Phylogenomics and historical biogeography of Hydrangeeae (Hydrangeaceae) elucidate the effects of geologic and climatic dynamics on diversification.

Demonstrating the process of transregional biogeography and mechanisms underlying evolutionary radiations is crucial to understanding biological evolution. Here, we use Hydrangeeae (Hydrangeaceae), a tribe with a unique disjunct distribution and complex trait variations, using a solid phylogenetic framework, to investigate how geographical and climatic factors interact with functional traits to trigger plant evolutionary radiations. We constructed the first highly supported and dated phylogenetic framework using 79 protein-coding genes obtained from 81 plastomes, representing 63 species and all major clades, and found that most extant species originated from asynchronous diversification of two lineages undergoing repeated expansion and retraction, at middle and high latitudes of the Northern Hemisphere between East Asia and North America, during the Eocene to Pleistocene (driven by geologic and climatic dynamics). In accordance with these drivers, interactions of flora between central-eastern China and Japan occurred frequently after the Late Tertiary. We found that resource limitation and range fragmentation probably accelerated the diversification of Hydrangeeae, which supports the resource-use hypothesis. Our study sheds light on the evolutionary radiation and assembly of flora within East Asia, and the East Asian-North American disjunction, through integration of phylogenomic and biogeographic data with functional trait and ecological data.

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.

Decoupled evolution of soft and hard substrate communities during the Cambrian Explosion and Great Ordovician Biodiversification Event.

Contrasts between the Cambrian Explosion (CE) and the Great Ordovician Biodiversification Event (GOBE) have long been recognized. Whereas the vast majority of body plans were established as a result of the CE, taxonomic increases during the GOBE were manifested at lower taxonomic levels. Assessing changes of ichnodiversity and ichnodisparity as a result of these two evolutionary events may shed light on the dynamics of both radiations. The early Cambrian (series 1 and 2) displayed a dramatic increase in ichnodiversity and ichnodisparity in softground communities. In contrast to this evolutionary explosion in bioturbation structures, only a few Cambrian bioerosion structures are known. After the middle to late Cambrian diversity plateau, ichnodiversity in softground communities shows a continuous increase during the Ordovician in both shallow- and deep-marine environments. This Ordovician increase in bioturbation diversity was not paralleled by an equally significant increase in ichnodisparity as it was during the CE. However, hard substrate communities were significantly different during the GOBE, with an increase in ichnodiversity and ichnodisparity. Innovations in macrobioerosion clearly lagged behind animal-substrate interactions in unconsolidated sediment. The underlying causes of this evolutionary decoupling are unclear but may have involved three interrelated factors: (i) a Middle to Late Ordovician increase in available hard substrates for bioerosion, (ii) increased predation, and (iii) higher energetic requirements for bioerosion compared with bioturbation.

Evolutionary radiations in the species-rich mountain genus Saxifraga L.

BACKGROUND: A large number of taxa have undergone evolutionary radiations in mountainous areas, rendering alpine systems particularly suitable to study the extrinsic and intrinsic factors that have shaped diversification patterns in plants. The species-rich genus Saxifraga L. is widely distributed throughout the Northern Hemisphere, with high species numbers in the regions adjacent to the Qinghai-Tibet Plateau (QTP) in particular the Hengduan Mountains and the Himalayas. Using a dataset of 297 taxa (representing at least 60% of extant Saxifraga species), we explored the variation of infrageneric diversification rates. In addition, we used state-dependent speciation and extinction models to test the effects of geographic distribution in the Hengduan Mountains and the entire QTP region as well as of two morphological traits (cushion habit and specialized lime-secreting glands, so-called hydathodes) on the diversification of this genus. RESULTS: We detected two to three rate shifts across the Saxifraga phylogeny and two of these shifts led to radiations within two large subclades of Saxifraga, sect. Ciliatae Haworth subsect. Hirculoideae Engl. & Irmsch. and sect. Porphyrion Tausch subsect. Kabschia Engl. GEOSSE analyses showed that presence in the Hengduan Mountains had a positive effect on diversification across Saxifraga. Influence of these mountains was strongest in Saxifraga sect. Ciliatae subsect. Hirculoideae given its pronounced distribution there, and thus the radiation in this group can be classified at least partially as geographic. In contrast, the evolution of the cushion life form and lime-secreting hydathodes had positive effects on diversification only in selected Saxifraga sections, including sect. Porphyrion subsect. Kabschia. We therefore argue that radiation in this group was likely adaptive. CONCLUSIONS: Our study underlines the complexity of processes and factors underpinning plant radiations: Even in closely related lineages occupying the same life zone, shifts in diversification are not necessarily governed by similar factors. In conclusion, alpine plant radiations result from a complex interaction among geographical settings and/or climatic modifications providing key opportunities for diversification as well as the evolution of key innovations.

