Speciation Rates Research Articles

What drove the evolutionary trend of planktic foraminifers during the Cretaceous: Oceanic Anoxic Events (OAEs) directly affected it?

Abstract The oceanic redox state has played an essential role in the evolution of life on earth, and oceanic “anoxic events” have been proposed as one of the causal mechanisms for mass extinctions. During the mid-Cretaceous, oceanic anoxic events (OAEs) occurred several times and had a substantial impact on the biosphere. Planktic foraminifers are marine planktons with calcite tests, and their shells constitute approximately 30%–80% of modern deep-marine calcite; thus, they play a key role in the global carbon cycle. Previous studies have reported that at, or near, the times of major Cretaceous OAEs, planktic foraminifers have a high turnover (extinction and speciation) rate. However, the precise impact of anoxic conditions on the evolutionary trend of planktic foraminifers remained obscure. In this study, we investigate this by assessing the extinction/speciation rate of planktic foraminifers around OAEs. Our results suggest that the development of anoxia during OAEs would not have had a direct effect on the evolutionary trend (i.e., species number and turnover ratio). Two foraminiferal turnovers occurred around OAE1a and OAE2, however, all five turnover peaks seem to be largely associated with a relatively short-term (0.5–3 Myr) eustatic curve. Decreasing species numbers of planktic foraminifers are associated with a relatively lower sea eustatic level (second-order; ~20 Myr) and a small latitudinal temperature gradient around OAE1b, which are not anoxic conditions. Changes in oceanographical parameters (i.e., surface biological productivity, water column structure, carbonate chemistry, and nutrients) related to lowering sea-levels might have had a significant effect on foraminiferal evolutionary trends.

Using full-length metabarcoding and DNA barcoding to infer community assembly for speciose taxonomic groups: a case study

How insect communities are assembled in nature remains largely unknown. In particular, whether habitat filtering or competition serves as the main mechanism in forming insect communities is rarely subject to an in-depth investigation. One bottleneck lies in the difficulty of species identification when dealing with a large number of diverse insects. However, high-throughput sequencing technology coupled with classic DNA barcoding offers a great opportunity to infer community assembly for this speciose group. In this study, using 13,909 full-length barcodes obtained by Sanger sequencing or the full-length metabarcoding method (SOAPBarcode), we showed that competition was the main assembly mechanism for the moth communities in the younger Taihang Mountain, while habitat filtering for those in the old Yanshan Mountain. The two sequencing methods showed highly consistent results with regards to both diversity composition and community assembly mechanism. Significant phylogenetic signals and structure suggested that the focal moth communities were the result of the non-neutral assembly process, which was further confirmed by results of neutral assembly test that accounted for immigration and speciation rates. Our study showed that the full-length metabarcoding method can facilitate community assembly inferences, even for speciose taxonomic groups.

Insectivorous birds in the Neotropics: Ecological radiations, specialization, and coexistence in species-rich communities

AbstractInsectivorous birds reach their highest diversity in the tropics and represent a striking variety of morphological and behavioral specializations for foraging, yet explanations for these patterns are inadequate because of both our limited understanding of the drivers of ecological diversification within and among clades and of coexistence mechanisms in particular. Here we synthesize recent information on Neotropical insectivorous birds, including their diversity, evolutionary ages and locations of origin, phylogenies, and both competitive and predator–prey species interactions. We propose a novel evolutionary hypothesis for the origin and coexistence of the phenotypic diversity of insectivore foraging morphologies in species-rich communities, based on their extraordinary food-resource specializations. Specifically, we develop the Biotic Challenge Hypothesis to explain the evolution of these specializations, and we provide preliminary evidence in support of this hypothesis based on a synopsis of both Neotropical insectivore specializations by family and arthropod antipredator adaptations by category. We argue that, from the perspective of tropical insectivorous birds, and particularly in the most species-rich, mainland Neotropical communities, the environment is an arthropod desert. Coexistence with all of the other insectivores requires feeding specialization to compete exploitatively and diffusely against evolutionarily diverse species and far less frequently against sister species. The arthropod desert arises primarily because of (1) the tactical diversity of arthropod predators as insectivore competitors and (2) the evolutionary arms races involving arthropod predators with their prey, which render many arthropods inaccessible to most insectivorous predators. Our idea provides an explicit mechanism for pervasive, diffuse tropical interspecific competition, for evolutionary specialization, and for positive feedback on speciation rates at low latitudes, thereby generating new predictions and insights into tropical life histories and the Latitudinal Diversity Gradient. Other recent ideas concerning the coexistence of Neotropical insectivores, including positive species interactions within mixed species flocks, are recognized and evaluated. We discuss ways to test predictions resulting from the new view of communities developed here, including a case study of diet specialization by Costa Rican tyrannid flycatchers. Our synthesis of the origin and nature of Neotropical insectivore communities injects new life into the “zombie” idea that evolution works differently in the species-rich tropics.

