome size to trait evolution during angiosperm radiation.

Angiosperm diversity arises from trait flexibility and repeated evolutionary radiations, but the role of genomic characters in these radiations remains unclear. In this opinion article, we discuss how genome size can influence angiosperm diversification via its intricate link with cell size, tissue packing, and physiological processes which, in turn, influence the macroevolution of functional traits. We propose that integrating genome size, functional traits, and phylogenetic data across a wide range of lineages allows us to test whether genome size decrease consistently leads to increased trait flexibility, while genome size increase constrains trait evolution. Combining theories from molecular biology, functional ecology and macroevolution, we provide a framework to better understand the role of genome size in trait evolution, evolutionary radiations, and the global distribution of angiosperms.

The evolution of insular woodiness.

Insular woodiness (IW)-the evolutionary transition from herbaceousness toward woodiness on islands-is one of the most iconic features of island floras. Since pioneering work by Darwin and Wallace, a number of drivers of IW have been proposed, such as 1) competition for sunlight requiring plants with taller and stronger woody stems and 2) drought favoring woodiness to safeguard root-to-shoot water transport. Alternatively, IW may be the indirect result of increased lifespan related to 3) a favorable aseasonal climate and/or 4) a lack of large native herbivores. However, information on the occurrence of IW is fragmented, hampering tests of these potential drivers. Here, we identify 1,097 insular woody species on 375 islands and infer at least 175 evolutionary transitions on 31 archipelagos, concentrated in six angiosperm families. Structural equation models reveal that the insular woody species richness on oceanic islands correlates with a favorable aseasonal climate, followed by increased drought and island isolation (approximating competition). When continental islands are also included, reduced herbivory pressure by large native mammals, increased drought, and island isolation are most relevant. Our results illustrate different trajectories leading to rampant convergent evolution toward IW and further emphasize archipelagos as natural laboratories of evolution, where similar abiotic or biotic conditions replicated evolution of similar traits.

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.

Earth history events shaped the evolution of uneven biodiversity across tropical moist forests.

Far from a uniform band, the biodiversity found across Earth's tropical moist forests varies widely between the high diversity of the Neotropics and Indomalaya and the relatively lower diversity of the Afrotropics. Explanations for this variation across different regions, the "pantropical diversity disparity" (PDD), remain contentious, due to difficulty teasing apart the effects of contemporary climate and paleoenvironmental history. Here, we assess the ubiquity of the PDD in over 150,000 species of terrestrial plants and vertebrates and investigate the relationship between the present-day climate and patterns of species richness. We then investigate the consequences of paleoenvironmental dynamics on the emergence of biodiversity gradients using a spatially explicit model of diversification coupled with paleoenvironmental and plate tectonic reconstructions. Contemporary climate is insufficient in explaining the PDD; instead, a simple model of diversification and temperature niche evolution coupled with paleoaridity constraints is successful in reproducing the variation in species richness and phylogenetic diversity seen repeatedly among plant and animal taxa, suggesting a prevalent role of paleoenvironmental dynamics in combination with niche conservatism. The model indicates that high biodiversity in Neotropical and Indomalayan moist forests is driven by complex macroevolutionary dynamics associated with mountain uplift. In contrast, lower diversity in Afrotropical forests is associated with lower speciation rates and higher extinction rates driven by sustained aridification over the Cenozoic. Our analyses provide a mechanistic understanding of the emergence of uneven diversity in tropical moist forests across 110 Ma of Earth's history, highlighting the importance of deep-time paleoenvironmental legacies in determining biodiversity patterns.

Africa as an evolutionary arena for large fruits.

