Sequential trait evolution did not drive deep-time diversification in sharks.

Estimating how traits evolved and impacted diversification across the tree of life represents a critical topic in ecology and evolution. Although there has been considerable research in comparative biology, large parts of the tree of life remain underexplored. Sharks are an iconic clade of marine vertebrates, and key components of marine ecosystems since the early Mesozoic. However, few studies have addressed how traits evolved or whether they impacted their extant diversity patterns. Our study aimed to fill this gap by reconstructing the largest time-calibrated species-level phylogeny of sharks and compiling an exhaustive database for ecological (diet, habitat) and biological (reproduction, maximum body length) traits. Using state-of-the-art models of evolution and diversification, we outlined the major character shifts and modes of trait evolution across shark species. We found support for sequential models of trait evolution and estimated a small to medium-sized lecithotrophic and coastal-dwelling most recent common ancestor for extant sharks. However, our exhaustive hidden traits analyses do not support trait-dependent diversification for any examined traits, challenging previous works. This suggests that the role of traits in shaping sharks' diversification dynamics might have been previously overestimated and should motivate future macroevolutionary studies to investigate other drivers of diversification in this clade.

The Angiosperm Terrestrial Revolution buffered ants against extinction.

With ~14,000 extant species, ants are ubiquitous and of tremendous ecological importance. They have undergone remarkable diversification throughout their evolutionary history. However, the drivers of their diversity dynamics are not well quantified or understood. Previous phylogenetic analyses have suggested patterns of diversity dynamics associated with the Angiosperm Terrestrial Revolution (ATR), but these studies have overlooked valuable information from the fossil record. To address this gap, we conducted a comprehensive analysis using a large dataset that includes both the ant fossil record (~24,000 individual occurrences) and neontological data (~14,000 occurrences), and tested four hypotheses proposed for ant diversification: co-diversification, competitive extinction, hyper-specialization, and buffered extinction. Taking into account biases in the fossil record, we found three distinct diversification periods (the latest Cretaceous, Eocene, and Oligo-Miocene) and one extinction period (Late Cretaceous). The competitive extinction hypothesis between stem and crown ants is not supported. Instead, we found support for the co-diversification, buffered extinction, and hyper-specialization hypotheses. The environmental changes of the ATR, mediated by the angiosperm radiation, likely played a critical role in buffering ants against extinction and favoring their diversification by providing new ecological niches, such as forest litter and arboreal nesting sites, and additional resources. We also hypothesize that the decline and extinction of stem ants during the Late Cretaceous was due to their hyper-specialized morphology, which limited their ability to expand their dietary niche in changing environments. This study highlights the importance of a holistic approach when studying the interplay between past environments and the evolutionary trajectories of organisms.

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.

The angiosperm radiation played a dual role in the diversification of insects and insect pollinators.

Interactions with angiosperms have been hypothesised to play a crucial role in driving diversification among insects, with a particular emphasis on pollinator insects. However, support for coevolutionary diversification in insect-plant interactions is weak. Macroevolutionary studies of insect and plant diversities support the hypothesis that angiosperms diversified after a peak in insect diversity in the Early Cretaceous. Here, we used the family-level fossil record of insects as a whole, and insect pollinator families in particular, to estimate diversification rates and the role of angiosperms on insect macroevolutionary history using a Bayesian process-based approach. We found that angiosperms played a dual role that changed through time, mitigating insect extinction in the Cretaceous and promoting insect origination in the Cenozoic, which is also recovered for insect pollinator families only. Although insects pollinated gymnosperms before the angiosperm radiation, a radiation of new pollinator lineages began as angiosperm lineages increased, particularly significant after 50 Ma. We also found that global temperature, increases in insect diversity, and spore plants were strongly correlated with origination and extinction rates, suggesting that multiple drivers influenced insect diversification and arguing for the investigation of different explanatory variables in further studies.

Bayesian total-evidence dating revisits sloth phylogeny and biogeography: a cautionary tale on morphological clock analyses.

