Fabien L. Condamine

The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae)

Summary The tropical Andes of South America, the worlds richest biodiversity hotspot, are home to many rapid radiations. While geological, climatic, and ecological processes collectively explain such radiations, their relative contributions are seldom examined within a single clade. We explore the contribution of these factors by applying a series of diversification models that incorporate mountain building, climate change, and trait evolution to the first dated phylogeny of Andean bellflowers (Campanulaceae: Lobelioideae). Our framework is novel for its direct incorporation of geological data on Andean uplift into a macroevolutionary model. We show that speciation and extinction are differentially influenced by abiotic factors: speciation rates rose concurrently with Andean elevation, while extinction rates decreased during global cooling. Pollination syndrome and fruit type, both biotic traits known to facilitate mutualisms, played an additional role in driving diversification. These abiotic and biotic factors resulted in one of the fastest radiations reported to date: the centropogonids, whose 550 species arose in the last 5 million yr. Our study represents a significant advance in our understanding of plant evolution in Andean cloud forests. It further highlights the power of combining phylogenetic and Earth science models to explore the interplay of geology, climate, and ecology in generating the worlds biodiversity.

Cretaceous environmental changes led to high extinction rates in a hyperdiverse beetle family

BackgroundAs attested by the fossil record, Cretaceous environmental changes have significantly impacted the diversification dynamics of several groups of organisms. A major biome turnover that occurred during this period was the rise of angiosperms starting ca. 125 million years ago. Though there is evidence that the latter promoted the diversification of phytophagous insects, the response of other insect groups to Cretaceous environmental changes is still largely unknown. To gain novel insights on this issue, we assess the diversification dynamics of a hyperdiverse family of detritivorous beetles (Tenebrionidae) using molecular dating and diversification analyses.ResultsAge estimates reveal an origin after the Triassic-Jurassic mass extinction (older than previously thought), followed by the diversification of major lineages during Pangaean and Gondwanan breakups. Dating analyses indicate that arid-adapted species diversified early, while most of the lineages that are adapted to more humid conditions diversified much later. Contrary to other insect groups, we found no support for a positive shift in diversification rates during the Cretaceous; instead there is evidence for an 8.5-fold increase in extinction rates that was not compensated by a joint increase in speciation rates.ConclusionsWe hypothesize that this pattern is better explained by the concomitant reduction of arid environments starting in the mid-Cretaceous, which likely negatively impacted the diversification of arid-adapted species that were predominant at that time.

Recent origin and rapid speciation of Neotropical orchids in the world's richest plant biodiversity hotspot

Summary The Andean mountains of South America are the most species‐rich biodiversity hotspot worldwide with c. 15% of the worlds plant species, in only 1% of the worlds land surface. Orchids are a key element of the Andean flora, and one of the most prominent components of the Neotropical epiphyte diversity, yet very little is known about their origin and diversification. We address this knowledge gap by inferring the biogeographical history and diversification dynamics of the two largest Neotropical orchid groups (Cymbidieae and Pleurothallidinae), using two unparalleled, densely sampled orchid phylogenies (including more than 400 newly generated DNA sequences), comparative phylogenetic methods, geological and biological datasets. We find that the majority of Andean orchid lineages only originated in the last 20–15 million yr. Andean lineages are derived from lowland Amazonian ancestors, with additional contributions from Central America and the Antilles. Species diversification is correlated with Andean orogeny, and multiple migrations and recolonizations across the Andes indicate that mountains do not constrain orchid dispersal over long timescales. Our study sheds new light on the timing and geography of a major Neotropical diversification, and suggests that mountain uplift promotes species diversification across all elevational zones.

Global diversification of a tropical plant growth form: environmental correlates and historical contingencies in climbing palms