Strong paleoclimatic change and few Late Quaternary megafauna extinctions make mainland Africa unique among continents. Here, we hypothesize that, compared with elsewhere, these conditions created the ecological opportunity for the macroevolution and geographic distribution of large fruits. We assembled global phylogenetic, distribution and fruit size data for palms (Arecaceae), a pantropical, vertebrate-dispersed family with > 2600 species, and integrated these with data on extinction-driven body size reduction in mammalian frugivore assemblages since the Late Quaternary. We applied evolutionary trait, linear and null models to identify the selective pressures that have shaped fruit sizes. We show that African palm lineages have evolved towards larger fruit sizes and exhibited faster trait evolutionary rates than lineages elsewhere. Furthermore, the global distribution of the largest palm fruits across species assemblages was explained by occurrence in Africa, especially under low canopies, and extant megafauna, but not by mammalian downsizing. These patterns strongly deviated from expectations under a null model of stochastic (Brownian motion) evolution. Our results suggest that Africa provided a distinct evolutionary arena for palm fruit size evolution. We argue that megafaunal abundance and the expansion of savanna habitat since the Miocene provided selective advantages for the persistence of African plants with large fruits.

When lizards shift to a more plant-based lifestyle: The macroevolution of mutualistic lizard-plant-interactions (Squamata: Sauria/Lacertilia).

Pollination and seed dispersal of plants by animals are key mutualistic processes for the conservation of plant diversity and ecosystem functioning. Although different animals frequently act as pollinators or seed dispersers, some species can provide both functions, so-called 'double mutualists', suggesting that the evolution of pollination and seed dispersal may be linked. Here, we assess the macroevolution of mutualistic behaviours in lizards (Lacertilia) by applying comparative methods to a phylogeny comprising 2,838 species. We found that both flower visitation (potential pollination; recorded in 64 species [2.3% of total] across 9 families) and seed dispersal (recorded in 382 species [13,5% of total] across 26 families) have evolved repeatedly in Lacertilia. Furthermore, we found that seed dispersal activity pre-dated flower visitation and that the evolution of seed dispersal activity and flower visitation was correlated, illustrating a potential evolutionary mechanism behind the emergence of double mutualisms. Finally, we provide evidence that lineages with flower visitation or seed dispersal activity have higher diversification rates than lineages lacking these behaviours. Our study illustrates the repeated innovation of (double) mutualisms across Lacertilia and we argue that island settings may provide the ecological conditions under which (double) mutualisms persist over macroevolutionary timescales.

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.

Understanding the relationship between dispersal and range size.

The drivers of variability in species range sizes remain an outstanding enigma in ecology. The theoretical expectation of a positive dispersal-range size relationship has received mixed empirical support, despite dispersal being one of the most prominent hypothesised predictors of range size. Here, we synthesised results from 86 studies examining the dispersal-range size relationship for plants and animals in marine, terrestrial and freshwater realms. Overall, our meta-analysis showed that dispersal positively affects range size, but its effect is dependent on the clade and dispersal proxy studied. Moreover, despite potential differences in habitat connectivity, we did not find an effect of realm on the dispersal-range size relationship. Finally, the strength of the dispersal-range size relationship was dependent on latitude, range size metric and the taxonomic breadth of the study clade. Our synthesis emphasizes the importance of developing a mechanistic understanding of the trait to dispersal to range size relationship, considering the complexity of dispersal departure, transfer and settlement, as well as evolutionary components such as time for range expansion, speciation and past geological-environmental dynamics. We, therefore, call for a more integrative view of the dispersal process and its causal relationship with range size.

The megaherbivore gap after the non-avian dinosaur extinctions modified trait evolution and diversification of tropical palms.

The Cretaceous-Palaeogene (K-Pg) extinction of the non-avian dinosaurs (66 Ma) led to a 25 million year gap of megaherbivores (>1000 kg) before the evolution of megaherbivorous mammals in the Late Eocene (40 Ma). The botanical consequences of this 'Palaeocene megaherbivore gap' (PMHG) remain poorly explored. We hypothesize that the absence of megaherbivores should result in changes in the diversification and trait evolution of associated plant lineages. We used phylogenetic time- and trait-dependent diversification models with palms (Arecaceae) and show that the PMHG was characterized by speciation slowdowns, decreased evolution of armature and increased evolution of megafaunal (≥4 cm) fruits. This suggests that the absence of browsing by megaherbivores during the PMHG may have led to a loss of defence traits, but the absence of megaherbivorous seed dispersers did not lead to a loss of megafaunal fruits. Instead, increases in PMHG fruit sizes may be explained by simultaneously rising temperatures, rainforest expansion, and the subsequent radiation of seed-dispersing birds and mammals. We show that the profound impact of the PMHG on plant diversification can be detected even with the overwriting of adaptations by the subsequent Late Eocene opening up of megaherbivore-associated ecological opportunities. Our study provides a quantitative, comparative framework to assess diversification and adaptation during one of the most enigmatic periods in angiosperm history.

