Global variation in diversification rates of flowering plants: energy vs. climate change

We used the largest DNA-based phylogeny of flowering plants to date to evaluate the importance of energy vs. past climate change in predicting global patterns in diversification. Relative diversification rates increased towards the equator, suggesting that differences in per-lineage net diversification may be an important component of the latitudinal diversity gradient. The amplitude of Quaternary climate oscillations experienced by families explained variation in diversification equally well compared to contemporary energy measures, and energy and climate change measures were intercorrelated, making it difficult to reject either as a causal mechanism. Many putative mechanisms linking diversification to energy availability do not apply to plants, whereas the climate change mechanism has more support. We also present the first global map of angiosperm diversification, showing that, after correcting for family range-size, tropical diversification rates were fastest for clades currently in regions with high endemic species richness outside the main lowland rainforest areas.     

High tropical net diversification drives the New World latitudinal gradient in palm (Arecaceae) species richness

Aim Species richness exhibits striking geographical variation, but the processes that drive this variation are unresolved. We investigated the relative importance of two hypothesized evolutionary causes for the variation in palm species richness across the New World: time for diversification and evolutionary (net diversification) rate. Palms have a long history in the region, with the major clades diversifying during the Tertiary (65–2 Ma). Location Tropical and subtropical America (34° N–34° S; 33–120° W). Methods Using range maps, palm species richness was estimated in a 1° × 1° grid. Mean lineage net diversification was estimated by the mean phylogenetic root distance (MRD), the average number of nodes separating a species from the base of the palm phylogeny for the species in each grid cell. If evolutionary rate limits richness, then richness should increase with MRD. If time limits richness, then old, relict species (with low root distance) should predominantly occur in long‐inhabited and therefore species‐rich areas. Hence, richness should decrease with MRD. To determine the influence of net diversification across different time frames, MRD was computed for subtribe, genus and species levels within the phylogeny, and supplemented with the purely tip‐level measure, mean number of species per genus (MS/G). Correlations and regressions, in combination with eigenvector‐based spatial filtering, were used to assess the relationship between species richness, the net diversification measures, and potential environmental and geographical drivers. Results Species richness increased with all net diversification measures. The regression models showed that richness and the net diversification measures increased with decreasing (absolute) latitude and, less strongly, with increasing energy/temperature and water availability. These patterns therefore reflect net diversification at both deep and shallow levels in the phylogeny. Richness also increased with range in elevation, but this was only reflected in the MS/G pattern and therefore reflects recent diversification. Main conclusions The geographical patterns in palm species richness appear to be predominantly the result of elevated net diversification rates towards the equator and in warm, wet climates, sustained throughout most of the Tertiary. Late‐Tertiary orogeny has caused localized increases in net diversification rates that have also made a mark on the richness pattern.     

Evolutionary diversification of reef corals: a comparison of the molecular and fossil records

Understanding historical patterns of diversity dynamics is of paramount importance for many evolutionary questions. The fossil record has long been the only source of information on patterns of diversification, but the molecular record, derived from time-calibrated phylogenies, is becoming an important additional resource. Both fossil and molecular approaches have shortcomings and biases. These have been well studied for fossil data but much less so for molecular data and empirical comparisons between approaches are lacking. Here, we compare the patterns of diversification derived from fossil and molecular data in scleractinian reef coral species. We also assess the robustness of molecular diversification rates to poor taxon sampling. We find that the temporal pattern of molecular diversification rates is robust to incomplete sampling when rates are calculated per interval. The major obstacle of molecular methods is that rate estimates are distorted because diversification rates can never be negative, whereas the fossil record suffers from incomplete preservation and inconsistent taxonomy. Nevertheless, the molecular pattern of diversification is comparable to the pattern we observe in the fossil record, with the timing of major diversification pulses coinciding in each dataset. For example, both agree that the end-Triassic coral extinction was a catastrophic bottleneck in scleractinian evolution.     

