Environmental DNA recovers fish composition turnover of the coral reefs of West Indian Ocean islands.

Islands have been used as model systems to study ecological and evolutionary processes, and they provide an ideal set-up for validating new biodiversity monitoring methods. The application of environmental DNA metabarcoding for monitoring marine biodiversity requires an understanding of the spatial scale of the eDNA signal, which is best tested in island systems. Here, we investigated the variation in Actinopterygii and Elasmobranchii species composition recovered from eDNA metabarcoding along a gradient of distance-to-reef in four of the five French Scattered Islands in the Western Indian Ocean. We collected surface water samples at an increasing distance from reefs (0 m, 250 m, 500 m, 750 m). We used a metabarcoding protocol based on the 'teleo' primers to target marine reef fishes and classified taxa according to their habitat types (benthic or pelagic). We investigated the effect of distance-to-reef on ß diversity variation using generalised linear mixed models and estimated species-specific distance-to-reef effects using a model-based approach for community data. Environmental DNA metabarcoding analyses recovered distinct fish species compositions across the four inventoried islands and variations along the distance-to-reef gradient. The analysis of ß-diversity variation showed significant taxa turnover between the eDNA samples on and away from the reefs. In agreement with a spatially localised signal from eDNA, benthic species were distributed closer to the reef than pelagic ones. Our findings demonstrate that the combination of eDNA inventories and spatial modelling can provide insights into species habitat preferences related to distance-to-reef gradients at a small scale. As such, eDNA can not only recover large compositional differences among islands but also help understand habitat selection and distribution of marine species at a finer spatial scale.

Using ancient sedimentary DNA to forecast ecosystem trajectories under climate change.

Ecosystem response to climate change is complex. In order to forecast ecosystem dynamics, we need high-quality data on changes in past species abundance that can inform process-based models. Sedimentary ancient DNA (sedaDNA) has revolutionised our ability to document past ecosystems' dynamics. It provides time series of increased taxonomic resolution compared to microfossils (pollen, spores), and can often give species-level information, especially for past vascular plant and mammal abundances. Time series are much richer in information than contemporary spatial distribution information, which have been traditionally used to train models for predicting biodiversity and ecosystem responses to climate change. Here, we outline the potential contribution of sedaDNA to forecast ecosystem changes. We showcase how species-level time series may allow quantification of the effect of biotic interactions in ecosystem dynamics, and be used to estimate dispersal rates when a dense network of sites is available. By combining palaeo-time series, process-based models, and inverse modelling, we can recover the biotic and abiotic processes underlying ecosystem dynamics, which are traditionally very challenging to characterise. Dynamic models informed by sedaDNA can further be used to extrapolate beyond current dynamics and provide robust forecasts of ecosystem responses to future climate change. This article is part of the theme issue 'Ecological novelty and planetary stewardship: biodiversity dynamics in a transforming biosphere'.

Recurrent gene flow events occurred during the diversification of clownfishes of the skunk complex.

Clownfish (subfamily Amphiprioninae) are an iconic group of coral reef fish that evolved a mutualistic interaction with sea anemones, which triggered the adaptive radiation of the clade. Within clownfishes, the "skunk complex" is particularly interesting. Besides ecological speciation, interspecific gene flow and hybrid speciation are thought to have shaped the evolution of the group. We investigated the mechanisms characterizing the diversification of this complex. By taking advantage of their disjunct geographical distribution, we obtained whole-genome data of sympatric and allopatric populations of the three main species of the complex (Amphiprion akallopisos, A. perideraion and A. sandaracinos). We examined population structure, genomic divergence and introgression signals and performed demographic modelling to identify the most realistic diversification scenario. We excluded scenarios of strict isolation or hybrid origin of A. sandaracinos. We discovered moderate gene flow from A. perideraion to the ancestor of A. akallopisos + A. sandaracinos and weak gene flow between the species in the Indo-Australian Archipelago throughout the diversification of the group. We identified introgressed regions in A. sandaracinos and detected in A. perideraion two large regions of high divergence from the two other species. While we found that gene flow has occurred throughout the species' diversification, we also observed that recent admixture was less pervasive than initially thought, suggesting a role of host repartition or behavioural barriers in maintaining the genetic identity of the species in sympatry.

Speed of thermal adaptation of terrestrial vegetation alters Earth's long-term climate.