Green Web or megabiased clock? Plant fossils from Gondwanan Patagonia speak on evolutionary radiations.

Evolutionary divergence-age estimates derived from molecular 'clocks' are frequently correlated with paleogeographic, paleoclimatic and extinction events. One prominent hypothesis based on molecular data states that the dominant pattern of Southern Hemisphere biogeography is post-Gondwanan clade origins and subsequent dispersal across the oceans in a metaphoric 'Green Web'. We tested this idea against well-dated Patagonian fossils of 19 plant lineages, representing organisms that actually lived on Gondwana. Most of these occurrences are substantially older than their respective, often post-Gondwanan molecular dates. The Green Web interpretation probably results from directional bias in molecular results. Gondwanan history remains fundamental to understanding Southern Hemisphere plant radiations, and we urge significantly greater caution when using molecular dating to interpret the biological impacts of geological events.

Recently evolved diversity and convergent radiations of rainforest mahoganies (Meliaceae) shed new light on the origins of rainforest hyperdiversity.

Tropical rainforest hyperdiversity is often suggested to have evolved over a long time-span (the 'museum' model), but there is also evidence for recent rainforest radiations. The mahoganies (Meliaceae) are a prominent plant group in lowland tropical rainforests world-wide but also occur in all other tropical ecosystems. We investigated whether rainforest diversity in Meliaceae has accumulated over a long time or has more recently evolved. We inferred the largest time-calibrated phylogeny for the family to date, reconstructed ancestral states for habitat and deciduousness, estimated diversification rates and modeled potential shifts in macro-evolutionary processes using a recently developed Bayesian method. The ancestral Meliaceae is reconstructed as a deciduous species that inhabited seasonal habitats. Rainforest clades have diversified from the Late Oligocene or Early Miocene onwards. Two contemporaneous Amazonian clades have converged on similar ecologies and high speciation rates. Most species-level diversity of Meliaceae in rainforest is recent. Other studies have found steady accumulation of lineages, but the large majority of plant species diversity in rainforests is recent, suggesting (episodic) species turnover. Rainforest hyperdiversity may best be explained by recent radiations from a large stock of higher level taxa.

The interplay of environmental constraints and bioturbation on matground development along the marine depositional profile during the Ordovician Radiation.

This study documents the distribution of matgrounds in a wide variety of environments recorded in the Ordovician Lashkerak and Ghelli Formations in the Alborz Mountains of northern Iran in order to evaluate controls on their distribution along the marine depositional profile. Detailed facies analysis allowed differentiating three groups of facies associations in the Lower to Upper Ordovician deposits of the Lashkerak formation: (i) estuarine system; (ii) wave-dominated shoreface-offshore complex; and (iii) mixed river- and wave-influenced deltaic system. The Middle to Upper Ordovician deposits of the Ghelli formation are divided into two groups of facies associations: (i) tide-influenced deltaic succession and (ii) deep-water fan system. Microbially induced sedimentary structures (MISS) are present in deposits formed in the central estuarine basin (Lashkerak formation) and in proximal lobes and lobe fringes of deep-water turbidite fans (Ghelli formation). On the contrary, MISS are absent in deposits from the wave-dominated shoreface-offshore complex, river- and tide-dominated deltas, and various subenvironments of the incised wave-dominated estuary (i.e., bayhead delta and estuary mouth) and the deep-marine turbidite fan system (i.e., turbidite channel, slope, and outer lobe). The lack of evidence of mat-building microorganisms in the deltaic systems may have resulted from two factors: (1) high physico-chemical stressors caused by river-induced processes, and (2) increase in degree of sediment disturbance, biodiffusion, and bioirrigation by burrowing organisms. Formation of microbial mats in the wave-dominated shoreface-offshore complex was inhibited by the activity of an abundant and diverse infauna capable of reworking the sediment. Our analysis shows that the spatial distribution of microbial mats was controlled by an interplay of environmental factors and innovations in animal-substrate interactions, mostly expressed by secular changes in bioturbation. This study supports the notion that the agronomic revolution was diachronic, with marginal-marine and deep-sea ecosystems lagging behind shallow-marine settings.

A new balaenopterid whale from the late Miocene of the Southern North Sea Basin and the evolution of balaenopterid diversity (Cetacea, Mysticeti).