Combining morphological and molecular characters through Bayesian total-evidence dating allows inferring the phylogenetic and timescale framework of both extant and fossil taxa, while accounting for the stochasticity and incompleteness of the fossil record. Such an integrative approach is particularly needed when dealing with clades such as sloths (Mammalia: Folivora), for which developmental and biomechanical studies have shown high levels of morphological convergence whereas molecular data can only account for a limited percentage of their total species richness. Here, we propose an alternative hypothesis of sloth evolution that emphasizes the pervasiveness of morphological convergence and the importance of considering the fossil record and an adequate taxon sampling in both phylogenetic and biogeographic inferences. Regardless of different clock models and morphological datasets, the extant sloth Bradypus is consistently recovered as a megatherioid, and Choloepus as a mylodontoid, in agreement with molecular-only analyses. The recently extinct Caribbean sloths (Megalocnoidea) are found to be a monophyletic sister-clade of Megatherioidea, in contrast to previous phylogenetic hypotheses. Our results contradict previous morphological analyses and further support the polyphyly of "Megalonychidae", whose members were found in five different clades. Regardless of taxon sampling and clock models, the Caribbean colonization of sloths is compatible with the exhumation of islands along Aves Ridge and its geological time frame. Overall, our total-evidence analysis illustrates the difficulty of positioning highly incomplete fossils, although a robust phylogenetic framework was recovered by an a posteriori removal of taxa with high percentages of missing characters. Elimination of these taxa improved topological resolution by reducing polytomies and increasing node support. However, it introduced a systematic and geographic bias because most of these incomplete specimens are from northern South America. This is evident in biogeographic reconstructions, which suggest Patagonia as the area of origin of many clades when taxa are underrepresented, but Amazonia and/or Central and Southern Andes when all taxa are included. More generally, our analyses demonstrate the instability of topology and divergence time estimates when using different morphological datasets and clock models, and thus caution against making macroevolutionary inferences when node support is weak or when uncertainties in the fossil record are not considered.

Drivers of the artiodactyl turnover in insular western Europe at the Eocene-Oligocene Transition.

Simultaneously investigating the effects of abiotic and biotic factors on diversity dynamics is essential to understand the evolutionary history of clades. The Grande Coupure corresponds to a major faunal turnover at the Eocene-Oligocene transition (EOT) (~34.1 to 33.55 Mya) and is defined in western Europe as an extinction of insular European mammals coupled with the arrival of crown clades from Asia. Here, we focused on the species-rich group of endemic European artiodactyls to determine the drivers of the Grande Coupure during the major environmental disruptions at the EOT. Using Bayesian birth-death models, we analyzed an original high-resolution fossil dataset (90 species, >2,100 occurrences) from southwestern France (Quercy area) and estimated the regional diversification and diversity dynamics of endemic and immigrant artiodactyls. We show that the endemic artiodactyl radiation was mainly related to the Eocene tropical conditions, combined with biotic controls on speciation and clade-related diversity dependence. We further highlight that the major environmental changes at the transition (77% of species became extinct) and the concurrent increase in seasonality in Europe during the Oligocene were likely the main drivers of their decline. Surprisingly, our results do not support the widely-held hypothesis of active competition between endemic and immigrant artiodactyls but rather suggest a passive or opportunistic replacement by immigrants, which is further supported by morphological clustering of specific ecological traits across the Eocene-Oligocene transition. Our analyses provide insights into the evolutionary and ecological processes driving the diversification and decline of mammalian clades during a major biological and climatic crisis.

Genomics of the relict species Baronia brevicornis sheds light on its demographic history and genome size evolution across swallowtail butterflies.

