Landscape dynamics and diversification of the megadiverse South American freshwater fish fauna.

Landscape dynamics are widely thought to govern the tempo and mode of continental radiations, yet the effects of river network rearrangements on dispersal and lineage diversification remain poorly understood. We integrated an unprecedented occurrence dataset of 4,967 species with a newly compiled, time-calibrated phylogeny of South American freshwater fishes-the most species-rich continental vertebrate fauna on Earth-to track the evolutionary processes associated with hydrogeographic events over 100 Ma. Net lineage diversification was heterogeneous through time, across space, and among clades. Five abrupt shifts in net diversification rates occurred during the Paleogene and Miocene (between 30 and 7 Ma) in association with major landscape evolution events. Net diversification accelerated from the Miocene to the Recent (c. 20 to 0 Ma), with Western Amazonia having the highest rates of in situ diversification, which led to it being an important source of species dispersing to other regions. All regional biotic interchanges were associated with documented hydrogeographic events and the formation of biogeographic corridors, including the Early Miocene (c. 23 to 16 Ma) uplift of the Serra do Mar and Serra da Mantiqueira and the Late Miocene (c. 10 Ma) uplift of the Northern Andes and associated formation of the modern transcontinental Amazon River. The combination of high diversification rates and extensive biotic interchange associated with Western Amazonia yielded its extraordinary contemporary richness and phylogenetic endemism. Our results support the hypothesis that landscape dynamics, which shaped the history of drainage basin connections, strongly affected the assembly and diversification of basin-wide fish faunas.

Morphometrics and Phylogenomics of Coca (Erythroxylum spp.) Illuminate Its Reticulate Evolution, With Implications for Taxonomy.

South American coca (Erythroxylum coca and E. novogranatense) has been a keystone crop for many Andean and Amazonian communities for at least 8,000 years. However, over the last half-century, global demand for its alkaloid cocaine has driven intensive agriculture of this plant and placed it in the center of armed conflict and deforestation. To monitor the changing landscape of coca plantations, the United Nations Office on Drugs and Crime collects annual data on their areas of cultivation. However, attempts to delineate areas in which different varieties are grown have failed due to limitations around identification. In the absence of flowers, identification relies on leaf morphology, yet the extent to which this is reflected in taxonomy is uncertain. Here, we analyze the consistency of the current naming system of coca and its four closest wild relatives (the "coca clade"), using morphometrics, phylogenomics, molecular clocks, and population genomics. We include name-bearing type specimens of coca's closest wild relatives E. gracilipes and E. cataractarum. Morphometrics of 342 digitized herbarium specimens show that leaf shape and size fail to reliably discriminate between species and varieties. However, the statistical analyses illuminate that rounder and more obovate leaves of certain varieties could be associated with the subtle domestication syndrome of coca. Our phylogenomic data indicate extensive gene flow involving E. gracilipes which, combined with morphometrics, supports E. gracilipes being retained as a single species. Establishing a robust evolutionary-taxonomic framework for the coca clade will facilitate the development of cost-effective genotyping methods to support reliable identification.

Global variation in diversification rate and species richness are unlinked in plants.

Species richness varies immensely around the world. Variation in the rate of diversification (speciation minus extinction) is often hypothesized to explain this pattern, while alternative explanations invoke time or ecological carrying capacities as drivers. Focusing on seed plants, the world's most important engineers of terrestrial ecosystems, we investigated the role of diversification rate as a link between the environment and global species richness patterns. Applying structural equation modeling to a comprehensive distribution dataset and phylogenetic tree covering all circa 332,000 seed plant species and 99.9% of the world's terrestrial surface (excluding Antarctica), we test five broad hypotheses postulating that diversification serves as a mechanistic link between species richness and climate, climatic stability, seasonality, environmental heterogeneity, or the distribution of biomes. Our results show that the global patterns of species richness and diversification rate are entirely independent. Diversification rates were not highest in warm and wet climates, running counter to the Metabolic Theory of Ecology, one of the dominant explanations for global gradients in species richness. Instead, diversification rates were highest in edaphically diverse, dry areas that have experienced climate change during the Neogene. Meanwhile, we confirmed climate and environmental heterogeneity as the main drivers of species richness, but these effects did not involve diversification rates as a mechanistic link, calling for alternative explanations. We conclude that high species richness is likely driven by the antiquity of wet tropical areas (supporting the "tropical conservatism hypothesis") or the high ecological carrying capacity of warm, wet, and/or environmentally heterogeneous environments.