Quantitative estimates of glacial refugia for chimpanzees (Pan troglodytes) since the Last Interglacial (120,000 BP).

Paleoclimate reconstructions have enhanced our understanding of how past climates have shaped present-day biodiversity. We hypothesize that the geographic extent of Pleistocene forest refugia and suitable habitat fluctuated significantly in time during the late Quaternary for chimpanzees (Pan troglodytes). Using bioclimatic variables representing monthly temperature and precipitation estimates, past human population density data, and an extensive database of georeferenced presence points, we built a model of changing habitat suitability for chimpanzees at fine spatio-temporal scales dating back to the Last Interglacial (120,000 BP). Our models cover a spatial resolution of 0.0467° (approximately 5.19 km2 grid cells) and a temporal resolution of between 1000 and 4000 years. Using our model, we mapped habitat stability over time using three approaches, comparing our modeled stability estimates to existing knowledge of Afrotropical refugia, as well as contemporary patterns of major keystone tropical food resources used by chimpanzees, figs (Moraceae), and palms (Arecacae). Results show habitat stability congruent with known glacial refugia across Africa, suggesting their extents may have been underestimated for chimpanzees, with potentially up to approximately 60,000 km2 of previously unrecognized glacial refugia. The refugia we highlight coincide with higher species richness for figs and palms. Our results provide spatio-temporally explicit insights into the role of refugia across the chimpanzee range, forming the empirical foundation for developing and testing hypotheses about behavioral, ecological, and genetic diversity with additional data. This methodology can be applied to other species and geographic areas when sufficient data are available.

Palm fruit colours are linked to the broad-scale distribution and diversification of primate colour vision systems.

A long-standing hypothesis in ecology and evolution is that trichromatic colour vision (the ability to distinguish red from green) in frugivorous primates has evolved as an adaptation to detect conspicuous (reddish) fruits. This could provide a competitive advantage over dichromatic frugivores which cannot distinguish reddish colours from a background of green foliage. Here, we test whether the origin, distribution and diversity of trichromatic primates is positively associated with the availability of conspicuous palm fruits, i.e. keystone fruit resources for tropical frugivores. We combine global data of colour vision, distribution and phylogenetic data for more than 400 primate species with fruit colour data for more than 1700 palm species, and reveal that species richness of trichromatic primates increases with the proportion of palm species that have conspicuous fruits, especially in subtropical African forests. By contrast, species richness of trichromats in Asia and the Americas is not positively associated with conspicuous palm fruit colours. Macroevolutionary analyses further indicate rapid and synchronous radiations of trichromats and conspicuous palms on the African mainland starting 10 Ma. These results suggest that the distribution and diversification of African trichromatic primates is strongly linked to the relative availability of conspicuous (versus non-conspicuous) palm fruits, and that interactions between primates and palms are related to the coevolutionary dynamics of primate colour vision systems and palm fruit colours.

Darwin's second 'abominable mystery': trait flexibility as the innovation leading to angiosperm diversity.

The fact that angiosperms are so species-rich and ecologically diverse - Darwin's second abominable mystery - could be explained by their ability to 'reinvent' themselves by evolving functional traits repeatedly over time, space and taxonomic clades. These trait innovations may facilitate adaptation and increase diversification rates. In this article, I quantify this 'trait flexibility' by reviewing the literature on trait transition rates and trait-dependent diversification rates in angiosperms and their extant sister clade, acrogymnosperms. I show that angiosperms indeed evolved elevated trait transition and trait-dependent diversification rates compared to gymnosperms, and rates are highest within species-rich angiosperm orders (e.g. Fabales, Lamiales). The (genetic) ability of certain angiosperm lineages to repeatedly evolve adaptive traits may have facilitated sustained high net diversification resulting from numerous episodic radiations.

