The abiotic and biotic drivers of rapid diversification in Andean bellflowers (Campanulaceae).
ABSTRACT: The tropical Andes of South America, the world's 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 world's biodiversity.
Project description:The Andean mountains of South America are the most species-rich biodiversity hotspot worldwide with c. 15% of the world's plant species, in only 1% of the world's 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.
Project description:Tropical Africa is home to an astonishing biodiversity occurring in a variety of ecosystems. Past climatic change and geological events have impacted the evolution and diversification of this biodiversity. During the last two decades, around 90 dated molecular phylogenies of different clades across animals and plants have been published leading to an increased understanding of the diversification and speciation processes generating tropical African biodiversity. In parallel, extended geological and palaeoclimatic records together with detailed numerical simulations have refined our understanding of past geological and climatic changes in Africa. To date, these important advances have not been reviewed within a common framework. Here, we critically review and synthesize African climate, tectonics and terrestrial biodiversity evolution throughout the Cenozoic to the mid-Pleistocene, drawing on recent advances in Earth and life sciences. We first review six major geo-climatic periods defining tropical African biodiversity diversification by synthesizing 89 dated molecular phylogeny studies. Two major geo-climatic factors impacting the diversification of the sub-Saharan biota are highlighted. First, Africa underwent numerous climatic fluctuations at ancient and more recent timescales, with tectonic, greenhouse gas, and orbital forcing stimulating diversification. Second, increased aridification since the Late Eocene led to important extinction events, but also provided unique diversification opportunities shaping the current tropical African biodiversity landscape. We then review diversification studies of tropical terrestrial animal and plant clades and discuss three major models of speciation: (i) geographic speciation via vicariance (allopatry); (ii) ecological speciation impacted by climate and geological changes, and (iii) genomic speciation via genome duplication. Geographic speciation has been the most widely documented to date and is a common speciation model across tropical Africa. We conclude with four important challenges faced by tropical African biodiversity research: (i) to increase knowledge by gathering basic and fundamental biodiversity information; (ii) to improve modelling of African geophysical evolution throughout the Cenozoic via better constraints and downscaling approaches; (iii) to increase the precision of phylogenetic reconstruction and molecular dating of tropical African clades by using next generation sequencing approaches together with better fossil calibrations; (iv) finally, as done here, to integrate data better from Earth and life sciences by focusing on the interdisciplinary study of the evolution of tropical African biodiversity in a wider geodiversity context.
Project description:<h4>Aim</h4>Despite the greatest butterfly diversity on Earth occurring in the Neotropical Andes and Amazonia, there is still keen debate about the origins of this exceptional biota. A densely sampled calibrated phylogeny for a widespread butterfly subtribe, Oleriina (Nymphalidae: Ithomiini) was used to estimate the origin, colonization history and diversification of this species-rich group.<h4>Location</h4>Neotropics.<h4>Methods</h4>Ancestral elevation and biogeographical ranges were reconstructed using data generated from detailed range maps and applying the dispersal-extinction-cladogenesis model using stratified palaeogeographical time slice matrices. The pattern of diversification through time was examined by comparing constant and variable rate models. We also tested the hypothesis that a change in elevation is associated with speciation.<h4>Results</h4>The Oleriina likely originated in the Andes in the Early to Middle Miocene and rapidly diversified to include four genera all of which also originated in the Andes. These clades, together with four species groups, experienced varying spatial and temporal patterns of diversification. An overall early burst and decreasing diversification rate is identified, and this pattern is reflected for most subclades.<h4>Main conclusions</h4>Changes in the palaeogeological landscape, particularly the prolonged uplift of the Andes, had a profound impact on the diversification of the subtribe. The Oleriina mostly remained within the Andes and vicariant speciation resulted in some instances. Dynamic dispersal occurred with the disappearance of geological barriers such as the Acre System and the subtribe exploited newly available habitats. Our results confirm the role of the Andean uplift in the evolution of Neotropical biodiversity.