Environmental causes for plant biodiversity gradients

One of the most pervasive patterns observed in biodiversity studies is the tendency for species richness to decline towards the poles. One possible explanation is that high levels of environmental energy promote higher species richness nearer the equator. Energy input may set a limit to the number of species that can coexist in an area or alternatively may influence evolutionary rates. Within flowering plants (angiosperms), families exposed to a high energy load tend to be both more species rich and possess faster evolutionary rates, although there is no evidence that one drives the other. Specific environmental effects are likely to vary among lineages, reflecting the interaction between biological traits and environmental conditions in which they are found. One example of this is demonstrated by the high species richness of the iris family (Iridaceae) in the Cape of South Africa, a likely product of biological traits associated with reproductive isolation and the steep ecological and climatic gradients of the region. Within any set of conditions some lineages will tend to be favoured over others; however, the identity of these lineages will fluctuate with a changing environment, explaining the highly labile nature of diversification rates observed among major lineages of flowering plants.     

Morphological disparity opposes latitudinal diversity gradient in lacertid lizards

While global variation in taxonomic diversity is strongly linked to latitude, the extent to which morphological disparity follows geographical gradients is less well known. We estimated patterns of lineage diversification, morphological disparity and rates of phenotypic evolution in the Old World lizard family Lacertidae, which displays a nearly inverse latitudinal diversity gradient with decreasing species richness towards the tropics. We found that lacertids exhibit relatively constant rates of lineage accumulation over time, although the majority of morphological variation appears to have originated during recent divergence events, resulting in increased partitioning of disparity within subclades. Among subclades, tropical arboreal taxa exhibited the fastest rates of shape change while temperate European taxa were the slowest, resulting in an inverse relationship between latitudinal diversity and rates of phenotypic evolution. This pattern demonstrates a compelling counterexample to the ecological opportunity theory of diversification, suggesting an uncoupling of the processes generating species diversity and morphological differentiation across spatial scales.     

Divergent timing and patterns of species accumulation in lowland and highland neotropical birds

Late Pliocene and Pleistocene climatic instability has been invoked to explain the buildup of Neotropical biodiversity, although other theories date Neotropical diversification to earlier periods. If these climatic fluctuations drove Neotropical diversification, then a large proportion of species should date to this period and faunas should exhibit accelerated rates of speciation. However, the unique role of recent climatic fluctuations in promoting diversification could be rejected if late Pliocene and Pleistocene rates declined. To test these temporal predictions, dateable molecular phylogenies for 27 avian taxa were used to contrast the timing and rates of diversification in lowland and highland Neotropical faunas. Trends in diversification rates were analyzed in two ways. First, rates within taxa were analyzed for increasing or decreasing speciation rates through time. There was a significant trend within lowland taxa towards decreasing speciation rates, but no significant trend was observed within most highland taxa. Second, fauna wide diversification rates through time were estimated during one-million-year intervals by combining rates across taxa. In the lowlands, rates were highest during the late Miocene and then decreased towards the present. The decline in rates observed both within taxa and for the fauna as a whole probably resulted from density dependent cladogenesis. In the highlands, faunawide rates did not vary greatly before the Pleistocene but did increase significantly during the last one million years of the Pleistocene following the onset of severe glacial cycles in the Andes. These contrasting patterns of species accumulation suggest that lowland and highland regions were affected differently by recent climatic fluctuations. Evidently, habitat alterations associated with global climate change were not enough to promote an increase in the rate of diversification in lowland faunas. In contrast, direct fragmentation of habitats by glaciers and severe altitudinal migration of montane vegetation zones during climatic cycles may have resulted in the late Pleistocene increase in highland diversification rates. This increase resulted in a fauna with one third of its species dating to the last one million years.     

