Seed dispersal modes play a crucial role in angiosperm migration, adaptation, and responses to climate change, yet their global spatiotemporal patterns and underlying drivers remain largely unexplored. Here, using a global dataset on seed dispersal modes (zoochory, anemochory, hydrochory, and autochory) of 35 131 angiosperm species, we provide a large-scale assessment of their evolutionary dynamics, diversification impact, and geographic variation. We found that the increase in zoochorous lineages began after c. 105 Ma, and the transition rate from abiotic-to-biotic dispersal strongly correlated with paleotemperature, being positive from 105 to 90 Ma and negative thereafter. However, contrary to previous hypotheses, we found no significant effect of seed dispersal mode on diversification rates across angiosperms. Spatially, the prevalence of zoochory declined, and that of autochory increased with latitude, both closely linked to contemporary temperature. Meanwhile, the frequency of zoochory and anemochory was positively associated with temperature anomalies since the Last Glacial Maximum, suggesting that dispersal modes facilitating long-distance dispersal are favored in climatically unstable regions. These findings highlight the key role of climate fluctuations in shaping the spatiotemporal patterns of angiosperm seed dispersal modes and suggest a more complex relationship between dispersal modes and angiosperm diversification than previously assumed.
Mountain regions harbor extraordinary biodiversity, yet the mechanisms underlying this pattern remain unclear. Here we use the phylogenetically and geographically replicated radiations of Berberis (barberries) in the Andes and Hengduan-Himalaya Mountains (HHM) to test how functional trait innovations, orogeny, and climate change influenced the buildup of species richness in each region. In barberries (Berberis), the successive evolution of deciduousness and small, densely-veined leaves enabled the lineage to take advantage of expanding alpine and subalpine habitats in the HHM during the Miocene. The resulting pulse in the origin of new species contrasts with the more modest rate of species accumulation in the Andes, where barberry species remained evergreen and the availability of high-elevation habitats was more limited. In this study, the phylogeny of barberries exemplifies context-dependent macroevolutionary dynamics, in which intrinsic innovations and extrinsic ecological opportunities interacted to generate exceptional plant diversity in a mountain hotspot.
Speciation shapes biodiversity, yet why some lineages diversify faster than others remains unclear. Theory predicts that traits promote ecological speciation through adaptation, but their evolvability ('trait flexibility') may be impacted by allometric and genomic constraints. Here we test this by integrating phylogenetic, trait and genome size data for palms (Arecaceae)-a large pantropical family (>2500 species) with 167-fold variation in certain traits (e.g. fruit size) and 60-fold genome size variation. Using structural equation modelling, we test three hypotheses: trait evolution promotes speciation (H1: trait flexibility hypothesis), and speciation and trait evolution rates are constrained by allometry (H2: allometric constraint hypothesis) and genome size (H3: large genome constraint hypothesis). We detected seven major speciation rate shifts during approximately 110-million-years of palm evolution. Tip-derived speciation rates increased with faster evolution in leaf size and plant height, supporting H1, whereas correlated evolution between all traits indirectly influenced speciation, supporting H2. Large genomes were associated with decreased plant height and stem diameter evolution rates supporting H3, but the genome size-speciation association was sensitive to phylogenetic autocorrelation. Our findings illustrate how the interplay between genome size, allometry and trait evolvability affect speciation, emphasizing the importance of holistic approaches for uncovering general mechanisms driving speciation throughout the Tree of Life.
The evolutionary arms race between plants and herbivores led to numerous plant adaptations, including spinescence. However, the balance between herbivory and abiotic conditions in the evolution of spinescence remains unclear. We integrated phylogenetic, geographic, and trait data for 2686 species of an ecologically diverse and spinescent pantropical lineage, mimosoid legumes, with distribution data on 368 extant and extinct mammalian herbivores ≥ 10 kg. Using structural equation models, we assessed how herbivores, climate, soil, and fire directly and indirectly affected the proportion of spinescent mimosoids across global and continental assemblages. Models incorporating extinct herbivore assemblages explained more variation in the proportion of spiny species than those based solely on extant herbivores. Dry-season length and soil pH increased spinescence both directly and indirectly through their effects on herbivore richness. These abiotic effects exceeded herbivore effects at continental scales. Fire influenced spinescence only indirectly via its positive relationship with herbivore richness. Finally, spinescence evolved repeatedly across mimosoids from c. 35 million years ago, pre-dating the Miocene savanna expansion. Our study suggests that past herbivore communities have left a lasting imprint on present-day plant defence patterns and that long-term climatic transitions and the emergence of open, herbivore-rich landscapes played crucial roles in the evolution and distribution of spinescence.