Patterns and drivers of heat production in the plant genus Amorphophallus.

Thermogenesis - the ability to generate metabolic heat - is much more common in animals than in plants, but it has been documented in several plant families, most prominently the Araceae. Metabolic heat is produced in floral organs during the flowering time (anthesis), with the hypothesised primary functions being to increase scent volatilisation for pollinator attraction, and/or to provide a heat reward for invertebrate pollinators. Despite in-depth studies on the thermogenesis of single species, no attempts have yet been made to examine plant thermogenesis across an entire clade. Here, we apply time-series clustering algorithms to 119 measurements of the full thermogenic patterns in inflorescences of 80 Amorphophallus species. We infer a new time-calibrated phylogeny of this genus and use phylogenetic comparative methods to investigate the evolutionary determinants of thermogenesis. We find striking phenotypic variation across the phylogeny, with heat production in multiple clades reaching up to 15°C, and in one case 21.7°C above ambient temperature. Our results show that the thermogenic capacity is phylogenetically conserved and is also associated with inflorescence thickness. Our study paves the way for further investigations of the eco-evolutionary benefits of thermogenesis in plants.

Two Major Extinction Events in the Evolutionary History of Turtles: One Caused by an Asteroid, the Other by Hominins.

AbstractWe live in a time of accelerated biological extinctions that has the potential to mirror past mass extinction events. However, the rarity of mass extinctions and the restructuring of diversity they cause complicate direct comparisons between the current extinction crisis and earlier events. Among animals, turtles (Testudinata) are one of few groups that have both a rich fossil record and sufficiently stable ecological and functional roles to enable meaningful comparisons between the end-Cretaceous mass extinction (∼66 Ma) and the ongoing wave of extinctions. Here we analyze the fossil record of the entire turtle clade and identify two peaks in extinction rates over their evolutionary history. The first coincides with the Cretaceous-Paleogene transition, reflecting patterns previously reported for other taxa. The second major extinction event started in the Pliocene and continues until now. This peak is detectable only for terrestrial turtles and started much earlier in Africa and Eurasia than elsewhere. On the basis of the timing, geography, and functional group of this extinction event, we postulate a link to co-occurring hominins rather than climate change as the cause. These results lend further support to the view that negative biodiversity impacts were already incurred by our ancestors and related lineages and demonstrate the severity of this continued impact through human activities.

Reliable biogeography requires fossils: insights from a new species-level phylogeny of extinct and living carnivores.

A central objective of historical biogeography is to understand where clades originated and how they moved across space and over time. However, given the dynamic history of ecosystem changes in response to climate change and geological events, the manifold long-distance dispersals over evolutionary timescales, and regional and global extinctions, it remains uncertain how reliable inferences based solely on extant taxa can be achieved. Using a novel species-level phylogeny of all known extant and extinct species of the mammalian order Carnivora and related extinct groups, we show that far more precise and accurate ancestral areas can be estimated by fully integrating extinct species into the analyses, rather than solely relying on extant species or identifying ancestral areas only based on the geography of the oldest fossils. Through a series of simulations, we further show that this conclusion is robust under realistic scenarios in which the unknown extinct taxa represent a biased subset of all extinct species. Our results highlight the importance of integrating fossil taxa into a phylogenetic framework to further improve our understanding of historical biogeography and reveal the dynamic dispersal and diversification history of carnivores.

Plant diversity darkspots for global collection priorities.