Polyploidy promotes species diversification of Allium through ecological shifts.

Despite the role of polyploidy in multiple evolutionary processes, its impact on plant diversification remains controversial. An increased polyploid frequency may facilitate speciation through shifts in ecology, morphology or both. Here we used Allium to evaluate: (1) the relationship between intraspecific polyploid frequency and species diversification rate; and (2) whether this process is associated with habitat and/or trait shifts. Using eight plastid and nuclear ribosomal markers, we built a phylogeny of 448 Allium species, representing 46% of the total. We quantified intraspecific ploidy diversity, heterogeneity in diversification rates and their relationship along the phylogeny using trait-dependent diversification models. Finally, we evaluated the association between polyploidisation and habitat or trait shifts. We detected high ploidy diversity in Allium and a polyploidy-related diversification rate shift with a probability of 95% in East Asia. Allium lineages with high polyploid frequencies had higher species diversification rates than those of diploids or lineages with lower polyploid frequencies. Shifts in speciation rates were strongly correlated with habitat shifts linked to particular soil conditions; 81.7% of edaphic variation could be explained by polyploidisation. Our study emphasises the role of intraspecific polyploid frequency combined with ecological drivers on Allium diversification, which may explain plant radiations more generally.

Associated evolution of fruit size, fruit colour and spines in Neotropical palms.

Understanding how ecological interactions have shaped the evolutionary dynamics of species traits remains a challenge in evolutionary ecology. Combining trait evolution models and phylogenies, we analysed the evolution of characters associated with seed dispersal (fruit size and colour) and herbivory (spines) in Neotropical palms to infer the role of these opposing animal-plant interactions in driving evolutionary patterns. We found that the evolution of fruit colour and fruit size was associated in Neotropical palms, supporting the adaptive interpretation of seed-dispersal syndromes and highlighting the role of frugivores in shaping plant evolution. Furthermore, we revealed a positive association between fruit size and the presence of spines on palm leaves, bracteas and stems. We hypothesize that interactions between palms and large-bodied frugivores/herbivores may explain the evolutionary relationship between fruit size and spines. Large-bodied frugivores, such as extinct megafauna, besides consuming the fruits and dispersing large seeds, may also have consumed the leaves or damaged the plants, thus simultaneously favouring the evolution of large fruits and defensive structures. Our findings show how current trait patterns can be understood as the result of the interplay between antagonistic and mutualistic interactions that have happened throughout the evolutionary history of a clade.

Estimating divergence times and ancestral breeding systems in Ficus and Moraceae.

Background and Aims: Although dioecy, which characterizes only 6 % of angiosperm species, has been considered an evolutionary dead end, recent studies have demonstrated that this is not necessarily the case. Moraceae (40 genera, 1100 spp., including Ficus, 750 spp.) are particularly diverse in breeding systems (including monoecy, gynodioecy, androdioecy and dioecy) and thus represent a model clade to study macroevolution of dioecy. Methods: Ancestral breeding systems of Ficus and Moraceae were inferred. To do so, a new dated phylogenetic tree of Ficus and Moraceae was first reconstructed by combining a revised 12-fossil calibration set and a densely sampled molecular data set of eight markers and 320 species. Breeding system evolution was then reconstructed using both parsimony and model-based (maximum likelihood and Bayesian) approaches with this new time scale. Key Results: The crown group ages of Ficus and Moraceae were estimated in the Eocene (40.6-55.9 Ma) and Late Cretaceous (73.2-84.7 Ma), respectively. Strong support was found for ancestral dioecy in Moraceae. Although the ancestral state of Ficus remained particularly sensitive to model selection, the results show that monoecy and gynodioecy evolved from dioecy in Moraceae, and suggest that gynodioecy probably evolved from monoecy in Ficus. Conclusions: Dioecy was found not to be an evolutionary dead end in Moraceae. This study provides a new time scale for the phylogeny and a new framework of breeding system evolution in Ficus and Moraceae.

To adapt or go extinct? The fate of megafaunal palm fruits under past global change.