Modeling colonization rates over time: Generating null models and testing model adequacy in phylogenetic analyses of species assemblages.

A central theme connecting macroevolutionary processes to macroecological patterns is the shaping of regional biodiversity over time through speciation, extinction, migration, and range shifts. The use of phylogenies to explore the dynamics of diversification due to variation in speciation and extinction rates has been well-developed and there are established methods for inferring speciation times from phylogenies and generating its null distributions (as represented by node heights on molecular phylogenies). But inferring colonization events from phylogenies is more challenging. Unlike speciation events, represented by nodes, colonization events could occur at any point along a branch connecting species in the assemblage to the regional pool. We account for uncertainty in identification of colonization lineages and timing of colonization events by using an efficient analytical solution to inferring the distribution of colonization times from an assemblage phylogeny. Using the same solution, we efficiently derive the null distribution of colonization times, which provides us with a general approach to testing the adequacy of a model to describe colonization events into the assemblage. We illustrate this approach by demonstrating how the movement of squamate lineages into Madagascar has been uneven over time, peaking in the early Cenozoic when ocean conditions favored colonization.

Do key innovations unlock diversification? A case-study on the morphological and ecological impact of pharyngognathy in acanthomorph fishes.

Key innovations may allow lineages access to new resources and facilitate the invasion of new adaptive zones, potentially influencing diversification patterns. Many studies have focused on the impact of key innovations on speciation rates, but far less is known about how they influence phenotypic rates and patterns of ecomorphological diversification. We use the repeated evolution of pharyngognathy within acanthomorph fishes, a commonly cited key innovation, as a case study to explore the predictions of key innovation theory. Specifically, we investigate whether transitions to pharyngognathy led to shifts in the rate of phenotypic evolution, as well as shifts and/or expansion in the occupation of morphological and dietary space, using a dataset of 8 morphological traits measured across 3,853 species of Acanthomorpha. Analyzing the 6 evolutionarily independent pharyngognathous clades together, we found no evidence to support pharyngognathy as a key innovation; however, comparisons between individual pharyngognathous lineages and their sister clades did reveal some consistent patterns. In morphospace, most pharyngognathous clades cluster in areas that correspond to deeper-bodied morphologies relative to their sister clades, while occupying greater areas in dietary space that reflects a more diversified diet. Additionally, both Cichlidae and Labridae exhibited higher univariate rates of phenotypic evolution compared with their closest relatives. However, few of these results were exceptional relative to our null models. Our results suggest that transitions to pharyngognathy may only be advantageous when combined with additional ecological or intrinsic factors, illustrating the importance of accounting for lineage-specific effects when testing key innovation hypotheses. Moreover, the challenges we experienced formulating informative comparisons, despite the ideal evolutionary scenario of multiple independent evolutionary origins of pharyngognathous clades, illustrates the complexities involved in quantifying the impact of key innovations. Given the issues of lineage specific effects and rate heterogeneity at macroevolutionary scales we observed, we suggest a reassessment of the expected impacts of key innovations may be warranted.

Phylogeny, Evolution, and Biogeography of the North American Trapdoor Spider Family Euctenizidae (Araneae: Mygalomorphae) and the Discovery of a New ‘Endangered Living Fossil’ Along California’s Central Coast