ABSTRACT Neotropical seasonally dry biomes are amongst the world's most threatened ecosystems and are predicted to lose more biodiversity with climate change. The capacity of natural populations to respond to these changes depends on their genetic variation, but is poorly understood in most Neotropical seasonally dry forest species. Here, we used genome‐wide single nucleotide polymorphism (SNP) data for 109 individuals across 12 Colombian populations of Enterolobium cyclocarpum, a widespread deciduous legume tree found in seasonally dry tropical forests, human‐disturbed and open landscapes from Central and Northern South America, to (1) explore population structure across the landscape, (2) determine local adaptation to heat and drought stress, and (3) assess genomic offset and adaptive potential under future climate change. Our results suggest clear genomic differentiation among regions and populations, as well as an uneven spatial distribution of adaptive alleles associated with drought and heat stress, together suggesting different degrees of local adaptation to climate across the landscape. Furthermore, all regions investigated (i.e., Caribbean, inter‐Andean valleys, and Orinoquía) showed limited adaptive potential under future climate change scenarios. For some regions, gene flow may help buffer the effects of environmental change by bringing in adaptive alleles, however, this will likely be insufficient to counteract predicted mal‐adaptation in certain regions, such as in the Orinoquía. Our results suggest that both barriers to gene flow (e.g., orography) and varying heat and drought stress conditions have shaped the genomic composition and adaptive potential of the species. Enterolobium cyclocarpum populations have adapted locally to current climate, but this adaptation may not be sufficient to cope with future climate change, particularly where population connectivity is low. Our findings have relevance for the conservation of species in highly threatened Neotropical biomes, such as seasonally dry tropical forests, which are expected to experience rising temperatures and greater drought under future climate change.
Invasive plant species present a growing ecological and economic challenge, and often adapt rapidly to their novel environments through complex demographic and evolutionary processes. Invasion genomics offers powerful tools to disentangle these processes, but most studies rely on geographically narrow sampling across native and non-native ranges. Erigeron canadensis is a cosmopolitan weed native to North America that has successfully invaded diverse climates worldwide. We used double-digest restriction site-associated DNA sequencing (ddRADseq) to investigate the genetic diversity and structure of 280 E. canadensis populations across the Northern Hemisphere. We found that native and non-native populations maintained comparable genetic diversity. Population structure analyses revealed four genetic clusters that were mainly differentiated along latitudinal and aridity gradients. However, one cluster was strongly overrepresented in the non-native compared to the native range. In the native range, genetic differentiation was shaped by spatial and environmental gradients, while in non-native regions human-mediated dispersal and repeated introductions disrupted environmentally driven genetic structure. Migration network analyses revealed limited intercontinental connectivity and a possible role of long-distance dispersal in within-range expansions. Genomic offset analyses showed that genotype-environment mismatches in non-native populations associated with reduced growth and reproduction. Together, our results indicate that the invasion dynamics of E. canadensis were driven by multiple introductions, population admixture, and lineage sorting, while some genotypes contributed disproportionately to the spread of this invader. The presence of apparent maladaptation suggests that even long-established invaders may still be evolving in response to their novel environment, raising concerns about potential future expansions.