More than 15% of all vascular plant species may remain scientifically undescribed, and many of the > 350 000 described species have no or few geographic records documenting their distribution. Identifying and understanding taxonomic and geographic knowledge shortfalls is key to prioritising future collection and conservation efforts. Using extensive data for 343 523 vascular plant species and time-to-event analyses, we conducted multiple tests related to plant taxonomic and geographic data shortfalls, and identified 33 global diversity darkspots (those 'botanical countries' predicted to contain most undescribed and not yet recorded species). We defined priority regions for future collection according to several socio-economic and environmental scenarios. Most plant diversity darkspots are found within global biodiversity hotspots, with the exception of New Guinea. We identify Colombia, Myanmar, New Guinea, Peru, Philippines and Turkey as global collection priorities under all environmental and socio-economic conditions considered. Our study provides a flexible framework to help accelerate the documentation of global plant diversity for the implementation of conservation actions. As digitisation of the world's herbaria progresses, collection and conservation priorities may soon be identifiable at finer scales.

The origin and speciation of orchids.

Orchids constitute one of the most spectacular radiations of flowering plants. However, their origin, spread across the globe, and hotspots of speciation remain uncertain due to the lack of an up-to-date phylogeographic analysis. We present a new Orchidaceae phylogeny based on combined high-throughput and Sanger sequencing data, covering all five subfamilies, 17/22 tribes, 40/49 subtribes, 285/736 genera, and c. 7% (1921) of the 29 524 accepted species, and use it to infer geographic range evolution, diversity, and speciation patterns by adding curated geographical distributions from the World Checklist of Vascular Plants. The orchids' most recent common ancestor is inferred to have lived in Late Cretaceous Laurasia. The modern range of Apostasioideae, which comprises two genera with 16 species from India to northern Australia, is interpreted as relictual, similar to that of numerous other groups that went extinct at higher latitudes following the global climate cooling during the Oligocene. Despite their ancient origin, modern orchid species diversity mainly originated over the last 5 Ma, with the highest speciation rates in Panama and Costa Rica. These results alter our understanding of the geographic origin of orchids, previously proposed as Australian, and pinpoint Central America as a region of recent, explosive speciation.

Online tree expansion could help solve the problem of scalability in Bayesian phylogenetics.

Bayesian phylogenetics is now facing a critical point. Over the last 20 years, Bayesian methods have reshaped phylogenetic inference and gained widespread popularity due to their high accuracy, the ability to quantify the uncertainty of inferences and the possibility of accommodating multiple aspects of evolutionary processes in the models that are used. Unfortunately, Bayesian methods are computationally expensive, and typical applications involve at most a few hundred sequences. This is problematic in the age of rapidly expanding genomic data and increasing scope of evolutionary analyses, forcing researchers to resort to less accurate but faster methods, such as maximum parsimony and maximum likelihood. Does this spell doom for Bayesian methods? Not necessarily. Here, we discuss some recently proposed approaches that could help scale up Bayesian analyses of evolutionary problems considerably. We focus on two particular aspects: online phylogenetics, where new data sequences are added to existing analyses, and alternatives to Markov chain Monte Carlo (MCMC) for scalable Bayesian inference. We identify 5 specific challenges and discuss how they might be overcome. We believe that online phylogenetic approaches and Sequential Monte Carlo hold great promise and could potentially speed up tree inference by orders of magnitude. We call for collaborative efforts to speed up the development of methods for real-time tree expansion through online phylogenetics.

Global hotspots of plant phylogenetic diversity.

Regions harbouring high unique phylogenetic diversity (PD) are priority targets for conservation. Here, we analyse the global distribution of plant PD, which remains poorly understood despite plants being the foundation of most terrestrial habitats and key to human livelihoods. Capitalising on a recently completed, comprehensive global checklist of vascular plants, we identify hotspots of unique plant PD and test three hypotheses: (1) PD is more evenly distributed than species diversity; (2) areas of highest PD (often called 'hotspots') do not maximise cumulative PD; and (3) many biomes are needed to maximise cumulative PD. Our results support all three hypotheses: more than twice as many regions are required to cover 50% of global plant PD compared to 50% of species; regions that maximise cumulative PD substantially differ from the regions with outstanding individual PD; and while (sub-)tropical moist forest regions dominate across PD hotspots, other forest types and open biomes are also essential. Safeguarding PD in the Anthropocene (including the protection of some comparatively species-poor areas) is a global, increasingly recognised responsibility. Having highlighted countries with outstanding unique plant PD, further analyses are now required to fully understand the global distribution of plant PD and associated conservation imperatives across spatial scales.