Project description:Species radiations provide unique insights into evolutionary processes underlying species diversification and patterns of biodiversity. To compare plant diversification over a similar time period to the recent cichlid fish radiations, which are an order of magnitude faster than documented bird, arthropod, and plant radiations, we focus on the high-altitude flora of the Andes, which is the most species-rich of any tropical mountains. Because of the recent uplift of the northern Andes, the upland environments where much of this rich endemic flora is found have been available for colonization only since the late Pliocene or Pleistocene, 2-4 million years (Myr) ago. Using DNA sequence data we identify a monophyletic group within the genus Lupinus representing 81 species endemic to the Andes. The age of this clade is estimated to be 1.18-1.76 Myr, implying a diversification rate of 2.49-3.72 species per Myr. This exceeds previous estimates for plants, providing the most spectacular example of explosive plant species diversification documented to date. Furthermore, it suggests that the high cichlid diversification rates are not unique. Lack of key innovations associated with the Andean Lupinus clade suggests that diversification was driven by ecological opportunities afforded by the emergence of island-like habitats after Andean uplift. Data from other genera indicate that lupines are one of a set of similarly rapid Andean plant radiations, continental in scale and island-like in stimulus, suggesting that the high-elevation Andean flora provides a system that rivals other groups, including cichlids, for understanding rapid species diversification.
Project description:The Neotropics harbour the most diverse flora and fauna on Earth. The Andes are a major centre of diversification and source of diversity for adjacent areas in plants and vertebrates, but studies on insects remain scarce, even though they constitute the largest fraction of terrestrial biodiversity. Here, we combine molecular and morphological characters to generate a dated phylogeny of the butterfly genus Pteronymia (Nymphalidae: Danainae), which we use to infer spatial, elevational and temporal diversification patterns. We first propose six taxonomic changes that raise the generic species total to 53, making Pteronymia the most diverse genus of the tribe Ithomiini. Our biogeographic reconstruction shows that Pteronymia originated in the Northern Andes, where it diversified extensively. Some lineages colonized lowlands and adjacent montane areas, but diversification in those areas remained scarce. The recent colonization of lowland areas was reflected by an increase in the rate of evolution of species' elevational ranges towards present. By contrast, speciation rate decelerated with time, with no extinction. The geological history of the Andes and adjacent regions have likely contributed to Pteronymia diversification by providing compartmentalized habitats and an array of biotic and abiotic conditions, and by limiting dispersal between some areas while promoting interchange across others.
Project description:A common hypothesis for the rich biodiversity found in mountains is uplift-driven diversification-that orogeny creates conditions favoring rapid in situ speciation of resident lineages. We tested this hypothesis in the context of the Qinghai-Tibetan Plateau (QTP) and adjoining mountain ranges, using the phylogenetic and geographic histories of multiple groups of plants to infer the tempo (rate) and mode (colonization versus in situ diversification) of biotic assembly through time and across regions. We focused on the Hengduan Mountains region, which in comparison with the QTP and Himalayas was uplifted more recently (since the late Miocene) and is smaller in area and richer in species. Time-calibrated phylogenetic analyses show that about 8 million y ago the rate of in situ diversification increased in the Hengduan Mountains, significantly exceeding that in the geologically older QTP and Himalayas. By contrast, in the QTP and Himalayas during the same period the rate of in situ diversification remained relatively flat, with colonization dominating lineage accumulation. The Hengduan Mountains flora was thus assembled disproportionately by recent in situ diversification, temporally congruent with independent estimates of orogeny. This study shows quantitative evidence for uplift-driven diversification in this region, and more generally, tests the hypothesis by comparing the rate and mode of biotic assembly jointly across time and space. It thus complements the more prevalent method of examining endemic radiations individually and could be used as a template to augment such studies in other biodiversity hotspots.