Earth's long-term climate is driven by the cycling of carbon between geologic reservoirs and the atmosphere-ocean system. Our understanding of carbon-climate regulation remains incomplete, with large discrepancies remaining between biogeochemical model predictions and the geologic record. Here, we evaluate the importance of the continuous biological climate adaptation of vegetation as a regulation mechanism in the geologic carbon cycle since the establishment of forest ecosystems. Using a model, we show that the vegetation's speed of adaptation to temperature changes through eco-evolutionary processes can strongly influence global rates of organic carbon burial and silicate weathering. Considering a limited thermal adaptation capacity of the vegetation results in a closer balance of reconstructed carbon fluxes into and out of the atmosphere-ocean system, which is a prerequisite to maintain habitable conditions on Earth's surface on a multimillion-year timescale. We conclude that the long-term carbon-climate system is more sensitive to biological dynamics than previously expected, which may help to explain large shifts in Phanerozoic climate.

Escarpment evolution drives the diversification of the Madagascar flora.

Madagascar exhibits high endemic biodiversity that has evolved with sustained and stable rates of speciation over the past several tens of millions of years. The topography of Madagascar is dominated by a mountainous continental rift escarpment, with the highest plant diversity and rarity found along the steep, eastern side of this geographic feature. Using a process-explicit model, we show that precipitation-driven erosion and landward retreat of this high-relief topography creates transient habitat organization through multiple mechanisms, including catchment expansion, isolation of highland remnants, and formation of topographic barriers. Habitat isolation and reconnection on a million-year timescale serves as an allopatric speciation pump creating the observed biodiversity.

Contrasted host specificity of gut and endosymbiont bacterial communities in alpine grasshoppers and crickets.

Bacteria colonize the body of macroorganisms to form associations ranging from parasitic to mutualistic. Endosymbiont and gut symbiont communities are distinct microbiomes whose compositions are influenced by host ecology and evolution. Although the composition of horizontally acquired symbiont communities can correlate to host species identity (i.e. harbor host specificity) and host phylogeny (i.e. harbor phylosymbiosis), we hypothesize that the microbiota structure of vertically inherited symbionts (e.g. endosymbionts like Wolbachia) is more strongly associated with the host species identity and phylogeny than horizontally acquired symbionts (e.g. most gut symbionts). Here, using 16S metabarcoding on 336 guts from 24 orthopteran species (grasshoppers and crickets) in the Alps, we observed that microbiota correlated to host species identity, i.e. hosts from the same species had more similar microbiota than hosts from different species. This effect was ~5 times stronger for endosymbionts than for putative gut symbionts. Although elevation correlated with microbiome composition, we did not detect phylosymbiosis for endosymbionts and putative gut symbionts: closely related host species did not harbor more similar microbiota than distantly related species. Our findings indicate that gut microbiota of studied orthopteran species is more correlated to host identity and habitat than to the host phylogeny. The higher host specificity in endosymbionts corroborates the idea that-everything else being equal-vertically transmitted microbes harbor stronger host specificity signal, but the absence of phylosymbiosis suggests that host specificity changes quickly on evolutionary time scales.

Global multifaceted biodiversity patterns, centers, and conservation needs in angiosperms.

The Convention on Biological Diversity seeks to conserve at least 30% of global land and water areas by 2030, which is a challenge but also an opportunity to better preserve biodiversity, including flowering plants (angiosperms). Herein, we compiled a large database on distributions of over 300,000 angiosperm species and the key functional traits of 67,024 species. Using this database, we constructed biodiversity-environment models to predict global patterns of taxonomic, phylogenetic, and functional diversity in terrestrial angiosperms and provide a comprehensive mapping of the three diversity facets. We further evaluated the current protection status of the biodiversity centers of these diversity facets. Our results showed that geographical patterns of the three facets of plant diversity exhibited substantial spatial mismatches and nonoverlapping conservation priorities. Idiosyncratic centers of functional diversity, particularly of herbaceous species, were primarily distributed in temperate regions and under weaker protection compared with other biodiversity centers of taxonomic and phylogenetic facets. Our global assessment of multifaceted biodiversity patterns and centers highlights the insufficiency and unbalanced conservation among the three diversity facets and the two growth forms (woody vs. herbaceous), thus providing directions for guiding the future conservation of global plant diversity.

SWECO25: a cross-thematic raster database for ecological research in Switzerland.