Relict species, like coelacanth, gingko, tuatara, are the remnants of formerly more ecologically and taxonomically diverse lineages. It raises the questions of why they are currently species-poor, have restrained ecology, and are often vulnerable to extinction. Estimating heterozygosity level and demographic history can guide our understanding of the evolutionary history and conservation status of relict species. However, few studies have focused on relict invertebrates compared to vertebrates. We sequenced the genome of Baronia brevicornis (Lepidoptera: Papilionidae), which is an endangered species, the sister species of all swallowtail butterflies, and is the oldest lineage of all extant butterflies. From a dried specimen, we were able to generate both long-read and short-read data and assembled a genome of 406 Mb for Baronia. We found a fairly high level of heterozygosity (0.58%) compared to other swallowtail butterflies, which contrasts with its endangered and relict status. Taking into account the high ratio of recombination over mutation, demographic analyses indicated a sharp decline of the effective population size initiated in the last million years. Moreover, the Baronia genome was used to study genome size variation in Papilionidae. Genome sizes are mostly explained by transposable elements activities, suggesting that large genomes appear to be a derived feature in swallowtail butterflies as transposable elements activity is recent and involves different transposable elements classes among species. This first Baronia genome provides a resource for assisting conservation in a flagship and relict insect species as well as for understanding swallowtail genome evolution.

Convergence in sympatric swallowtail butterflies reveals ecological interactions as a key driver of worldwide trait diversification.

Ecological interactions can promote phenotypic diversification in sympatric species. While competition can enhance trait divergence, other ecological interactions may promote convergence in sympatric species. Within butterflies, evolutionary convergences in wing color patterns have been reported between distantly related species, especially in females of palatable species, where mimetic color patterns are promoted by predator communities shared with defended species living in sympatry. Wing color patterns are also often involved in species recognition in butterflies, and divergence in this trait has been reported in closely related species living in sympatry as a result of reproductive character displacement. Here, we investigate the effect of sympatry between species on the convergence vs. divergence of their wing color patterns in relation to phylogenetic distance, focusing on the iconic swallowtail butterflies (family Papilionidae). We developed an unsupervised machine learning-based method to estimate phenotypic distances among wing color patterns of 337 species, enabling us to finely quantify morphological diversity at the global scale among species and allowing us to compute pairwise phenotypic distances between sympatric and allopatric species pairs. We found phenotypic convergence in sympatry, stronger among distantly related species, while divergence was weaker and restricted to closely related males. The convergence was stronger among females than males, suggesting that differential selective pressures acting on the two sexes drove sexual dimorphism. Our results highlight the significant effect of ecological interactions driven by predation pressures on trait diversification in Papilionidae and provide evidence for the interaction between phylogenetic proximity and ecological interactions in sympatry, acting on macroevolutionary patterns of phenotypic diversification.

A sequential diversification with Miocene extinction and Pliocene speciation linked to mountain uplift explains the diversity of the African rain forest clade Monodoreae (Annonaceae).

BACKGROUND AND AIMS: Throughout the Cenozoic, Africa underwent several climatic and geological changes impacting the evolution of tropical rain forests (TRF). African TRF are thought to have extended from East to West in a 'pan-African' TRF, followed by several events of fragmentation during drier climate periods. During the Miocene, climate cooling and mountain uplift led to the aridification of tropical Africa and open habitats expanded at the expense of TRF, which likely experienced local extinctions. However, in plants, these drivers were previously inferred using limited taxonomic and molecular data. Here, we tested the impact of climate and geological changes on diversification within the diverse clade Monodoreae (Annonaceae) composed of 90 tree species restricted to African TRF. METHODS: We reconstructed a near complete phylogenetic tree, based on 32 nuclear genes, and dated using relaxed clocks and fossil calibrations in a Bayesian framework. We inferred the biogeographic history and the diversification dynamics of the clade using multiple birth-death models. KEY RESULTS: Monodoreae originated in East African TRF ca. 25 million years ago (Ma) and expanded toward Central Africa during the Miocene. We inferred range contractions during the middle Miocene and document important connections between East and West African TRF after 15-13 Ma. Our results indicated a sudden extinction event during the late Miocene, followed by an increase in speciation rates. Birth-death models suggested that African elevation change (orogeny) is positively linked to speciation in this clade. CONCLUSION: East Africa is inferred as an important source of Monodoreae species, and possibly for African plant diversity in general. Our results support a "sequential scenario of diversification" where increased aridification triggered extinction of TRF species in Monodoreae. This was quickly followed by rain forests fragmentation, subsequently enhancing lagged speciation resulting from vicariance and improved climate conditions. In contrast to previous ideas, the uplift of East Africa is shown to have played a positive role in Monodoreae diversification.