Tightly congruent bursts of lineage and phenotypic diversification identified in a continental ant radiation

Adaptive diversification is thought to be shaped by ecological opportunity. A prediction of this ecological process of diversification is that it should result in congruent bursts of lineage and phenotypic diversification, but few studies have found this expected association. Here, we study the relationship between rates of lineage diversification and body size evolution in the turtle ants, a diverse Neotropical clade. Using a near complete, time‐calibrated phylogeny we investigated lineage diversification dynamics and body size disparity through model fitting analyses and estimation of per‐lineage rates of cladogenesis and phenotypic evolution. We identify an exceptionally high degree of congruence between the high rates of lineage and body size diversification in a young clade undergoing renewed diversification in the ecologically distinct Chacoan biogeographical region of South America. It is likely that the region presented turtle ants with novel ecological opportunity, which facilitated a nested burst of diversification and phenotypic evolution within the group. Our results provide a compelling quantitative example of tight congruence between rates of lineage and phenotypic diversification, meeting the key predicted pattern of adaptive diversification shaped by ecological opportunity.     

Cultural phylogeography of the Bantu Languages of sub-Saharan Africa

There is disagreement about the routes taken by populations speaking Bantu languages as they expanded to cover much of sub-Saharan Africa. Here, we build phylogenetic trees of Bantu languages and map them onto geographical space in order to assess the likely pathway of expansion and test between dispersal scenarios. The results clearly support a scenario in which groups first moved south through the rainforest from a homeland somewhere near the Nigeria–Cameroon border. Emerging on the south side of the rainforest, one branch moved south and west. Another branch moved towards the Great Lakes, eventually giving rise to the monophyletic clade of East Bantu languages that inhabit East and Southeastern Africa. These phylogenies also reveal information about more general processes involved in the diversification of human populations into distinct ethnolinguistic groups. Our study reveals that Bantu languages show a latitudinal gradient in covering greater areas with increasing distance from the equator. Analyses suggest that this pattern reflects a true ecological relationship rather than merely being an artefact of shared history. The study shows how a phylogeographic approach can address questions relating to the specific histories of certain groups, as well as general cultural evolutionary processes.     

High speciation rate at temperate latitudes explains unusual diversity gradients in a clade of ectomycorrhizal fungi

Understanding the patterns of biodiversity through time and space is a challenging task. However, phylogeny‐based macroevolutionary models allow us to account and measure many of the processes responsible for diversity buildup, namely speciation and extinction. The general latitudinal diversity gradient (LDG) is a well‐recognized pattern describing a decline in species richness from the equator polewards. Recent macroecological studies in ectomycorrhizal (EM) fungi have shown that their LDG is shifted, peaking at temperate rather than tropical latitudes. Here we investigate this phenomenon from a macroevolutionary perspective, focusing on a well‐sampled group of edible EM mushrooms from the genus Amanita—the Caesar's mushrooms, which follow similar diversity patterns. Our approach consisted in applying a suite of models including (1) nontrait‐dependent time‐varying diversification (Bayesian analysis of macroevolutionary mixtures [BAMM]), (2) continuous trait‐dependent diversification (quantitative‐state speciation and extinction [QuaSSE]), and (3) diversity‐dependent diversification. In short, results give strong support for high speciation rates at temperate latitudes (BAMM and QuaSSE). We also find some evidence for different diversity‐dependence thresholds in “temperate” and “tropical” subclades, and little differences in diversity due to extinction. We conclude that our analyses on the Caesar's mushrooms give further evidence of a temperate‐peaking LDG in EM fungi, highlighting the importance and the implications of macroevolutionary processes in explaining diversity gradients in microorganisms.     

Rapid allopatric speciation in logperch darters (Percidae: Percina)