Standard and easily accessible cross-thematic spatial databases are key resources in ecological research. In Switzerland, as in many other countries, available data are scattered across computer servers of research institutions and are rarely provided in standard formats (e.g., different extents or projections systems, inconsistent naming conventions). Consequently, their joint use can require heavy data management and geomatic operations. Here, we introduce SWECO25, a Swiss-wide raster database at 25-meter resolution gathering 5,265 layers. The 10 environmental categories included in SWECO25 are: geologic, topographic, bioclimatic, hydrologic, edaphic, land use and cover, population, transportation, vegetation, and remote sensing. SWECO25 layers were standardized to a common grid sharing the same resolution, extent, and geographic coordinate system. SWECO25 includes the standardized source data and newly calculated layers, such as those obtained by computing focal or distance statistics. SWECO25 layers were validated by a data integrity check, and we verified that the standardization procedure had a negligible effect on the output values. SWECO25 is available on Zenodo and is intended to be updated and extended regularly.

Transnational conservation to anticipate future plant shifts in Europe.

To meet the COP15 biodiversity framework in the European Union (EU), one target is to protect 30% of its land by 2030 through a resilient transnational conservation network. The European Alps are a key hub of this network hosting some of the most extensive natural areas and biodiversity hotspots in Europe. Here we assess the robustness of the current European reserve network to safeguard the European Alps' flora by 2080 using semi-mechanistic simulations. We first highlight that the current network needs strong readjustments as it does not capture biodiversity patterns as well as our conservation simulations. Overall, we predict a strong shift in conservation need through time along latitudes, and from lower to higher elevations as plants migrate upslope and shrink their distribution. While increasing species, trait and evolutionary diversity, migration could also threaten 70% of the resident flora. In the face of global changes, the future European reserve network will need to ensure strong elevation and latitudinal connections to complementarily protect multifaceted biodiversity beyond national borders.

Projection of current and future distribution of adaptive genetic units in an alpine ungulate.

Climate projections predict major changes in alpine environments by the end of the 21st century. To avoid climate-induced maladaptation and extinction, many animal populations will either need to move to more suitable habitats or adapt in situ to novel conditions. Since populations of a species exhibit genetic variation related to local adaptation, it is important to incorporate this variation into predictive models to help assess the ability of the species to survive climate change. Here, we evaluate how the adaptive genetic variation of a mountain ungulate-the Northern chamois (Rupicapra rupicapra)-could be impacted by future global warming. Based on genotype-environment association analyses of 429 chamois using a ddRAD sequencing approach, we identified genetic variation associated with climatic gradients across the European Alps. We then delineated adaptive genetic units and projected the optimal distribution of these adaptive groups in the future. Our results suggest the presence of local adaptation to climate in Northern chamois with similar genetic adaptive responses in geographically distant but climatically similar populations. Furthermore, our results predict that future climatic changes will modify the Northern chamois adaptive landscape considerably, with various degrees of maladaptation risk.

Novel community data in ecology-properties and prospects.

New technologies for monitoring biodiversity such as environmental (e)DNA, passive acoustic monitoring, and optical sensors promise to generate automated spatiotemporal community observations at unprecedented scales and resolutions. Here, we introduce 'novel community data' as an umbrella term for these data. We review the emerging field around novel community data, focusing on new ecological questions that could be addressed; the analytical tools available or needed to make best use of these data; and the potential implications of these developments for policy and conservation. We conclude that novel community data offer many opportunities to advance our understanding of fundamental ecological processes, including community assembly, biotic interactions, micro- and macroevolution, and overall ecosystem functioning.

Diversity across organisational scale emerges through dispersal ability and speciation dynamics in tropical fish.

BACKGROUND: Biodiversity exists at different levels of organisation: e.g. genetic, individual, population, species, and community. These levels of organisation all exist within the same system, with diversity patterns emerging across organisational scales through several key processes. Despite this inherent interconnectivity, observational studies reveal that diversity patterns across levels are not consistent and the underlying mechanisms for variable continuity in diversity across levels remain elusive. To investigate these mechanisms, we apply a spatially explicit simulation model to simulate the global diversification of tropical reef fishes at both the population and species levels through emergent population-level processes. RESULTS: We find significant relationships between the population and species levels of diversity which vary depending on both the measure of diversity and the spatial partitioning considered. In turn, these population-species relationships are driven by modelled biological trait parameters, especially the divergence threshold at which populations speciate. CONCLUSIONS: To explain variation in multi-level diversity patterns, we propose a simple, yet novel, population-to-species diversity partitioning mechanism through speciation which disrupts continuous diversity patterns across organisational levels. We expect that in real-world systems this mechanism is driven by the molecular dynamics that determine genetic incompatibility, and therefore reproductive isolation between individuals. We put forward a framework in which the mechanisms underlying patterns of diversity across organisational levels are universal, and through this show how variable patterns of diversity can emerge through organisational scale.