Abstract We report here the discovery of a remarkable new monotypic mygalomorph spider genus, known only from one geographical location along the central coast of California. The single relict species comprising Cryptocteniza kawtakn. gen. n. sp., is morphologically distinct and geographically isolated from other related genera, with its closest phylogenetic relatives found much further to the east in New Mexico and Arizona. Using a phylogenomic approach employing anchored hybrid enrichment, we reconstruct the evolutionary history of the family Euctenizidae Raven, 1985 to explore relationships among genera, affirmatively place previously undescribed taxa, explore rates of diversification, and reconstruct the group’s biogeography. A biogeographic analysis shows that extinction likely played a significant role in shaping the observed disjunct modern-day distribution of Cryptocteniza and its sister taxa. Our extinction hypothesis is further bolstered by a diversification rate analysis identifying considerably higher rates of speciation in other euctenizid lineages like AptostichusSimon, 1891. Consequently, changes in environmental conditions (or other related biotic and/or abiotic factors) may have spurred an adaptive radiation in related genera now widely distributed across the California Floristic Province biodiversity hotspot, with concomitant extinction in Cryptocteniza following the Miocene and establishment of a Mediterranean climate. Owing to its phylogenetic distinctiveness, incredibly narrow distribution and age, we show that Cryptocteniza meets all the criteria of an ‘Endangered Living Fossil’ and is consequently of grave conservation concern.

Modeling the Evolution of Aquatic Organisms in Dynamic River Basins

AbstractRivers are conduits for aquatic organisms and host an exceptional number of species. Over geologic time, rivers and the aquatic organisms that live in them are subject to changes in topography that can alter where rivers flow. Differences in erosion rates across drainage divides cause some river basins to grow and others to shrink. Occasionally, rivers are abruptly rerouted by river captures that create both new dispersal corridors and barriers for aquatic organisms. These changes in habitat connectivity can lead to the evolution of new species, which has prompted suggestions that river captures may be a mechanism to produce high freshwater biodiversity. We test this hypothesis by building a model, Bio‐SLANT (Biodiversity on Simulated LAndscapes using Neutral Theory). Bio‐SLANT couples a computational landscape model that simulates river basin reorganization to a macroevolutionary model that simulates the dispersal, speciation, and extinction of organisms. We first show that modeled basin area exerts a primary control on within‐basin species richness due to the species‐area relationship. We then describe the effects of drainage area exchange between river basins. River capture increases species richness, but only temporarily, whereas elevated rates of speciation and extinction provide a persistent biological record of river network reorganization. When river captures are frequent, speciation rates increase more than extinction rates, resulting in a positive diversification rate under most of the biological parameters tested. We explore the implications of our results for species richness in landscapes with basins of different relative sizes and for diversification in tectonically active and inactive settings.

Dimensions of amphibian alpha diversity in the New World

AbstractAimThe links between taxonomic, functional, and phylogenetic diversity and how these vary geographically are key to understanding how historical and contemporary processes have shaped communities at regional and local scales. Here, we evaluate the links between taxonomic, functional and phylogenetic diversity for the amphibians in the Continental Americas and how these vary geographically under an explicit hypothesis testing framework.LocationContinental Americas.TaxonAmphibia.MethodsWe identify spatial disparities between biodiversity dimensions (taxonomic, functional and phylogenetic) using geographically weighted regressions. Based on these mismatches we examined whether different eco‐evolutionary processes would fit (competitive exclusion, habitat filtering, available ecological space, strong biotic interactions, speciation rates, and dispersion).ResultsWe found extensive variation in spatial mismatches between the three dimensions of biodiversity examined here. In general, at higher latitudes, we detected relatively little phylogenetic diversity, suggesting rapid functional diversification from temperate clades. In contrast, at low latitudes, environmental filtering mechanisms appear to be restricting functional diversity.Main conclusionsThe geographical mismatches between dimensions of diversity suggest different eco‐evolutionary causes. Patterns of diversification across amphibian lineages demonstrate how different environments can have contrasting effects on the different dimensions of diversity, potentially leading to decoupling. Neither dimension of alpha diversity of amphibians is a general predictor for another, and thus, general explanations for amphibian diversity and evolution should be avoided. Nonetheless, these dimensions can provide critical insights about conservation measures that explicitly emphasize evolutionary history, functionality or classic species richness.

The ecological and genomic basis of explosive adaptive radiation.