An eosimiid primate of South Asian affinities in the Paleogene of Western Amazonia and the origin of New World monkeys.

Recent fossil discoveries in Western Amazonia revealed that two distinct anthropoid primate clades of African origin colonized South America near the Eocene/Oligocene transition (ca. 34 Ma). Here, we describe a diminutive fossil primate from Brazilian Amazonia and suggest that, surprisingly, a third clade of anthropoids was involved in the Paleogene colonization of South America by primates. This new taxon, Ashaninkacebus simpsoni gen. et sp. nov., has strong dental affinities with Asian African stem anthropoids: the Eosimiiformes. Morphology-based phylogenetic analyses of early Old World anthropoids and extinct and extant New World monkeys (platyrrhines) support relationships of both Ashaninkacebus and Amamria (late middle Eocene, North Africa) to the South Asian Eosimiidae. Afro-Arabia, then a mega island, played the role of a biogeographic stopover between South Asia and South America for anthropoid primates and hystricognathous rodents. The earliest primates from South America bear little adaptive resemblance to later Oligocene-early Miocene platyrrhine monkeys, and the scarcity of available paleontological data precludes elucidating firmly their affinities with or within Platyrrhini. Nonetheless, these data shed light on some of their life history traits, revealing a particularly small body size and a diet consisting primarily of insects and possibly fruit, which would have increased their chances of survival on a natural floating island during this extraordinary over-water trip to South America from Africa. Divergence-time estimates between Old and New World taxa indicate that the transatlantic dispersal(s) could source in the intense flooding events associated with the late middle Eocene climatic optimum (ca. 40.5 Ma) in Western Africa.

Phylogeny and diversification of planthoppers (Hemiptera: Fulgoromorpha) based on a comprehensive molecular dataset and large taxon sampling.

Our understanding of the evolution of Fulgoromorpha (Insects, Hemiptera) has relied on molecular studies that have only considered either a limited number of taxa where all the families were not represented simultaneously, or a reduced number of genes.The absence of a global analysis comparing all the available data has thus led to significant biases in the analyzes, as evidenced by the incongruence of the results reported for planthopper phylogeny. Here we provide a phylogenetic and dating analysis of the Fulgoromorpha with a large sampling of 531 ingroup taxa, representing about 80% of the currently described suprageneric taxonomic diversity in this group. This study is based on most of the molecular sequences available to date and duly verified, for a set of nuclear and mitochondrial genes from a taxonomic sampling as complete as possible. The most significant results of our study are: (1) the unexpected paraphyly of Delphacidae whose Protodelphacida seem more related to Cixiidae than to other Delphacidae;(2) the group Meenoplidae-Kinnaridae recovered sister to the remaining Fulgoroidea families; (3) the early branching node of Tettigometridae sister of all the other families;(4) the Achilidae-Derbidae clade with Achilidae Plectoderini including Achilixiidae recovered as monophyletic as well as theFulgoridae-Dictyopharidae clade; and (5) the Tropiduchidae placed sister to the other so called 'higher' families (sec. Shcherbakov, 2006).Our divergence times analysis, calibrated with a set of duly verified fossils, suggests that the first diversification of planthoppers occurred in the Early Triassic around 240 Mya and those of the superfamilies Delphacoidea and Fulgoroidea in the Middle-Late Triassic around 210 Mya and 230 Mya, respectively. By the end of the Jurassic, all major planthopper lineages were originated, and all families, around 125 Mya, might havebeen driven in their distribution and evolution (in their first subfamilial divisions) by the geographical constraints of the Gondwanan break-up.Rapid evolutionary radiations occurred particularly in Fulgoridae around 125-130 Mya. Our results stress the importance of the good quality of the sequences used in the molecular analyzes and the primordial importance of a large sampling when analyzing the phylogeny of the group.