Theory predicts that clades diversifying via sympatric speciation will exhibit high diversification rates. However, the expected rate of diversification in clades characterized by allopatric speciation is less clear. Previous studies have documented significantly higher speciation rates in freshwater fish clades diversifying via sympatric versus allopatric modes, leading to suggestions that the geographic pattern of speciation can be inferred solely from knowledge of the diversification rate. We tested this prediction using an example from darters, a clade of approximately 200 species of freshwater fishes endemic to eastern North America. A resolved phylogeny was generated using mitochondrial DNA gene sequences for logperches, a monophyletic group of darters composed of 10 recognized species. Divergence times among logperch species were estimated using a fossil calibrated molecular clock in centrarchid fishes, and diversification rates in logperches were estimated using several methods. Speciation events in logperches are recent, extending from 4.20 +/- 1.06 million years ago (mya) to 0.42 +/- 0.22 mya, with most speciation events occurring in the Pleistocene. Diversification rates are high in logperches, at some nodes exceeding rates reported for well-studied adaptive radiations such as Hawaiian silverswords. The geographic pattern of speciation in logperches was investigated by examining the relationship between degree of sympatry and the absolute age of the contrast, with the result that diversification in logperches appears allopatric. The very high diversification rate observed in the logperch phylogeny is more similar to freshwater fish clades thought to represent examples of sympatric speciation than to clades representing allopatric speciation. These results demonstrate that the geographic mode of speciation for a clade cannot be inferred from the diversification rate. The empirical observation of high diversification rates in logperches demonstrates that allopatric speciation can occur rapidly.     

EXPLOSIVE EVOLUTIONARY RADIATIONS: DECREASING SPECIATION OR INCREASING EXTINCTION THROUGH TIME?

A common pattern in time-calibrated molecular phylogenies is a signal of rapid diversification early in the history of a radiation. Because the net rate of diversification is the difference between speciation and extinction rates, such "explosive-early" diversification could result either from temporally declining speciation rates or from increasing extinction rates through time. Distinguishing between these alternatives is challenging but important, because these processes likely result from different ecological drivers of diversification. Here we develop a method for estimating speciation and extinction rates that vary continuously through time. By applying this approach to real phylogenies with explosive-early diversification and by modeling features of lineage-accumulation curves under both declining speciation and increasing extinction scenarios, we show that a signal of explosive-early diversification in phylogenies of extant taxa cannot result from increasing extinction and can only be explained by temporally declining speciation rates. Moreover, whenever extinction rates are high, "explosive early" patterns become unobservable, because high extinction quickly erases the signature of even large declines in speciation rates. Although extinction may obscure patterns of evolutionary diversification, these results show that decreasing speciation is often distinguishable from increasing extinction in the numerous molecular phylogenies of radiations that retain a preponderance of early lineages.     

Niche evolution and diversification in a Neotropical radiation of birds (Aves: Furnariidae)

Rapid diversification may be caused by ecological adaptive radiation via niche divergence. In this model, speciation is coupled with niche divergence and lineage diversification is predicted to be correlated with rates of niche evolution. Studies of the role of niche evolution in diversification have generally focused on ecomorphological diversification but climatic‐niche evolution may also be important. We tested these alternatives using a phylogeny of 298 species of ovenbirds (Aves: Furnariidae). We found that within Furnariidae, variation in species richness and diversification rates of subclades were best predicted by rate of climatic‐niche evolution than ecomorphological evolution. Although both are clearly important, univariate regression and multivariate model averaging more consistently supported the climatic‐niche as the best predictor of lineage diversification. Our study adds to the growing body of evidence, suggesting that climatic‐niche divergence may be an important driver of rapid diversification in addition to ecomorphological evolution. However, this pattern may depend on the phylogenetic scale at which rate heterogeneity is examined.     

Dispersal has inhibited avian diversification in Australasian archipelagoes

Different models of speciation predict contrasting patterns in the relationship between the dispersal ability of lineages and their diversification rates. This relationship is expected to be negative in isolation-limited models and positive in founder-event models. In addition, the combination of negative and positive effects of dispersal on speciation can result in higher diversification rates at intermediate levels of dispersal ability. Using molecular phylogenies to estimate diversification rates, and wing morphology to estimate dispersal ability, we analysed the influence of dispersal on diversification in the avifauna of Australasian archipelagoes. Contrary to expectations given the fragmented nature of island systems, the relationship between dispersal ability and diversification rate was monotonically negative. While multiple mechanisms could generate this pattern, they all share a phase of range expansion that is decoupled from speciation.     