Speciation rates vary considerably among lineages, and our understanding of what drives the rapid succession of speciation events within young adaptive radiations remains incomplete1-11. The cichlid fish family provides a notable example of such variation, with many slowly speciating lineages as well as several exceptionallylarge and rapid radiations12. Here, by reconstructing a large phylogeny of all currently described cichlid species, we show that explosive speciation is solely concentrated in species flocks of several large young lakes. Increases in the speciation rate are associated with the absence of top predators; however, this does not sufficiently explain explosive speciation. Across lake radiations, we observe a positive relationship between the speciation rate and enrichment of large insertion or deletion polymorphisms. Assembly of 100 cichlid genomes within the most rapidly speciating cichlid radiation, which is found in Lake Victoria, reveals exceptional 'genomic potential'-hundreds of ancient haplotypes bear insertion or deletion polymorphisms, many of which are associated with specific ecologies and shared with ecologically similar species from other older radiations elsewhere in Africa. Network analysis reveals fundamentally non-treelike evolution through recombining old haplotypes, and the origins of ecological guilds are concentrated early in the radiation. Our results suggest that the combination of ecological opportunity, sexual selection and exceptional genomic potential is the key to understanding explosive adaptive radiation.

POPOVICH, encoding a C2H2 zinc-finger transcription factor, plays a central role in the development of a key innovation, floral nectar spurs, in Aquilegia

The evolution of novel features, such as eyes or wings, that allow organisms to exploit their environment in new ways can lead to increased diversification rates. Therefore, understanding the genetic and developmental mechanisms involved in the origin of these key innovations has long been of interest to evolutionary biologists. In flowering plants, floral nectar spurs are a prime example of a key innovation, with the independent evolution of spurs associated with increased diversification rates in multiple angiosperm lineages due to their ability to promote reproductive isolation via pollinator specialization. As none of the traditional plant model taxa have nectar spurs, little is known about the genetic and developmental basis of this trait. Nectar spurs are a defining feature of the columbine genus Aquilegia (Ranunculaceae), a lineage that has experienced a relatively recent and rapid radiation. We use a combination of genetic mapping, gene expression analyses, and functional assays to identify a gene crucial for nectar spur development, POPOVICH (POP), which encodes a C2H2 zinc-finger transcription factor. POP plays a central role in regulating cell proliferation in the Aquilegia petal during the early phase (phase I) of spur development and also appears to be necessary for the subsequent development of nectaries. The identification of POP opens up numerous avenues for continued scientific exploration, including further elucidating of the genetic pathway of which it is a part, determining its role in the initial evolution of the Aquilegia nectar spur, and examining its potential role in the subsequent evolution of diverse spur morphologies across the genus.

Latitudinal gradient of termite diversity indicates higher diversification and narrower thermal niches in the tropics

AbstractAimTo investigate the contributions of ecosystem productivity, temperature‐dependent metabolism and climatic tolerances to the latitudinal gradient in species richness and changes in species composition in tropical and subtropical regions.LocationGlobal.Time periodContemporary.Major taxa studiedTermites.MethodsWe compiled termite occurrence data from papers using the standardized sampling protocol proposed 20 years ago by Jones and Eggleton. Three continents, 28 countries and 494 sampling plots were included in our database. We used structural equation models to determine the direct and indirect effects of productivity, and the average and extreme values of temperature and precipitation on termite species richness. We also compared the observed association between diversity and temperature with predictions from the metabolic theory of ecology and compared how the similarity in species composition relates to geographic distance and environmental differences in tropical versus subtropical regions.ResultsTermite species richness was, directly and indirectly, related to average and extreme temperatures, but not to productivity. However, the association of species richness and temperature was much stronger than predicted by the metabolic theory of ecology. Moreover, species composition changed more rapidly with geographic distance and temperature differences between plots in the tropics than in the subtropics.Main conclusionsThese results suggest that the increase of species richness toward the equator cannot be explained by productivity gradients. Instead, the increase in the speciation rates and the narrow species niches along the temperature gradient in tropical regions likely determine the distribution of termites at broad spatial scales.

Does migration promote or inhibit diversification? A case study involving the dominant radiation of temperate Southern Hemisphere freshwater fishes.