Reconciling fossils with phylogenies reveals the origin and macroevolutionary processes explaining the global cycad biodiversity.

The determinants of biodiversity patterns can be understood using macroevolutionary analyses. The integration of fossils into phylogenies offers a deeper understanding of processes underlying biodiversity patterns in deep time. Cycadales are considered a relict of a once more diverse and globally distributed group but are restricted to low latitudes today. We still know little about their origin and geographic range evolution. Combining molecular data for extant species and leaf morphological data for extant and fossil species, we study the origin of cycad global biodiversity patterns through Bayesian total-evidence dating analyses. We assess the ancestral geographic origin and trace the historical biogeography of cycads with a time-stratified process-based model. Cycads originated in the Carboniferous on the Laurasian landmass and expanded in Gondwana in the Jurassic. Through now-vanished continental connections, Antarctica and Greenland were crucial biogeographic crossroads for cycad biogeography. Vicariance is an essential speciation mode in the deep and recent past. Their latitudinal span increased in the Jurassic and restrained toward subtropical latitudes in the Neogene in line with biogeographic inferences of high-latitude extirpations. We show the benefits of integrating fossils into phylogenies to estimate ancestral areas of origin and to study evolutionary processes explaining the global distribution of present-day relict groups.

A global phylogeny of butterflies reveals their evolutionary history, ancestral hosts and biogeographic origins.

Butterflies are a diverse and charismatic insect group that are thought to have evolved with plants and dispersed throughout the world in response to key geological events. However, these hypotheses have not been extensively tested because a comprehensive phylogenetic framework and datasets for butterfly larval hosts and global distributions are lacking. We sequenced 391 genes from nearly 2,300 butterfly species, sampled from 90 countries and 28 specimen collections, to reconstruct a new phylogenomic tree of butterflies representing 92% of all genera. Our phylogeny has strong support for nearly all nodes and demonstrates that at least 36 butterfly tribes require reclassification. Divergence time analyses imply an origin ~100 million years ago for butterflies and indicate that all but one family were present before the K/Pg extinction event. We aggregated larval host datasets and global distribution records and found that butterflies are likely to have first fed on Fabaceae and originated in what is now the Americas. Soon after the Cretaceous Thermal Maximum, butterflies crossed Beringia and diversified in the Palaeotropics. Our results also reveal that most butterfly species are specialists that feed on only one larval host plant family. However, generalist butterflies that consume two or more plant families usually feed on closely related plants.

Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa.

Africa has undergone a progressive aridification during the last 20 My that presumably impacted organisms and fostered the evolution of life history adaptations. We test the hypothesis that shift to living in ant nests and feeding on ant brood by larvae of phyto-predaceous Lepidochrysops butterflies was an adaptive response to the aridification of Africa that facilitated the subsequent radiation of butterflies in this genus. Using anchored hybrid enrichment we constructed a time-calibrated phylogeny for Lepidochrysops and its closest, non-parasitic relatives in the Euchrysops section (Poloyommatini). We estimated ancestral areas across the phylogeny with process-based biogeographical models and diversification rates relying on time-variable and clade-heterogeneous birth-death models. The Euchrysops section originated with the emerging Miombo woodlands about 22 million years ago (Mya) and spread to drier biomes as they became available in the late Miocene. The diversification of the non-parasitic lineages decreased as aridification intensified around 10 Mya, culminating in diversity decline. In contrast, the diversification of the phyto-predaceous Lepidochrysops lineage proceeded rapidly from about 6.5 Mya when this unusual life history likely first evolved. The Miombo woodlands were the cradle for diversification of the Euchrysops section, and our findings are consistent with the hypothesis that aridification during the Miocene selected for a phyto-predaceous life history in species of Lepidochrysops, with ant nests likely providing caterpillars a safe refuge from fire and a source of food when vegetation was scarce.