Project description:Phylogenies recurrently demonstrate that oceanic island systems have been home to rapid clade diversification and adaptive radiations. The existence of adaptive radiations posits a central role of natural selection causing ecological divergence and speciation, and some plant radiations have been highlighted as paradigmatic examples of such radiations. However, neutral processes may also drive speciation during clade radiations, with ecological divergence occurring following speciation. Here, we document an exceptionally rapid and unique radiation of Lamiaceae within the New Caledonian biodiversity hotspot. Specifically, we investigated various biological, ecological, and geographical drivers of species diversification within the genus Oxera. We found that Oxera underwent an initial process of rapid cladogenesis likely triggered by a dramatic period of aridity during the early Pliocene. This early diversification of Oxera was associated with an important phase of ecological diversification triggered by significant shifts of pollination syndromes, dispersal modes, and life forms. Finally, recent diversification of Oxera appears to have been further driven by the interplay of allopatry and habitat shifts likely related to climatic oscillations. This suggests that Oxera could be regarded as an adaptive radiation at an early evolutionary stage that has been obscured by more recent joint habitat diversification and neutral geographical processes. Diversification within Oxera has perhaps been triggered by varied ecological and biological drivers acting in a leapfrog pattern, but geographic processes may have been an equally important driver. We suspect that strictly adaptive radiations may be rare in plants and that most events of rapid clade diversification may have involved a mixture of geographical and ecological divergence.
Project description:The cacti are one of the most celebrated radiations of succulent plants. There has been much speculation about their age, but progress in dating cactus origins has been hindered by the lack of fossil data for cacti or their close relatives. Using a hybrid phylogenomic approach, we estimated that the cactus lineage diverged from its closest relatives ?35 million years ago (Ma). However, major diversification events in cacti were more recent, with most species-rich clades originating in the late Miocene, ?10-5 Ma. Diversification rates of several cactus lineages rival other estimates of extremely rapid speciation in plants. Major cactus radiations were contemporaneous with those of South African ice plants and North American agaves, revealing a simultaneous diversification of several of the world's major succulent plant lineages across multiple continents. This short geological time period also harbored the majority of origins of C(4) photosynthesis and the global rise of C(4) grasslands. A global expansion of arid environments during this time could have provided new ecological opportunity for both succulent and C(4) plant syndromes. Alternatively, recent work has identified a substantial decline in atmospheric CO(2) ?15-8 Ma, which would have strongly favored C(4) evolution and expansion of C(4)-dominated grasslands. Lowered atmospheric CO(2) would also substantially exacerbate plant water stress in marginally arid environments, providing preadapted succulent plants with a sharp advantage in a broader set of ecological conditions and promoting their rapid diversification across the landscape.
Project description:Lineages arriving on islands may undergo explosive evolutionary radiations owing to the wealth of ecological opportunities. Although studies on insular taxa have improved our understanding of macroevolutionary phenomena, we know little about the macroevolutionary dynamics of continental exchanges. Here we study the evolution of eight Carnivora families that have migrated across the Northern Hemisphere to investigate if continental invasions also result in explosive diversification dynamics. We used a Bayesian approach to estimate speciation and extinction rates from a substantial dataset of fossil occurrences while accounting for the incompleteness of the fossil record. Our analyses revealed a strongly asymmetrical pattern in which North American lineages invading Eurasia underwent explosive radiations, whereas lineages invading North America maintained uniform diversification dynamics. These invasions into Eurasia were characterized by high rates of speciation and extinction. The radiation of the arriving lineages in Eurasia coincide with the decline of established lineages or phases of climate change, suggesting differences in the ecological settings between the continents may be responsible for the disparity in diversification dynamics. These results reveal long-term outcomes of biological invasions and show that the importance of explosive radiations in shaping diversity extends beyond insular systems and have significant impact at continental scales.
Project description:The relative importance of equilibrium and nonequilibrium processes in shaping patterns of species richness is one of the most fundamental questions in biodiversity studies. If equilibrium processes predominate, then ecological interactions presumably limit species diversity, potentially through diversity dependence of immigration, speciation, and extinction rates. Alternatively, species richness may be limited by the rate at which diversity arises or by the amount of time available for diversification. These latter explanations constitute nonequilibrium processes and can apply only to biotas that are unsaturated or far from diversity equilibria. Recent studies have challenged whether equilibrium models apply to biotas assembled through in situ speciation, as this process may be too slow to achieve steady-state diversities. Here we demonstrate that speciation rates in replicate Caribbean lizard radiations have undergone parallel declines to equilibrium conditions on three of four major islands. Our results suggest that feedback between total island diversity and per-capita speciation rates scales inversely with island area, with proportionately greater declines occurring on smaller islands. These results are consistent with strong ecological controls on species richness and suggest that the iconic adaptive radiation of Caribbean anoles may have reached an endpoint.