Although theory predicts that dispersal has a pivotal influence on speciation and extinction rates, it can have contradictory effects on each, such that empirical quantification of its role is required. In many studies, dispersal reduction appears to promote diversification, although some comparisons of migratory and nonmigratory species suggest otherwise. We tested for a relationship between migratory status and diversification rate within the dominant radiation of temperate Southern Hemisphere freshwater fishes, the Galaxiidae. We reconstructed a molecular phylogeny comprising >95% of extant taxa, and applied State-dependent Speciation Extinction models to estimate speciation, extinction, and diversification rates. In contrast to some previous studies, we revealed higher diversification rates in nonmigratory lineages. The reduced gene flow experienced by nonmigratory galaxiids appears to have increased diversification under conditions of allopatry or local adaptation. Migratory galaxiid lineages, by contrast, are genetically homogeneous within landmasses, but may also be rarely able to diversify by colonizing other landmasses in the temperate Southern Hemisphere. Apparent contradictions among studies of dispersal-diversification relationships may be explained by the spatial context of study systems relative to species dispersal abilities, by means of the "intermediate dispersal" model; the accurate quantification of dispersal abilities will aid in the understanding of these proposed interactions.

Changes in Sedimentary Phosphorus Burial Following Artificial Eutrophication of Lake 227, Experimental Lakes Area, Ontario, Canada

AbstractLake 227 of the Experimental Lakes Area (ELA) in Ontario, Canada, has been fertilized with phosphorus (P) since 1969, which resulted in a rapid transition from oligotrophic to eutrophic conditions. Sediment cores collected from the oxygenated epilimnion, and the mostly anoxic hypolimnion of this unique lake contain a historical record of the changes in sediment P speciation and burial rates across the trophic transition. To elucidate these changes, results of chemical extractions were combined with 210Pb sediment dating, and with 31P NMR, Mössbauer, and XANES spectroscopies. Prior to 1969, organic P (POrg) was the major sedimentary P sink in Lake 227. Eutrophication of the lake coincided with marked increases in the burial rate of total P (TP), as well as in the relative contribution of the NaHCO3‐extractable P pool (humic‐bound P, PHum). Together, PHum and POrg account for ≥70% of total P burial in the sediments deposited since artificial fertilization started. The PHum fraction likely comprises phosphate complexes with humic substances. The strong linear correlation between P and iron (Fe) extracted by NaHCO3 implies a close association of the two elements in the humic fraction. Mössbauer and XANES spectra further indicate that most Fe in the post‐1969 sediments remained in the Fe (III) oxidation state, which is attributed to the stabilization of reducible Fe by organic matter, in part via the formation of phosphate‐Fe (III)‐humic complexes. Importantly, our results show that the eutrophication experimentation of Lake 227 caused the accumulation of a large reservoir of reactive sediment P, which may continue to fuel internal P loading to the water column once artificial fertilization is terminated.

Spatiotemporal Diversification of Tree Squirrels: Is the South American Invasion and Speciation Really That Recent and Fast?

Tree squirrels (Sciurinae, Sciurini) represent a diverse radiation that successfully colonized Europe, Asia and the Americas during the Miocene-Pliocene, but information on their evolutionary history remains unclear. In the Neotropics, they have been shown to exhibit the highest rate of diversification amongst all arboreal squirrels, with strikingly high species accumulation rates in the past 3 My. In this study, we investigated the tempo and mode of diversification of tree squirrels using a mitogenome dataset that includes 43 Sciurini species. Our results corroborate the date of origin of the tribe Sciurini around 14 Mya (13.4-15.5) but suggest that their ancestral area was most likely in North America. This is in contrast to previous findings that suggested that the ancestors of this tribe occupied Eurasia. We estimated that cladogenetic events leading to the Eurasian lineages occurred twice at 10.5 and 9.7 Mya. Current North American genera originated in a temporal window from 6.2 to 2.3 Mya, and the origin of the Neotropical radiation was estimated to have occurred around 6 Mya in northwestern South America in the Pacific dominion. Remarkably, our results indicate that tree squirrels entered South America at an earlier date than previously estimated. This could have happened either through a land corridor connecting the Caribbean islands or through the Panamanian land bridge. Most cladogenetic events in Eurasia and North America appear to have occurred either late in the Miocene or in the Pleistocene, while the majority of Neotropical cladogenetic events occurred along the Pliocene—right after the South American invasion. We found a fairly constant speciation rate for tree squirrels (averaging 0.29), which contrasts with the peak of lineage accumulation observed in the Pliocene. The absence of fluctuations in the diversification rate may be the result of several extinction events that were responsible for equalizing the number of lineages maintained over time. Finally, we conclude that the South American invasion was not as recent as previously inferred, but the diversification there was indeed very fast.