Genomics, Population Divergence, and Historical Demography of the World's Largest and Endangered Butterfly, The Queen Alexandra's Birdwing.

The world's largest butterfly is the microendemic Papua New Guinean Ornithoptera alexandrae. Despite years of conservation efforts to protect its habitat and breed this up-to-28-cm butterfly, this species still figures as endangered in the IUCN Red List and is only known from two allopatric populations occupying a total of only ∼140 km². Here we aim at assembling reference genomes for this species to investigate its genomic diversity, historical demography and determine whether the population is structured, which could provide guidance for conservation programs attempting to (inter)breed the two populations. Using a combination of long and short DNA reads and RNA sequencing, we assembled six reference genomes of the tribe Troidini, with four annotated genomes of O. alexandrae and two genomes of related species Ornithoptera priamus and Troides oblongomaculatus. We estimated the genomic diversity of the three species, and we proposed scenarios for the historical population demography using two polymorphism-based methods taking into account the characteristics of low-polymorphic invertebrates. Indeed, chromosome-scale assemblies reveal very low levels of nuclear heterozygosity across Troidini, which appears to be exceptionally low for O. alexandrae (lower than 0.01%). Demographic analyses demonstrate low and steadily declining Ne throughout O. alexandrae history, with a divergence into two distinct populations about 10,000 years ago. These results suggest that O. alexandrae distribution has been microendemic for a long time. It should also make local conservation programs aware of the genomic divergence of the two populations, which should not be ignored if any attempt is made to cross the two populations.

A comprehensive phylogeny and revised taxonomy illuminate the origin and diversification of the global radiation of Papilio (Lepidoptera: Papilionidae).

The swallowtail genus Papilio (Lepidoptera: Papilionidae) is species rich, distributed worldwide, and has broad morphological habits and ecological niches. Because of its elevated species richness, it has been historically difficult to reconstruct a densely sampled phylogeny for this clade. Here we provide a taxonomic working list for the genus, resulting in 235 Papilio species, and assemble a molecular dataset of seven gene fragments representing ca. 80% of the currently described diversity. Phylogenetic analyses reconstructed a robust tree with highly supported relationships within subgenera, although a few nodes in the early history of the Old World Papilio remain unresolved. Contrasting with previous results, we found that Papilio alexanor is sister to all Old World Papilio and that the subgenus Eleppone is no longer monotypic. The latter includes the recently described Fijian Papilio natewa with the Australian Papilio anactus and is sister to subgenus Araminta (formerly included in subgenus Menelaides) occurring in Southeast Asia. Our phylogeny also includes rarely studied (P. antimachus, P. benguetana) or endangered species (P. buddha, P. chikae). Taxonomic changes resulting from this study are elucidated. Molecular dating and biogeographic analyses indicate that Papilio originated ca. 30 million years ago (Oligocene), in a northern region centered on Beringia. A rapid early Miocene radiation in the Paleotropics is revealed within Old World Papilio, potentially explaining their low early branch support. Most subgenera originated in the early to middle Miocene followed by synchronous southward biogeographic dispersals and repeated local extirpations in northern latitudes. This study provides a comprehensive phylogenetic framework for Papilio with clarification of subgeneric systematics and species taxonomic changes enumerated, which will facilitate further studies to address questions on their ecology and evolutionary biology using this model clade.

Global impact and selectivity of the Cretaceous-Paleogene mass extinction among sharks, skates, and rays.

The Cretaceous-Paleogene event was the last mass extinction event, yet its impact and long-term effects on species-level marine vertebrate diversity remain largely uncharacterized. We quantified elasmobranch (sharks, skates, and rays) speciation, extinction, and ecological change resulting from the end-Cretaceous event using >3200 fossil occurrences and 675 species spanning the Late Cretaceous-Paleocene interval at global scale. Elasmobranchs declined by >62% at the Cretaceous-Paleogene boundary and did not fully recover in the Paleocene. The end-Cretaceous event triggered a heterogeneous pattern of extinction, with rays and durophagous species reaching the highest levels of extinction (>72%) and sharks and nondurophagous species being less affected. Taxa with large geographic ranges and/or those restricted to high-latitude settings show higher survival. The Cretaceous-Paleogene event drastically altered the evolutionary history of marine ecosystems.