Slow and steady wins the race: Diversification rate is independent from body size and lifestyle in Malagasy skinks (Squamata: Scincidae: Scincinae).

Most of the unique and diverse vertebrate fauna that inhabits Madagascar derives from in situ diversification from colonisers that reached this continental island through overseas dispersal. The endemic Malagasy Scincinae lizards are amongst the most species-rich squamate groups on the island. They colonised all bioclimatic zones and display many ecomorphological adaptations to a fossorial (burrowing) lifestyle. Here we propose a new phylogenetic hypothesis for their diversification based on the largest taxon sampling so far compiled for this group. We estimated divergence times and investigated several aspects of their diversification (diversification rate, body size and fossorial lifestyle evolution, and biogeography). We found that diversification rate was constant throughout most of the evolutionary history of the group, but decreased over the last 6-4 million years and independently from body size and fossorial lifestyle evolution. Fossoriality has evolved from fully quadrupedal ancestors at least five times independently, which demonstrates that even complex morphological syndromes - in this case involving traits such as limb regression, body elongation, modification of cephalic scalation, depigmentation, and eyes and ear-opening regression - can evolve repeatedly and independently given enough time and eco-evolutionary advantages. Initial diversification of the group likely occurred in forests, and the divergence of sand-swimmer genera around 20 Ma appears linked to a period of aridification. Our results show that the large phenotypic variability of Malagasy Scincinae has not influenced diversification rate and that their rich species diversity results from a constant accumulation of lineages through time. By compiling large geographic and trait-related datasets together with the computation of a new time tree for the group, our study contributes important insights on the diversification of Malagasy vertebrates.

Addressing chemical pollution in biodiversity research.

Climate change, biodiversity loss, and chemical pollution are planetary-scale emergencies requiring urgent mitigation actions. As these "triple crises" are deeply interlinked, they need to be tackled in an integrative manner. However, while climate change and biodiversity are often studied together, chemical pollution as a global change factor contributing to worldwide biodiversity loss has received much less attention in biodiversity research so far. Here, we review evidence showing that the multifaceted effects of anthropogenic chemicals in the environment are posing a growing threat to biodiversity and ecosystems. Therefore, failure to account for pollution effects may significantly undermine the success of biodiversity protection efforts. We argue that progress in understanding and counteracting the negative impact of chemical pollution on biodiversity requires collective efforts of scientists from different disciplines, including but not limited to ecology, ecotoxicology, and environmental chemistry. Importantly, recent developments in these fields have now enabled comprehensive studies that could efficiently address the manifold interactions between chemicals and ecosystems. Based on their experience with intricate studies of biodiversity, ecologists are well equipped to embrace the additional challenge of chemical complexity through interdisciplinary collaborations. This offers a unique opportunity to jointly advance a seminal frontier in pollution ecology and facilitate the development of innovative solutions for environmental protection.

Spiny but photogenic: Amateur sightings complement herbarium specimens to reveal the bioregions of cacti.

PREMISE: Cacti are characteristic elements of the Neotropical flora and of major interest for biogeographic, evolutionary, and ecological studies. We tested global biogeographic boundaries for Neotropical Cactaceae using specimen-based occurrences, coupled with data from visual observations, as a means to tackle the known collection biases in the family. METHODS: Species richness and record density were assessed for preserved specimens and human observations, and a bioregional scheme tailored to Cactaceae was produced using the interactive web application Infomap Bioregions, based on data from 261,272 point records cleaned through automated and manual steps. RESULTS: We found that areas in Mexico and southwestern USA, in eastern Brazil, and along the Andean region have the greatest density of records and the highest species richness. Human observations complement information from preserved specimens substantially, especially along the Andes. We propose 24 cactus bioregions, among which the most species-rich are northern Mexico/southwestern USA, central Mexico, southern central Mexico, Central America, Mexican Pacific coast, central and southern Andes, northwestern Mexico/extreme southwestern USA, southwestern Bolivia, northeastern Brazil, and Mexico/Baja California. CONCLUSIONS: The bioregionalization proposed shows biogeographic boundaries specific to cacti and can thereby aid further evolutionary, biogeographic, and ecological studies by providing a validated framework for further analyses. This classification builds upon, and is distinctive from, other expert-derived regionalization schemes for other taxa. Our results showcase how observation data, including citizen-science records, can complement traditional specimen-based data for biogeographic research, particularly for taxa with specific specimen collection and preservation challenges and those that are threatened or internationally protected.