Speciation through chromosomal fusion and fission in Lepidoptera.

Changes in chromosome numbers may strongly affect reproductive barriers, because individuals heterozygous for distinct karyotypes are typically expected to be at least partially sterile or to show reduced recombination. Therefore, several classic speciation models are based on chromosomal changes. One import mechanism generating variation in chromosome numbers is fusion and fission of existing chromosomes, which is particularly likely in species with holocentric chromosomes, i.e. chromosomes that lack a single centromere. Holocentric chromosomes evolved repeatedly across the tree of life, including in Lepidoptera. Although changes in chromosome numbers are hypothesized to be an important driver of the spectacular diversification of Lepidoptera, comparative studies across the order are lacking. We performed the first comprehensive literature survey of karyotypes for Lepidoptera species since the 1970s and tested if, and how, chromosomal variation might affect speciation. Even though a meta-analysis of karyological differences between closely related taxa did not reveal an effect on the degree of reproductive isolation, phylogenetic diversification rate analyses across the 16 best-covered genera indicated a strong, positive association of rates of chromosome number evolution and speciation. These findings suggest a macroevolutionary impact of varying chromosome numbers in Lepidoptera and likely apply to other taxonomic groups, especially to those with holocentric chromosomes. This article is part of the theme issue 'Towards the completion of speciation: the evolution of reproductive isolation beyond the first barriers'.

Lake expansion elevates equilibrium diversity via increasing colonization

AbstractAimRates of colonization, speciation and extinction determine species richness and endemism in insular systems. The general dynamic model of island biogeography (GDM) predicts that speciation and extinction rates depend on island area and elevation via their control on ecological limits to diversification and therefore covary with an island's geological history. Additionally, the colonization rate may increase with area and elevation through the ‘target effect’, which can be mediated by reduced ‘environmental filtering’. Here we test whether the area and depth expansion of an island‐like ecosystem, a lake, caused a shift in diversity dynamics.LocationLake Biwa, Japan, whose geological history and biota are well documented.TaxonFishes.MethodsWe extended the phylogenetic island biogeography framework DAISIE (Dynamic Assembly of Island biota through Speciation, Immigration and Extinction) to accommodate time‐shifts in macroevolutionary rates and in carrying capacity. Using phylogenetic information on colonization and speciation times for the complete Lake Biwa fish community (70 taxa), we tested for a shift in macroevolutionary assembly rates and reconstructed the temporal diversity trajectory in the lake. We assessed the power to identify a shift through a wide range of scenarios and benchmarked against simulated fossil records.ResultsWe detected an increase in colonization rate of fishes at 0.2 million years ago (Ma), with limited support for the existence of ecological limits. The reconstructed diversity trajectory was close to a source‐sink equilibrium diversity prior to the shift and remained well below a new shift‐driven elevated equilibrium thereafter. We found sufficient power to identify an increase in colonization rate up to 1.5 Ma, whereas extinction concealed the signal of earlier shifts.Main conclusionsThe fish diversity dynamics of Lake Biwa show a response to changes in area and depth and phylogenies carry a signature of these changes. The detected increase in colonization rate following Lake Biwa's expansion, elevating the fish diversity, is unlikely due to a predicted increase in ecological limits feeding back on colonization rate. We therefore call for (additional) explanations: the target effect, whereby larger islands attract more species, and reduced environmental filtering due to higher habitat diversity associated with increased lake area/depth.

Recent accelerated diversification in rosids occurred outside the tropics

Conflicting relationships have been found between diversification rate and temperature across disparate clades of life. Here, we use a supermatrix comprising nearly 20,000 species of rosids—a clade of ~25% of all angiosperm species—to understand global patterns of diversification and its climatic association. Our approach incorporates historical global temperature, assessment of species’ temperature niche, and two broad-scale characterizations of tropical versus non-tropical niche occupancy. We find the diversification rates of most subclades dramatically increased over the last 15 million years (Myr) during cooling associated with global expansion of temperate habitats. Climatic niche is negatively associated with diversification rates, with tropical rosids forming older communities and experiencing speciation rates ~2-fold below rosids in cooler climates. Our results suggest long-term cooling had a disproportionate effect on non-tropical diversification rates, leading to dynamic young communities outside of the tropics, while relative stability in tropical climes led to older, slower-evolving but still species-rich communities.