Aim Long distance dispersal and the ability to delay germination under unfavourable conditions (dormancy) are critical for plant persistence and range expansion. However, how dispersal syndrome and dormancy interactively shape maximum dispersal distance and species range size across climate regions remains unclear. We tested the hypothesis that a trade-off between dormancy and dispersal distance operates differently in animal-mediated versus abiotic dispersal systems, and that climate modulates their influence on range size.Location Global.Time Period Current.Major Taxa Studied Seed plants.Methods We compiled data on dormancy, dispersal syndrome, maximum seed dispersal distance and range size for 631 plant species across 118 families worldwide. We used linear mixed effects models to examine how dormancy and dispersal syndromes interactively shape seed dispersal distance and range size across tropical and temperate regions.Results Non-dormant species had larger maximum dispersal distances than dormant species, but only in abiotic dispersal systems, consistent with a trade-off between dispersal and persistence traits (dormancy). In contrast, animal-mediated dispersal led to larger dispersal distances than abiotic dispersal, regardless of whether species were dormant or not. The influence of dormancy and dispersal syndrome on range size was climate-dependent. In tropical regions, animal-mediated dispersal enhanced range size, while dormancy had little effect. In temperate regions, maximum seed dispersal distance was positively associated with range size, but neither dormancy nor animal-mediated dispersal significantly affected range size.Main Conclusions The interplay between seed dormancy and dispersal syndromes shapes seed dispersal distance and species range size in climate-specific ways. Animal-mediated dispersal promotes larger maximum dispersal distances and larger range sizes in tropical regions. In contrast, in abiotic dispersal systems, dormancy leads to relatively small dispersal distances, but dormancy itself does not affect range sizes in temperate or tropical regions. Understanding dispersal-dormancy dynamics is essential for predicting how plants will respond to environmental changes.
Functional traits are critical for understanding species interactions within ecosystems and their responses to environmental changes. Yet, traits related to fruits and seeds are still underrepresented, especially in tropical ecosystems where mutualisms between fruits and fruit-eating animals are prominent. Here, we introduce AnnonFruitTraits 1.0, a comprehensive dataset of 34,772 records encompassing 26 frugivory-related traits for 2,266 species (ca. 90% of total species) of the pantropical plant family Annonaceae (Magnoliales). This dataset includes trait definitions and their significance for frugivory, as well as a description of our workflow from data acquisition to visualization. To facilitate data accessibility and reproducibility, we provide an accompanying R package (AnnonTraits) that enables users to explore, summarise, and visualise the dataset. By assessing species and trait coverage across genera and regions, we identified major data gaps in the Asia-Pacific region and in several Annonaceae genera (e.g., Artabotrys , Miliusa , Orophea, Polyalthia , and Uvaria ). Our findings show the importance of expanding trait data collection and taxonomic efforts, particularly in underrepresented regions and lineages. AnnonFruitTraits is a valuable resource for advancing research on seed dispersal, plant–animal interactions, and tropical forest conservation.
Studying the interaction between macroevolutionary and ecological factors is critical for understanding the principles of diversity regulation and predicting the effects of human activities. Here, we use the geological chronology of the Hawaiian archipelago as a testbed to examine the interaction between island age and climatic factors (i.e., precipitation) on contemporary patterns of tree taxonomic diversity. To this end, we estimated patterns of tree species diversity from 375 forest plots spread across steep precipitation gradients and different substrate ages on a younger island (Hawai‘i; ~ 0.5 million years old), an intermediate-aged island (Maui Nui complex; ~ 2 million years old), and an older island (O‘ahu; ~ 3 million years old). We found a clear positive relationship between precipitation and diversity on the oldest island (O‘ahu), but no such relationship on the two younger islands (islands in the Maui Nui complex and Hawai‘i). We also found high species turnover between drier and wetter environments on the oldest island, which suggests ecological specialization on these habitat types, but not on the younger islands. However, when we included plots that were highly invaded by alien species, the effect varied and precipitation had a larger effect on diversity and turnover on the younger islands. This could be because the younger islands may be more vulnerable to invasions. Our results suggest that the response of diversity to climate variation differs substantially across the Hawaiian Islands, possibly because of differences in the age of the islands; however, biological invasions are degrading this signature. Local diversity responses to a steep precipitation gradient are stronger on older Hawaiian Islands, likely due to longer timescales for macroevolutionary processes. Species turnover to distinct precipitation conditions varies across islands of the Hawaiian archipelago, with older islands exhibiting greater precipitation-driven ecological specialization. Alien species alter local diversity responses to precipitation, particularly on the youngest island of the archipelago. The presence of alien species is modifying the pattern of species turnover across distinct precipitation conditions, with dry and mesic habitats on intermediate-age islands showing higher species turnover. Biological invasions are currently reshaping plant diversity patterns in the Hawaiian archipelago.