Freshwater fish diversity in the western Amazon basin shaped by Andean uplift since the Late Cretaceous.

South America is home to the highest freshwater fish biodiversity on Earth, and the hotspot of species richness is located in the western Amazon basin. The location of this hotspot is enigmatic, as it is inconsistent with the pattern observed in river systems across the world of increasing species richness towards a river's mouth. Here we investigate the role of river capture events caused by Andean mountain building and repeated episodes of flooding in western Amazonia in shaping the modern-day richness pattern of freshwater fishes in South America, and in Amazonia in particular. To this end, we combine a reconstruction of river networks since 80 Ma with a mechanistic model simulating dispersal, allopatric speciation and extinction over the dynamic landscape of rivers and lakes. We show that Andean mountain building and consequent numerous small river capture events in western Amazonia caused freshwater habitats to be highly dynamic, leading to high diversification rates and exceptional richness. The history of marine incursions and lakes, including the Miocene Pebas mega-wetland system in western Amazonia, played a secondary role.

The geography of climate and the global patterns of species diversity.

Climate's effect on global biodiversity is typically viewed through the lens of temperature, humidity and resulting ecosystem productivity1-6. However, it is not known whether biodiversity depends solely on these climate conditions, or whether the size and fragmentation of these climates are also crucial. Here we shift the common perspective in global biodiversity studies, transitioning from geographic space to a climate-defined multidimensional space. Our findings suggest that larger and more isolated climate conditions tend to harbour higher diversity and species turnover among terrestrial tetrapods, encompassing more than 30,000 species. By considering both the characteristics of climate itself and its geographic attributes, we can explain almost 90% of the variation in global species richness. Half of the explanatory power (45%) may be attributed either to climate itself or to the geography of climate, suggesting a nuanced interplay between them. Our work evolves the conventional idea that larger climate regions, such as the tropics, host more species primarily because of their size7,8. Instead, we underscore the integral roles of both the geographic extent and degree of isolation of climates. This refined understanding presents a more intricate picture of biodiversity distribution, which can guide our approach to biodiversity conservation in an ever-changing world.

Elevational Goldilocks zone underlies the exceptional diversity of a large lizard radiation (Liolaemus; Liolaemidae).

Mountains are among the most biodiverse regions on the planet, and how these landforms shape diversification through the interaction of biological traits and geo-climatic dynamics is integral to understanding global biodiversity. In this study, we investigate the dual roles of climate change and mountain uplift on the evolution of a hyper-diverse radiation, Liolaemus lizards, with a spatially explicit model of diversification using a reconstruction of uplift and paleotemperature in central and southern South America. The diversification model captures a hotspot for Liolaemus around 40°S in lineages with low-dispersal ability and narrow niche breadths. Under the model, speciation rates are highest in low latitudes (<35°S) and mid elevations (~1,000 m), while extinction rates are highest at higher latitudes (>35°S) and higher elevations (>2,000 m). Temperature change through the Cenozoic explained variation in speciation and extinction rates through time and across different elevational bands. Our results point to the conditions of mid elevations being optimal for diversification (i.e., Goldilocks Zone), driven by the combination of (1) a complex topography that facilitates speciation during periods of climatic change, and (2) a relatively moderate climate that enables the persistence of ectothermic lineages and buffers species from extinction.

New deep learning-based methods for visualizing ecosystem properties using environmental DNA metabarcoding data.

Environmental DNA (eDNA) metabarcoding provides an efficient approach for documenting biodiversity patterns in marine and terrestrial ecosystems. The complexity of these data prevents current methods from extracting and analyzing all the relevant ecological information they contain, and new methods may provide better dimensionality reduction and clustering. Here we present two new deep learning-based methods that combine different types of neural networks (NNs) to ordinate eDNA samples and visualize ecosystem properties in a two-dimensional space: the first is based on variational autoencoders and the second on deep metric learning. The strength of our new methods lies in the combination of two inputs: the number of sequences found for each molecular operational taxonomic unit (MOTU) detected and their corresponding nucleotide sequence. Using three different datasets, we show that our methods accurately represent several biodiversity indicators in a two-dimensional latent space: MOTU richness per sample, sequence α-diversity per sample, Jaccard's and sequence ß-diversity between samples. We show that our nonlinear methods are better at extracting features from eDNA datasets while avoiding the major biases associated with eDNA. Our methods outperform traditional dimension reduction methods such as Principal Component Analysis, t-distributed Stochastic Neighbour Embedding, Nonmetric Multidimensional Scaling and Uniform Manifold Approximation and Projection for dimension reduction. Our results suggest that NNs provide a more efficient way of extracting structure from eDNA metabarcoding data, thereby improving their ecological interpretation and thus biodiversity monitoring.