Heterogeneity in the rate of molecular sequence evolution substantially impacts the accuracy of detecting shifts in diversification rates.

As species richness varies along the tree of life, there is a great interest in identifying factors that affect the rates by which lineages speciate or go extinct. To this end, theoretical biologists have developed a suite of phylogenetic comparative methods that aim to identify where shifts in diversification rates had occurred along a phylogeny and whether they are associated with some traits. Using these methods, numerous studies have predicted that speciation and extinction rates vary across the tree of life. In this study, we show that asymmetric rates of sequence evolution lead to systematic biases in the inferred phylogeny, which in turn lead to erroneous inferences regarding lineage diversification patterns. The results demonstrate that as the asymmetry in sequence evolution rates increases, so does the tendency to select more complicated models that include the possibility of diversification rate shifts. These results thus suggest that any inference regarding shifts in diversification pattern should be treated with great caution, at least until any biases regarding the molecular substitution rate have been ruled out.

The role of the Neotropics as a source of world tetrapod biodiversity

AbstractAimThe Neotropics currently host outstanding levels of species richness, with one‐third of the global tetrapod species. The underlying causes of these extraordinary levels of biodiversity are a topic debated in evolutionary ecology, but the main processes at work remain elusive.LocationNeotropics.Time periodCenozoic and Mesozoic.Major taxa studiedTetrapods.MethodsUsing global phylogenies for amphibians, birds, lepidosaurs and mammals, biogeographical and time‐variable (trait‐dependent and trait‐independent) diversification models, we examined changes in speciation and extinction rates through time in the Neotropics in relationship to other areas of the world, and estimated the time of Neotropical colonizations.ResultsWe found that from the origin of lepidosaurs and mammals until the Pliocene (the Miocene for birds), diversification rates within the Neotropics were lower than rates in other regions (i.e., turnover was high). Afterwards, extinction decreased relative to speciation, and Neotropical diversification outpaced diversification in other regions. Dispersal out of the Neotropics also increased after the Pliocene (the Miocene for birds), exceeding into‐the‐Neotropics migrations. For amphibians, diversification rates in the Neotropics have been higher than in other areas through time, and dispersal out of the Neotropics decreased in the Cenozoic.Main conclusionsThe common view that the Neotropics are an ancient source of world species diversity, with high in situ speciation, dispersal to other areas and low extinction, might be true only for amphibians. For mammals, birds and lepidosaurs, the Neotropics acted as a diversity sink from their origin until the Miocene–Pliocene (i.e., diversification rates were lower and turnover higher than in other areas). Only afterwards did the region turn into a diversity source. Our study highlights that models accounting for rates of diversification that vary through time could improve our capacity to assess evolutionary dynamics over long time‐scales.

Diversification of African Rainforest Restricted Clades: Piptostigmateae and Annickieae (Annonaceae)

African rainforests (ARFs) are species rich and occur in two main rainforest blocks: West/Central and East Africa. This diversity is suggested to be the result of recent diversification, high extinction rates and multiple vicariance events between west/central and East African forests. We reconstructed the diversification history of two subtribes (Annickieae and Piptostigmateae) from the ecologically dominant and diverse tropical rainforest plant family Annonaceae. Both tribes contain endemic taxa in the rainforests of West/Central and East Africa. Using a dated molecular phylogeny based on 32 nuclear markers, we estimated the timing of the origin of East African species. We then undertook several diversification analyses focusing on Piptostigmateae to infer variation in speciation and extinction rates, and test the impact of extinction events. Speciation in both tribes dated to the Pliocene and Pleistocene. In particular, Piptostigma (13 species) diversified mainly during the Pleistocene, representing one of the few examples of Pleistocene speciation in an African tree genus. Our results also provide evidence of an ARF fragmentation at the mid-Miocene linked to climatic changes across the region. Overall, our results suggest that continental-wide forest fragmentation during the Neogene (23.03–2.58 Myr), and potentially during the Pliocene, led to one or possibly two vicariance events within the ARF clade Piptostigmateae, in line with other studies. Among those tested, the best fitting diversification model was the one with an exponential speciation rate and no extinction. We did not detect any evidence of mass extinction events. This study gives weight to the idea that the ARF might not have been so negatively impacted by extinction during the Neogene, and that speciation mainly took place during the Pliocene and Pleistocene.