Understanding the processes that drive phenotypic diversification and underpin speciation is key to elucidating how biodiversity has evolved. Although these processes have been studied across a wide array of clades, adaptive radiations (ARs), which are systems with multiple closely related species and broad phenotypic diversity, have been particularly fruitful for teasing apart the factors that drive and constrain diversification. As such, ARs have become popular candidate study systems for determining the extent to which ecological features, including aspects of organisms and the environment, and inter- and intraspecific interactions, led to evolutionary diversification. Despite substantial past empirical and theoretical work, understanding mechanistically how ARs evolve remains a major challenge. Here, we highlight a number of understudied components of the environment and of lineages themselves, which may help further our understanding of speciation and AR. We also outline some substantial remaining challenges to achieving a detailed understanding of adaptation, speciation, and the role of ecology in these processes. These major challenges include identifying factors that have a causative impact in promoting or constraining ARs, gaining a more holistic understanding of features of organisms and their environment that interact resulting in adaptation and speciation, and understanding whether the role of these organismal and environmental features varies throughout the radiation process. We conclude by providing perspectives on how future investigations into the AR process can overcome these challenges, allowing us to glean mechanistic insights into adaptation and speciation.
More than 40 thousand species of plants and animals are facing extinction worldwide. Range size is one of the strongest determinants of extinction risk, but the causes underlying the wide variation in natural range sizes remain poorly understood. Here, we investigate how species' age is related to present-day range size for over 26,000 species of mammals, birds, reptiles, amphibians, reef fishes, and plants. We show that, on average, older species have larger ranges across all groups except for marine mammals, but the strength of the age-range size relationship depends on taxonomic scale. Furthermore, while our results confirm the well-established pattern of smaller range sizes for species restricted to islands (compared to mainland) or with limited dispersal abilities (compared to good dispersers), we show that the correlation between species age and range size is stronger in these groups, suggesting that island dynamics and dispersal ability modulate this relationship. Our study reveals that species with small ranges, and thus increased extinction risk, tend to be restricted to islands, are poor dispersers, or have recently evolved.
The elemental content of organisms links cellular biochemistry to ecological processes, from physiology to nutrient dynamics. While plant stoichiometry is thought to vary with climate and nutrient availability across latitudes, the consistency of these patterns across trophic groups and realms remains unclear. Using the StoichLife database, which includes nitrogen and phosphorus content data for 5443 species across 1390 sites, we examine how solar energy (temperature, radiation) and nutrients (nitrogen and phosphorus) influence stoichiometric variation. We find that plant stoichiometry in terrestrial and freshwater ecosystems is more strongly associated with environmental gradients, particularly nitrogen deposition, than animal stoichiometry. Contrary to expectations, temperature, radiation, and labile P show limited global effects. Latitudinal patterns in stoichiometry are more closely associated with species turnover rather than intraspecific variation. Given the strong links between stoichiometry and organismal performance, these findings underscore the need to predict the ecological consequences of anthropogenic disruption to global biogeochemical cycles. Organisms vary in their nitrogen and phosphorus content, shaping ecological and evolutionary processes. This study shows that nitrogen deposition is a consistent global factor associated with plant and animal stoichiometry.
Ongoing declines of large-bodied frugivores limit the dispersal of large-seeded plants, contributing to their (local) demise and 'downsizing' of seeds across assemblages. However, the extent to which human pressure leads to contemporary seed downsizing, and whether extinct megafrugivores have left imprints on seed size, remains unclear. Here, we integrate trait and distribution data for 2852 endozoochorous plant species, 48 extant and 15 extinct frugivore species across 361 assemblages on Madagascar. Using structural equation models, we show that assemblages with higher human footprint, a cumulative index of human pressure, have smaller maximum seed sizes, especially through downsizing of extant frugivores. Furthermore, among assemblages with 'mega-seeded' plants (i.e., seeds that cannot be swallowed by any extant Malagasy frugivore), larger seed sizes are associated with larger past megafrugivores, reflecting the legacy of past interactions. Human-driven seed downsizing highlights broader implications in erosions of important ecosystem functions such as forest carbon storage.