Catchment-based sampling of river eDNA integrates terrestrial and aquatic biodiversity of alpine landscapes.

Monitoring of terrestrial and aquatic species assemblages at large spatial scales based on environmental DNA (eDNA) has the potential to enable evidence-based environmental policymaking. The spatial coverage of eDNA-based studies varies substantially, and the ability of eDNA metabarcoding to capture regional biodiversity remains to be assessed; thus, questions about best practices in the sampling design of entire landscapes remain open. We tested the extent to which eDNA sampling can capture the diversity of a region with highly heterogeneous habitat patches across a wide elevation gradient for five days through multiple hydrological catchments of the Swiss Alps. Using peristaltic pumps, we filtered 60 L of water at five sites per catchment for a total volume of 1800 L. Using an eDNA metabarcoding approach focusing on vertebrates and plants, we detected 86 vertebrate taxa spanning 41 families and 263 plant taxa spanning 79 families across ten catchments. For mammals, fishes, amphibians and plants, the detected taxa covered some of the most common species in the region according to long-term records while including a few more rare taxa. We found marked turnover among samples from distinct elevational classes indicating that the biological signal in alpine rivers remains relatively localised and is not aggregated downstream. Accordingly, species compositions differed between catchments and correlated with catchment-level forest and grassland cover. Biomonitoring schemes based on capturing eDNA across rivers within biologically integrated catchments may pave the way toward a spatially comprehensive estimation of biodiversity.

Phytodiversity is associated with habitat heterogeneity from Eurasia to the Hengduan Mountains.

The geographic distribution of plant diversity matches the gradient of habitat heterogeneity from lowlands to mountain regions. However, little is known about how much this relationship is conserved across scales. Using the World Checklist of Vascular Plants and high-resolution biodiversity maps developed by species distribution models, we investigated the associations between species richness and habitat heterogeneity at the scales of Eurasia and the Hengduan Mountains (HDM) in China. Habitat heterogeneity explains seed plant species richness across Eurasia, but the plant species richness of 41/97 HDM families is even higher than expected from fitted statistical relationships. A habitat heterogeneity index combining growing degree days, site water balance, and bedrock type performs better than heterogeneity based on single variables in explaining species richness. In the HDM, the association between heterogeneity and species richness is stronger at larger scales. Our findings suggest that high environmental heterogeneity provides suitable conditions for the diversification of lineages in the HDM. Nevertheless, habitat heterogeneity alone cannot fully explain the distribution of species richness in the HDM, especially in the western HDM, and complementary mechanisms, such as the complex geological history of the region, may have contributed to shaping this exceptional biodiversity hotspot.

Leaf metabolic traits reveal hidden dimensions of plant form and function.

The metabolome is the biochemical basis of plant form and function, but we know little about its macroecological variation across the plant kingdom. Here, we used the plant functional trait concept to interpret leaf metabolome variation among 457 tropical and 339 temperate plant species. Distilling metabolite chemistry into five metabolic functional traits reveals that plants vary on two major axes of leaf metabolic specialization-a leaf chemical defense spectrum and an expression of leaf longevity. Axes are similar for tropical and temperate species, with many trait combinations being viable. However, metabolic traits vary orthogonally to life-history strategies described by widely used functional traits. The metabolome thus expands the functional trait concept by providing additional axes of metabolic specialization for examining plant form and function.

An updated floristic map of the world.

Floristic regions reflect the geographic organization of floras and provide essential tools for biological studies. Previous global floristic regions are generally based on floristic endemism, lacking a phylogenetic consideration that captures floristic evolution. Moreover, the contribution of tectonic dynamics and historical and current climate to the division of floristic regions remains unknown. Here, by integrating global distributions and a phylogeny of 12,664 angiosperm genera, we update global floristic regions and explore their temporal changes. Eight floristic realms and 16 nested sub-realms are identified. The previously-defined Holarctic, Neotropical and Australian realms are recognized, but Paleotropical, Antarctic and Cape realms are not. Most realms have formed since Paleogene. Geographic isolation induced by plate tectonics dominates the formation of floristic realms, while current/historical climate has little contribution. Our study demonstrates the necessity of integrating distributions and phylogenies in regionalizing floristic realms and the interplay of macroevolutionary and paleogeographic processes in shaping regional floras.