Tropical rain forests (TRF) are the most diverse terrestrial biome on Earth, but the diversification dynamics of their constituent growth forms remain largely unexplored. Climbing plants contribute significantly to species diversity and ecosystem processes in TRF. We investigate the broad-scale patterns and drivers of species richness as well as the diversification history of climbing and non-climbing palms (Arecaceae). We quantify to what extent macroecological diversity patterns are related to contemporary climate, forest canopy height, and paleoclimatic changes. We test whether diversification rates are higher for climbing than non-climbing palms and estimate the origin of the climbing habit. Climbers account for 22% of global palm species diversity, mostly concentrated in Southeast Asia. Global variation in climbing palm species richness can be partly explained by past and present-day climate and rain forest canopy height, but regional differences in residual species richness after accounting for current and past differences in environment suggest a strong role of historical contingencies in climbing palm diversification. Climbing palms show a higher net diversification rate than non-climbers. Diversification analyses of palms detected a diversification rate increase along the branches leading to the most species-rich clade of climbers. Ancestral character reconstructions revealed that the climbing habit originated between early Eocene and Miocene. These results imply that changes from non-climbing to climbing habits may have played an important role in palm diversification, resulting in the origin of one fifth of all palm species. We suggest that, in addition to current climate and paleoclimatic changes after the late Neogene, present-day diversity of climbing palms can be explained by morpho-anatomical innovations, the biogeographic history of Southeast Asia, and/or ecological opportunities due to the diversification of high-stature dipterocarps in Asian TRFs.

Toward a Self-Updating Platform for Estimating Rates of Speciation and Migration, Ages, and Relationships of Taxa

&NA; Rapidly growing biological data—including molecular sequences and fossils—hold an unprecedented potential to reveal how evolutionary processes generate and maintain biodiversity. However, researchers often have to develop their own idiosyncratic workflows to integrate and analyze these data for reconstructing time‐calibrated phylogenies. In addition, divergence times estimated under different methods and assumptions, and based on data of various quality and reliability, should not be combined without proper correction. Here we introduce a modular framework termed SUPERSMART (Self‐Updating Platform for Estimating Rates of Speciation and Migration, Ages, and Relationships of Taxa), and provide a proof of concept for dealing with the moving targets of evolutionary and biogeographical research. This framework assembles comprehensive data sets of molecular and fossil data for any taxa and infers dated phylogenies using robust species tree methods, also allowing for the inclusion of genomic data produced through next‐generation sequencing techniques. We exemplify the application of our method by presenting phylogenetic and dating analyses for the mammal order Primates and for the plant family Arecaceae (palms). We believe that this framework will provide a valuable tool for a wide range of hypothesis‐driven research questions in systematics, biogeography, and evolution. SUPERSMART will also accelerate the inference of a “Dated Tree of Life” where all node ages are directly comparable.

A first higher-level time-calibrated phylogeny of antlions (Neuroptera: Myrmeleontidae)

In this study, we reconstruct the first time-calibrated phylogeny of the iconic antlion family, the Myrmeleontidae (Neuroptera: Myrmeleontiformia). We use maximum likelihood and Bayesian inference to analyse a molecular dataset based on seven mitochondrial and nuclear gene markers. The dataset encompasses 106 species of Neuroptera, including 94 antlion species. The resulting phylogenetic framework provides support for a myrmeleontid classification distinguishing four subfamilies: Acanthaclisinae, Myrmeleontinae, Palparinae, and Stilbopteryginae. Within Myrmeleontinae, Myrmecaelurini and Nemoleontini are recovered as monophyletic clades; Gepini also appears as a valid tribe, distinct from Myrmecaelurini whereas Myrmecaelurini and Nesoleontini on one hand and Brachynemurini and Dendroleontini on the other hand, appear closely related. Some preliminary information related to generic and specific levels are also implied from our results, such as the paraphyly of several genera. Dating analyses based on thoroughly evaluated fossil calibrations indicate that the antlion family likely originated in the Cretaceous, between 135 and 138 million years ago (depending on the set of fossil calibrations), and that all higher-level lineages appeared during the Early Cretaceous. This first phylogenetic hypothesis will provide a valuable basis to further expand the taxonomic coverage and molecular sampling, and to lay the foundations of future systematic revisions.

Historical species losses in bumblebee evolution

Investigating how species coped with past environmental changes informs how modern species might face human-induced global changes, notably via the study of historical extinction, a dominant feature that has shaped current biodiversity patterns. The genus Bombus, which comprises 250 mostly cold-adapted species, is an iconic insect group sensitive to current global changes. Through a combination of habitat loss, pathogens and climate change, bumblebees have experienced major population declines, and several species are threatened with extinction. Using a time-calibrated tree of Bombus, we analyse their diversification dynamics and test hypotheses about the role of extinction during major environmental changes in their evolutionary history. These analyses support a history of fluctuating species dynamics with two periods of historical species loss in bumblebees. Dating estimates gauge that one of these events started after the middle Miocene climatic optimum and one during the early Pliocene. Both periods are coincident with global climate change that may have extirpated Bombus species. Interestingly, bumblebees experienced high diversification rates during the Plio-Pleistocene glaciations. We also found evidence for a major species loss in the past one million years that may be continuing today.