The rise of angiosperms pushed conifers to decline during global cooling.

Competition among species and entire clades can impact species diversification and extinction, which can shape macroevolutionary patterns. The fossil record shows successive biotic turnovers such that a dominant group is replaced by another. One striking example involves the decline of gymnosperms and the rapid diversification and ecological dominance of angiosperms in the Cretaceous. It is generally believed that angiosperms outcompeted gymnosperms, but the macroevolutionary processes and alternative drivers explaining this pattern remain elusive. Using extant time trees and vetted fossil occurrences for conifers, we tested the hypotheses that clade competition or climate change led to the decline of conifers at the expense of angiosperms. Here, we find that both fossil and molecular data show high congruence in revealing 1) low diversification rates, punctuated by speciation pulses, during warming events throughout the Phanerozoic and 2) that conifer extinction increased significantly in the Mid-Cretaceous (100 to 110 Ma) and remained high ever since. Their extinction rates are best explained by the rise of angiosperms, rejecting alternative models based on either climate change or time alone. Our results support the hypothesis of an active clade replacement, implying that direct competition with angiosperms increased the extinction of conifers by pushing their remaining species diversity and dominance out of the warm tropics. This study illustrates how entire branches on the Tree of Life may actively compete for ecological dominance under changing climates.

Disproportionate extinction of South American mammals drove the asymmetry of the Great American Biotic Interchange.

The interchange between the previously disconnected faunas of North and South America was a massive experiment in biological invasion. A major gap in our understanding of this invasion is why there was a drastic increase in the proportion of mammals of North American origin found in South America. Four nonmutually exclusive mechanisms may explain this asymmetry: 1) Higher dispersal rate of North American mammals toward the south, 2) higher origination of North American immigrants in South America, 3) higher extinction of mammals with South American origin, and 4) similar dispersal rate but a larger pool of native taxa in North versus South America. We test among these mechanisms by analyzing ∼20,000 fossil occurrences with Bayesian methods to infer dispersal and diversification rates and taxonomic selectivity of immigrants. We find no differences in the dispersal and origination rates of immigrants. In contrast, native South American mammals show higher extinction. We also find that two clades with North American origin (Carnivora and Artiodactyla) had significantly more immigrants in South America than other clades. Altogether, the asymmetry of the interchange was not due to higher origination of immigrants in South America as previously suggested, but resulted from higher extinction of native taxa in southern South America. These results from one of the greatest biological invasions highlight how biogeographic processes and biotic interactions can shape continental diversity.

Phylogenetic and functional clustering illustrate the roles of adaptive radiation and dispersal filtering in jointly shaping late-Quaternary mammal assemblages on oceanic islands.

Islands frequently harbour unique assemblages of species, yet their ecological roles and differences are largely ignored in island biogeography studies. Here, we examine eco-evolutionary processes structuring mammal assemblages on oceanic islands worldwide, including all extant and extinct late-Quaternary mammal species. We find island mammal assemblages tend to be phylogenetically clustered (share more recent evolutionary histories), with clustering increasing with island area and isolation. We also observe that mammal assemblages often tend to be functionally clustered (share similar traits), but the strength of clustering is weak and generally independent from island area or isolation. These findings indicate the important roles of in situ speciation and dispersal filtering in shaping island mammal assemblages under pre-anthropogenic conditions, notably through adaptive radiation of a few clades (e.g. bats, with generally high dispersal abilities). Our study demonstrates that considering the functional and phylogenetic axes of diversity can better reveal the eco-evolutionary processes of island community assembly.

Molecular Clocks and Archeogenomics of a Late Period Egyptian Date Palm Leaf Reveal Introgression from Wild Relatives and Add Timestamps on the Domestication.