Primate diversification inferred from phylogenies and fossils

Biodiversity arises from the balance between speciation and extinction. Fossils record the origins and disappearance of organisms, and the branching patterns of molecular phylogenies allow estimation of speciation and extinction rates, but the patterns of diversification are frequently incongruent between these two data sources. I tested two hypotheses about the diversification of primates based on ～600 fossil species and 90% complete phylogenies of living species: (1) diversification rates increased through time; (2) a significant extinction event occurred in the Oligocene. Consistent with the first hypothesis, analyses of phylogenies supported increasing speciation rates and negligible extinction rates. In contrast, fossils showed that while speciation rates increased, speciation and extinction rates tended to be nearly equal, resulting in zero net diversification. Partially supporting the second hypothesis, the fossil data recorded a clear pattern of diversity decline in the Oligocene, although diversification rates were near zero. The phylogeny supported increased extinction ～34 Ma, but also elevated extinction ～10 Ma, coinciding with diversity declines in some fossil clades. The results demonstrated that estimates of speciation and extinction ignoring fossils are insufficient to infer diversification and information on extinct lineages should be incorporated into phylogenetic analyses.     

Karyotypic Changes through Dysploidy Persist Longer over Evolutionary Time than Polyploid Changes

Chromosome evolution has been demonstrated to have profound effects on diversification rates and speciation in angiosperms. While polyploidy has predated some major radiations in plants, it has also been related to decreased diversification rates. There has been comparatively little attention to the evolutionary role of gains and losses of single chromosomes, which may or not entail changes in the DNA content (then called aneuploidy or dysploidy, respectively). In this study we investigate the role of chromosome number transitions and of possible associated genome size changes in angiosperm evolution. We model the tempo and mode of chromosome number evolution and its possible correlation with patterns of cladogenesis in 15 angiosperm clades. Inferred polyploid transitions are distributed more frequently towards recent times than single chromosome gains and losses. This is likely because the latter events do not entail changes in DNA content and are probably due to fission or fusion events (dysploidy), as revealed by an analysis of the relationship between genome size and chromosome number. Our results support the general pattern that recently originated polyploids fail to persist, and suggest that dysploidy may have comparatively longer-term persistence than polyploidy. Changes in chromosome number associated with dysploidy were typically observed across the phylogenies based on a chi-square analysis, consistent with these changes being neutral with respect to diversification.     

Mollusk species diversity in the Southeastern Pacific: why are there more species towards the pole?

The most ubiquitous and well recognized diversity pattern at large spatial scales is the latitudinal increase in species richness near the equator and decline towards the poles. Although several exceptions to this pattern have been documented, shallow water mollusks, the most specious group of marine invertebrates, are the epitome of the monotonic decline in species diversity toward higher latitudes along the Pacific and Atlantic coasts of North America. Here we analyze the geographic diversity of 629 mollusk species along the Pacific South American shelf. Our analyses are based on the most complete database of invertebrates assembled for this region of the world, consisting of latitudinal ranges of over 95% of all described mollusks between 10° and 55°S. Along this coast, mollusk diversity did not follow the typical latitudinal trend. The number of species remained constant and relatively low at intermediate latitudes and sharply increased toward higher latitudes, south of 42°S. This trend was explained by changes in shelf area, but not by sea surface temperature, unlike the pattern documented for Northern Hemisphere mollusks. Direct sampling of soft bottom communities along the gradient suggests that regional trends in species richness are produced by increased alpha diversity, and not only by artifacts produced by the increase in sampling area. We hypothesize that increased shelf area south of 42°S, geographic isolation produced by divergence of major oceanic currents, and the existence of refugia during glaciations, enabled species diversification. Radiation could have been limited by narrow continental shelves between 10°–42°. Asymmetries in latitudinal diversity trends between hemispheres show that there is not a single general factor determining large-scale diversity patterns.     