Multiple drivers and lineage-specific insect extinctions during the Permo-Triassic.

The Permo-Triassic interval encompasses three extinction events including the most dramatic biological crisis of the Phanerozoic, the latest Permian mass extinction. However, their drivers and outcomes are poorly quantified and understood for terrestrial invertebrates, which we assess here for insects. We find a pattern with three extinctions: the Roadian/Wordian (≈266.9 Ma; extinction of 64.5% insect genera), the Permian/Triassic (≈252 Ma; extinction of 82.6% insect genera), and the Ladinian/Carnian boundaries (≈237 Ma; extinction of 74.8% insect genera). We also unveil a heterogeneous effect of these extinction events across the major insect clades. Because extinction events have impacted Permo-Triassic ecosystems, we investigate the influence of abiotic and biotic factors on insect diversification dynamics and find that changes in floral assemblages are likely the strongest drivers of insects' responses throughout the Permo-Triassic. We also assess the effect of diversity dependence between three insect guilds; an effect ubiquitously found in current ecosystems. We find that herbivores held a central position in the Permo-Triassic interaction network. Our study reveals high levels of insect extinction that profoundly shaped the evolutionary history of the most diverse non-microbial lineage.

Combining palaeontological and neontological data shows a delayed diversification burst of carcharhiniform sharks likely mediated by environmental change.

Estimating deep-time species-level diversification processes remains challenging. Both the fossil record and molecular phylogenies allow the estimation of speciation and extinction rates, but each type of data may still provide an incomplete picture of diversification dynamics. Here, we combine species-level palaeontological (fossil occurrences) and neontological (molecular phylogenies) data to estimate deep-time diversity dynamics through process-based birth-death models for Carcharhiniformes, the most speciose shark order today. Despite their abundant fossil record dating back to the Middle Jurassic, only a small fraction of extant carcharhiniform species is recorded as fossils, which impedes relying only on the fossil record to study their recent diversification. Combining fossil and phylogenetic data, we recover a complex evolutionary history for carcharhiniforms, exemplified by several variations in diversification rates with an early low diversity period followed by a Cenozoic radiation. We further reveal a burst of diversification in the last 30 million years, which is partially recorded with fossil data only. We also find that reef expansion and temperature change can explain variations in speciation and extinction through time. These results pinpoint the primordial importance of these environmental variables in the evolution of marine clades. Our study also highlights the benefit of combining the fossil record with phylogenetic data to address macroevolutionary questions.

Diversification dynamics in the Neotropics through time, clades, and biogeographic regions.

The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense debate. A comprehensive understanding is hindered by the lack of deep-time comparative data across wide phylogenetic and ecological contexts. Here, we quantify the prevailing diversification trajectories and drivers of Neotropical diversification in a sample of 150 phylogenies (12,512 species) of seed plants and tetrapods, and assess their variation across Neotropical regions and taxa. Analyses indicate that Neotropical diversity has mostly expanded through time (70% of the clades), while scenarios of saturated and declining diversity account for 21% and 9% of Neotropical diversity, respectively. Five biogeographic areas are identified as distinctive units of long-term Neotropical evolution, including Pan-Amazonia, the Dry Diagonal, and Bahama-Antilles. Diversification dynamics do not differ across these areas, suggesting no geographic structure in long-term Neotropical diversification. In contrast, diversification dynamics differ across taxa: plant diversity mostly expanded through time (88%), while a substantial fraction (43%) of tetrapod diversity accumulated at a slower pace or declined towards the present. These opposite evolutionary patterns may reflect different capacities for plants and tetrapods to cope with past climate changes.