The date palm, Phoenix dactylifera, has been a cornerstone of Middle Eastern and North African agriculture for millennia. It was first domesticated in the Persian Gulf, and its evolution appears to have been influenced by gene flow from two wild relatives, P. theophrasti, currently restricted to Crete and Turkey, and P. sylvestris, widespread from Bangladesh to the West Himalayas. Genomes of ancient date palm seeds show that gene flow from P. theophrasti to P. dactylifera may have occurred by ∼2,200 years ago, but traces of P. sylvestris could not be detected. We here integrate archeogenomics of a ∼2,100-year-old P. dactylifera leaf from Saqqara (Egypt), molecular-clock dating, and coalescence approaches with population genomic tests, to probe the hybridization between the date palm and its two closest relatives and provide minimum and maximum timestamps for its reticulated evolution. The Saqqara date palm shares a close genetic affinity with North African date palm populations, and we find clear genomic admixture from both P. theophrasti, and P. sylvestris, indicating that both had contributed to the date palm genome by 2,100 years ago. Molecular-clocks placed the divergence of P. theophrasti from P. dactylifera/P. sylvestris and that of P. dactylifera from P. sylvestris in the Upper Miocene, but strongly supported, conflicting topologies point to older gene flow between P. theophrasti and P. dactylifera, and P. sylvestris and P. dactylifera. Our work highlights the ancient hybrid origin of the date palms, and prompts the investigation of the functional significance of genetic material introgressed from both close relatives, which in turn could prove useful for modern date palm breeding.

Target sequence capture of Barnadesioideae (Compositae) demonstrates the utility of low coverage loci in phylogenomic analyses.

Target sequence capture has emerged as a powerful method to sequence hundreds or thousands of genomic regions in a cost- and time-efficient approach. In most cases, however, targeted regions lack full sequence information for certain samples, due to taxonomic, laboratory, or stochastic factors. Loci lacking molecular data for a large number of samples are commonly excluded from downstream analyses, even though they may still contain valuable information. On the other hand, including data-poor loci may bias phylogenetic analyses. Here we use a target sequence capture dataset of an ecologically and taxonomically diverse group of spiny sunflowers (Asteraceae, or Compositae: Barnadesioideae) to test how the inclusion or exclusion of such data-poor loci affects phylogenetic inference. We investigate the sensitivity of concatenation and coalescent approaches to missing data with matrices of varying taxonomic completeness by filtering loci with different proportions of missing samples prior to data analysis. We find that missing data affect both the topology and branch support of the resulting phylogenies. The matrix containing all loci yielded the overall highest node support values, independently of the amount of missing nucleotides. These results provide empirical support to earlier suggestions based on single genes and data simulations that taxa with high amounts of missing data should not be readily dismissed as they can provide essential information for phylogenomic reconstruction.

Mapping Africa's Biodiversity: More of the Same Is Just Not Good Enough.

Species distribution data are fundamental to the understanding of biodiversity patterns and processes. Yet, such data are strongly affected by sampling biases, mostly related to site accessibility. The understanding of these biases is therefore crucial in systematics, biogeography, and conservation. Here we present a novel approach for quantifying sampling effort and its impact on biodiversity knowledge, focusing on Africa. In contrast to previous studies assessing sampling completeness (percentage of species recorded in relation to predicted), we investigate whether the lack of knowledge of a site attracts scientists to visit these areas and collect samples of species. We then estimate the time required to sample 90% of the continent under a Weibull distributed biodiversity sampling rate and the number of sampling events required to record $ \ge $50% of the species. Using linear and spatial regression models, we show that previous sampling has been strongly influencing the resampling of areas, attracting repeated visits. This bias has existed for over two centuries, has increased in recent decades, and is most pronounced among mammals. It may take between 172 and 274 years, depending on the group, to achieve at least one sampling event per grid cell in the entire continent. Just one visit will, however, not be enough: in order to record $ \ge $50% of the current diversity, it will require at least 12 sampling events for amphibians, 13 for mammals, and 27 for birds. Our results demonstrate the importance of sampling areas that lack primary biodiversity data and the urgency with which this needs to be done. Current practice is insufficient to adequately classify and map African biodiversity; it can lead to incorrect conclusions being drawn from biogeographic analyses and can result in misleading and self-reinforcing conservation priorities. [Amphibians; birds; mammals; sampling bias; sampling gaps; Wallacean shortfall.].