BACKGROUND: Balaenopterid mysticetes represent the most successful family-rank group of this clade. Their evolutionary history is characterized by a rich fossil record but the origin of the living genera is still largely not understood. Recent discoveries in the southern border of the North Sea revealed a number of well preserved fossil balaenopterid whales that may help resolving this problem. In particular, skull NMR 14035 shares morphological characters with the living humpback whale, Megaptera novaeangliae and, for this reason, its characteristics are investigated here. METHODS: The comparative anatomical analysis of the new specimen formed the basis of a new phylogenetic analysis of the Mysticeti based on a matrix including 350 morphological character states scored for 82 Operational Taxonomic Units. The stratigraphic age of the specimen was determined based on the analysis of the dinocyst assemblage recovered in the associated sediment. We assessed clade diversity in Balaenopteridae by counting the numbers of clades in given time intervals and then plotted the results. RESULTS: Nehalaennia devossi n. gen. et sp. is described for the first time from the late Tortonian (8.7-8.1 Ma) of the Westerschelde (The Netherlands). This new taxon belongs to Balaenopteridae and shows a surprisingly high number of advanced characters in the skull morphology. Nehalaennia devossi is compared to a large sample of balaenopterid mysticetes and a phylogenetic analysis placed it as the sister group of a clade including the genus Archaebalaenoptera. The inclusion of this fossil allowed to propose a phylogenetic hypothesis for Balaenopteridae in which (1) Eschrichtiidae (gray whales) represents a family of its own, (2) Balaenopteridae + Eschrichtiidae form a monophyletic group (superfamily Balaenopteroidea), (3) Cetotheriidae is the sister group of Balaenopteroidea, (4) living Balaenoptera species form a monophyletic group and (5) living M. novaeangliae is the sister group of Balaenoptera. Our work reveals a complex phylogenetic history of Balaenopteridae and N. devossi informs us about the early morphological transformations in this family. Over time, this family experienced a number of diversity pulses suggesting that true evolutionary radiations had taken place. The paleoecological drivers of these pulses are then investigated.

Evolutionary Rates Standardized for Evolutionary Space: Perspectives on Trait Evolution.

Characterization of evolutionary radiations benefits from describing the temporal patterns of trait disparification. Comparative methods attempt this by evaluating the statistical fit of trait distributions to a phylogenetic hypothesis under assumed evolutionary models. However, it can be challenging to differentiate between models, with discriminatory power depending on the modes of evolution underlying trait distributions. We suggest rates of 'trait space saturation', standardized for limits to evolutionary change, as an additional tool to distinguish between modes of trait evolution. We evaluate this approach using simulations and show that trait space saturation can identify the true model of trait evolution in cases where traditional comparative methods can fail. We illustrate our approach using diverse empirical studies that represent contrasting scenarios of evolutionary radiation.

The Evolving Theory of Evolutionary Radiations.

Evolutionary radiations have intrigued biologists for more than 100 years, and our understanding of the patterns and processes associated with these radiations continues to grow and evolve. Recently it has been recognized that there are many different types of evolutionary radiation beyond the well-studied adaptive radiations. We focus here on multifarious types of evolutionary radiations, paying special attention to the abiotic factors that might trigger diversification in clades. We integrate concepts such as exaptation, species selection, coevolution, and the turnover-pulse hypothesis (TPH) into the theoretical framework of evolutionary radiations. We also discuss other phenomena that are related to, but distinct from, evolutionary radiations that have relevance for evolutionary biology.

Evolutionary diversifications of plants on the Qinghai-Tibetan Plateau.

The Qinghai-Tibetan Plateau (QTP) is the highest and one of the most extensive plateaus in the world. Phylogenetic, phylogeographic, and ecological studies support plant diversifications on the QTP through multiple mechanisms such as allopatric speciation via geographic isolation, climatic oscillations and divergences, pollinator-mediated isolation, diploid hybridization and introgression, and allopolyploidy. These mechanisms have driven spectacular radiations and/or species diversifications in various groups of plants such as Pedicularis L., Saussurea DC., Rhododendron L., Primula L., Meconopsis Vig., Rhodiola L., and many lineages of gymnosperms. Nevertheless, much work is needed toward understanding the evolutionary mechanisms of plant diversifications on the QTP. Well-sampled biogeographic analyses of the QTP plants in the broad framework of the Northern Hemisphere as well as the Southern Hemisphere are still relatively few and should be encouraged in the next decade. This paper reviews recent evidence from phylogenetic and biogeographic studies in plants, in the context of rapid radiations, mechanisms of species diversifications on the QTP, and the biogeographic significance of the QTP in the broader context of both the Northern and Southern Hemisphere biogeography. Integrative multidimensional analyses of phylogeny, morphological innovations, geography, ecology, development, species interactions and diversifications, and geology are needed and should shed insights into the patterns of evolutionary assembly and radiations in this fascinating region.