Andean Mountain Building Did not Preclude Dispersal of Lowland Epiphytic Orchids in the Neotropics

The Andean uplift is one of the major orographic events in the New World and has impacted considerably the diversification of numerous Neotropical lineages. Despite its importance for biogeography, the specific role of mountain ranges as a dispersal barrier between South and Central American lowland plant lineages is still poorly understood. The swan orchids (Cycnoches) comprise ca 34 epiphytic species distributed in lowland and pre-montane forests of Central and South America. Here, we study the historical biogeography of Cycnoches to better understand the impact of the Andean uplift on the diversification of Neotropical lowland plant lineages. Using novel molecular sequences (five nuclear and plastid regions) and twelve biogeographic models, we infer that the most recent common ancestor of Cycnoches originated in Amazonia ca 5 Mya. The first colonization of Central America occurred from a direct migration event from Amazonia, and multiple bidirectional trans-Andean migrations between Amazonia and Central America took place subsequently. Notably, these rare biological exchanges occurred well after major mountain building periods. The Andes have limited plant migration, yet it has seldom allowed episodic gene exchange of lowland epiphyte lineages such as orchids with great potential for effortless dispersal because of the very light, anemochorous seeds.

Amazonia is the primary source of Neotropical biodiversity

Significance Amazonia is not only the world’s most diverse rainforest but is also the region in tropical America that has contributed most to its total biodiversity. We show this by estimating and comparing the evolutionary history of a large number of animal and plant species. We find that there has been extensive interchange of evolutionary lineages among different regions and biomes, over the course of tens of millions of years. Amazonia stands out as the primary source of diversity, which can be mainly explained by the total amount of time Amazonian lineages have occupied the region. The exceedingly rich and heterogeneous diversity of the American tropics could only be achieved by high rates of dispersal events across the continent. The American tropics (the Neotropics) are the most species-rich realm on Earth, and for centuries, scientists have attempted to understand the origins and evolution of their biodiversity. It is now clear that different regions and taxonomic groups have responded differently to geological and climatic changes. However, we still lack a basic understanding of how Neotropical biodiversity was assembled over evolutionary timescales. Here we infer the timing and origin of the living biota in all major Neotropical regions by performing a cross-taxonomic biogeographic analysis based on 4,450 species from six major clades across the tree of life (angiosperms, birds, ferns, frogs, mammals, and squamates), and integrate >1.3 million species occurrences with large-scale phylogenies. We report an unprecedented level of biotic interchange among all Neotropical regions, totaling 4,525 dispersal events. About half of these events involved transitions between major environmental types, with a predominant directionality from forested to open biomes. For all taxonomic groups surveyed here, Amazonia is the primary source of Neotropical diversity, providing >2,800 lineages to other regions. Most of these dispersal events were to Mesoamerica (∼1,500 lineages), followed by dispersals into open regions of northern South America and the Cerrado and Chaco biomes. Biotic interchange has taken place for >60 million years and generally increased toward the present. The total amount of time lineages spend in a region appears to be the strongest predictor of migration events. These results demonstrate the complex origin of tropical ecosystems and the key role of biotic interchange for the assembly of regional biotas.

The improbable journeys of epiphytic plants across the Andes: Historical biogeography of Cycnoches (Catasetinae, Orchidaceae)

The Andean uplift is one of the major orographic events in the New World and has impacted considerably the diversification of numerous Neotropical organisms. Despite its importance for biogeography, the specific role of mountain ranges as a dispersal barrier between South and Central American lowland plant lineages is still poorly understood. The swan orchids (Cycnoches) comprise ca 34 epiphytic species distributed in lowland and pre-montane forests of Central and South America. Here, we study the historical biogeography of Cycnoches to better understand the impact of the Andean uplift on the diversification of Neotropical lowland plant lineages. Using novel molecular sequences (five nuclear and plastid regions) and twelve biogeographic models with and without founder-event speciation, we infer that the most recent common ancestor of Cycnoches may have originated in Amazonia ca 5 Mya. The first colonization of Central America occurred from a direct migration event from Amazonia, and multiple bidirectional trans-Andean migrations between Amazonia and Central America took place subsequently. Notably, such biological exchange occurred well after major mountain building periods. The Andes have not acted as an impassable barrier for epiphytic lowland lineages such as orchids having a great potential for effortless dispersal because of the very light, anemochorous seeds.