Angiosperms are the most diverse and abundant plant taxon today and dominate the majority of Earth's terrestrial ecosystems. They underwent rapid divergence and biogeographic expansion from the early to the middle Cretaceous. Yet, transformative ecosystem change brought about by the increased ecological dominance of angiosperms unfolded progressively until the Late Cretaceous. After the Cretaceous-Paleogene (K-Pg) boundary, angiosperms restructured terrestrial ecosystems towards a modern form. By the Neogene, crown groups that make up modern terrestrial angiosperm biodiversity radiated, and regional floristic distinctions were established concurrently with the steepened latitudinal and vertical temperature gradients. Here, we summarize, based on fossils and molecular evidence, when and how angiosperms came to diversify, dominate, and shape terrestrial ecosystems, leading to the emergence and spread of angiosperm-dominated floras. We highlight five major phases of angiosperm evolution that took place against a background of palaeogeography and climate changes. There is a consistent delay in ecological dominance after lineage origination and taxonomic diversification, as a result of which angiosperms did not achieve ecological dominance across terrestrial biomes in a single step. The patterns of diversity seen among extant angiosperms, the dominant angiosperm groups within modern ecosystems, and the restriction of different groups of angiosperms to different parts of the world, reflect the contingent nature of the process of lineage diversification in the context of long-term, substantial and ongoing environmental change. Determining the origins, diversification, and ecological dominance of angiosperms continues to be a challenge and requires elucidation of their early forms, functions, habitats, and environmental interactions throughout evolutionary history.
Past megafaunal extinctions and ongoing declines of remaining large-bodied frugivores limit the dispersal of large-seeded plants, contributing to their (local) demise, thereby ‘downsizing’ plant seeds across assemblages. Here, we test this hypothesis by integrating trait and distribution data for 2,852 endozoochorous plant species, 48 extant and 15 extinct frugivore species across 361 assemblages on Madagascar. Using structural equation models, we show that mega-seeded plants – with seeds that are too large to be swallowed by any extant Malagasy frugivore – have larger seeds in assemblages where past megafrugivores were larger, highlighting the legacy of past interactions on persisting mega-seeded plants. Furthermore, human footprint reduces seed sizes directly and indirectly by downsizing of extant frugivore in the assemblages. Such human-driven seed downsizing can lead to erosions of important ecosystem functions such as tropical forest carbon storage. ### Competing Interest Statement The authors have declared no competing interest.
Defaunation of large-bodied animals threatens essential ecosystem functions, such as seed dispersal. However, the consequences of this human-induced downsizing of animal communities for plant-frugivore trait matching-the alignment between frugivory-related plant traits (e.g., fruit size) and frugivore traits (e.g., body mass)-remain unquantified at macroecological scales. Here, we examine how human disturbance and environmental conditions influence trait matching in tropical plant-frugivore networks. We compiled fruit size data for 1927 plant species from primary sources, along with body mass and dietary information for 1120 frugivorous animal species (birds, mammals and reptiles), and integrated these with 12,708 plant-frugivore interactions recorded across 102 networks. Using fourth-corner analyses and structural equation models (SEMs), we quantified how human disturbance and environmental conditions directly and indirectly affected trait matching strength (fruit-size-to-body-mass correlation) across networks. SEMs revealed that human disturbance weakened trait matching by reducing the range of frugivore body masses within networks, whereas wet and productive environments promoted a higher proportion of fruit in frugivore diets, leading to stronger trait matching. Our results demonstrate that human disturbance weakens plant-frugivore trait matching through the downsizing of animal communities, thereby providing a quantitative assessment of the decoupling of coevolved relationships between fruiting plants and their animal seed dispersers.