Past global change may have forced animal-dispersed plants with megafaunal fruits to adapt or go extinct, but these processes have remained unexplored at broad spatio-temporal scales. Here, we combine phylogenetic, distributional and fruit size data for more than 2500 palm (Arecaceae) species in a time-slice diversification analysis to quantify how extinction and adaptation have changed over deep time. Our results indicate that extinction rates of palms with megafaunal fruits have increased in the New World since the onset of the Quaternary (2.6 million years ago). In contrast, Old World palms show a Quaternary increase in transition rates towards evolving small fruits from megafaunal fruits. We suggest that Quaternary climate oscillations and concurrent habitat fragmentation and defaunation of megafaunal frugivores in the New World have reduced seed dispersal distances and geographical ranges of palms with megafaunal fruits, resulting in their extinction. The increasing adaptation to smaller fruits in the Old World could reflect selection for seed dispersal by ocean-crossing frugivores (e.g. medium-sized birds and bats) to colonize Indo-Pacific islands against a background of Quaternary sea-level fluctuations. Our macro-evolutionary results suggest that megafaunal fruits are increasingly being lost from tropical ecosystems, either due to extinctions or by adapting to smaller fruit sizes.

Vanishing refuge? Testing the forest refuge hypothesis in coastal East Africa using genome-wide sequence data for seven amphibians.

High-throughput sequencing data have greatly improved our ability to understand the processes that contribute to current biodiversity patterns. The "vanishing refuge" diversification model is speculated for the coastal forests of eastern Africa, whereby some taxa have persisted and diversified between forest refugia, while others have switched to becoming generalists also present in non-forest habitats. Complex arrangements of geographical barriers (hydrology and topography) and ecological gradients between forest and non-forest habitats may have further influenced the region's biodiversity, but elucidation of general diversification processes has been limited by lack of suitable data. Here, we explicitly test alternative diversification modes in the coastal forests using genome-wide single nucleotide polymorphisms, mtDNA, spatial and environmental data for three forest (Arthroleptis xenodactyloides, Leptopelis flavomaculatus and Afrixalus sylvaticus) and four generalist (Afrixalus fornasini, A. delicatus, Leptopelis concolor and Leptopelis argenteus) amphibians. Multiple analyses provide insight about divergence times, spatial population structure, dispersal barriers, environmental stability and demographic history. We reveal highly congruent intra-specific diversity and population structure across taxa, with most divergences occurring during the late Pliocene and Pleistocene. Although stability models support the existence of some forest refugia, dispersal barriers and demographic models point towards idiosyncratic diversification modes across taxa. We identify a consistent role for riverine barriers in the diversification of generalist taxa, but mechanisms of diversification are more complex for forest taxa and potentially include topographical barriers, forest refugia and ecological gradients. Our work demonstrates the complexity of diversification processes in this region, which vary between forest and generalist taxa, but also for ecologically similar species with shared population boundaries.

Multiple shifts to different pollinators fuelled rapid diversification in sexually deceptive Ophrys orchids.

Episodes of rapid speciation provide unique insights into evolutionary processes underlying species radiations and patterns of biodiversity. Here we investigated the radiation of sexually deceptive bee orchids (Ophrys). Based on a time-calibrated phylogeny and by means of ancestral character reconstruction and divergence time estimation, we estimated the tempo and mode of this radiation within a state-dependent evolutionary framework. It appears that, in the Pleistocene, the evolution of Ophrys was marked by episodes of rapid diversification coinciding with shifts to different pollinator types: from wasps to Eucera bees to Andrena and other bees. An abrupt increase in net diversification rate was detected in three clades. Among these, two phylogenetically distant lineages switched from Eucera to Andrena and other bees in a parallel fashion and at about the same time in their evolutionary history. Lack of early radiation associated with the evolution of the key innovation of sexual deception suggests that Ophrys diversification was mainly driven by subsequent ecological opportunities provided by the exploitation of novel pollinator groups, encompassing many bee species slightly differing in their sex pheromone communication systems, and by spatiotemporal fluctuations in the pollinator mosaic.