Diversification and biogeographic patterns in four island radiations of passerine birds

Declining diversification rates over time are a well-established evolutionary pattern, often interpreted as indicating initial rapid radiation with filling of ecological niche space. Here, we test the hypothesis that island radiations may show constant net diversification rates over time, due to continued expansion into new niche space in highly dispersive taxa. We investigate diversification patterns of four passerine bird families originating from the Indo-Pacific archipelagos, and link these to biogeographic patterns to provide independent indications of niche filling. We find a declining diversification rate for only one family, the Paradisaeidae (41 species). These are almost completely restricted to New Guinea, and have on average smaller species ranges and higher levels of species richness within grid cells than the other three families. In contrast, we cannot reject constant diversification rates for Campephagidae (93 species), Oriolidae (35 species), and Pachycephalidae (53 species), groups that have independently colonized neighboring archipelagos and continents. We propose that Paradisaeidae have reached the diversity limit imposed by their restricted distribution, whereas high dispersal and colonization success across the geologically dynamic Indo-Pacific archipelagos may have sustained high speciation rates for the other three families. Alternatively, increasing extinction rates may have obscured declining speciation rates in those three phylogenies.     

Density-dependent diversification in North American wood warblers

Evidence from both molecular phylogenies and the fossil record suggests that rates of species diversification often decline through time during evolutionary radiations. One proposed explanation for this pattern is ecological opportunity, whereby an initial abundance of resources and lack of potential competitors facilitate rapid diversification. This model predicts density-dependent declines in diversification rates, but has not been formally tested in any species-level radiation. Here we develop a new conceptual framework that distinguishes density dependence from alternative processes that also produce temporally declining diversification, and we demonstrate this approach using a new phylogeny of North American Dendroica wood warblers. We show that explosive lineage accumulation early in the history of this avian radiation is best explained by a density-dependent diversification process. Our results suggest that the tempo of wood warbler diversification was mediated by ecological interactions among species and that lineage and ecological diversification in this group are coupled, as predicted under the ecological opportunity model.     

Ancient tropical extinctions at high latitudes contributed to the latitudinal diversity gradient*

Global biodiversity currently peaks at the equator and decreases toward the poles. Growing fossil evidence suggest this hump-shaped latitudinal diversity gradient (LDG) has not been persistent through time, with similar diversity across latitudes flattening out the LDG during past greenhouse periods. However, when and how diversity declined at high latitudes to generate the modern LDG remains an open question. Although diversity-loss scenarios have been proposed, they remain mostly undemonstrated. We outline the “asymmetric gradient of extinction and dispersal” framework that contextualizes previous ideas behind the LDG under a time-variable scenario. Using phylogenies and fossils of Testudines, Crocodilia, and Lepidosauria, we find that the hump-shaped LDG could be explained by (1) disproportionate extinctions of high-latitude tropical-adapted clades when climate transitioned from greenhouse to icehouse, and (2) equator-ward biotic dispersals tracking their climatic preferences when tropical biomes became restricted to the equator. Conversely, equivalent diversification rates across latitudes can account for the formation of an ancient flat LDG. The inclusion of fossils in macroevolutionary studies allows revealing time-dependent extinction rates hardly detectable from phylogenies only. This study underscores that the prevailing evolutionary processes generating the LDG during greenhouses differed from those operating during icehouses.     

A comparative study of mammalian diversification pattern

Although mammals have long been regarded as a successful radiation, the diversification pattern among the clades is still poorly known. Higher-level phylogenies are conflicting and comprehensive comparative analyses are still lacking. Using a recently published supermatrix encompassing nearly all extant mammalian families and a novel comparative likelihood approach (MEDUSA), the diversification pattern of mammalian groups was examined. Both order- and family-level phylogenetic analyses revealed the rapid radiation of Boreoeutheria and Euaustralidelphia in the early mammalian history. The observation of a diversification burst within Boreoeutheria at approximately 100 My supports the Long Fuse model in elucidating placental diversification progress, and the rapid radiation of Euaustralidelphia suggests an important role of biogeographic dispersal events in triggering early Australian marsupial rapid radiation. Diversification analyses based on family-level diversity tree revealed seven additional clades with exceptional diversification rate shifts, six of which represent accelerations in net diversification rate as compared to the background pattern. The shifts gave origin to the clades Muridae+Cricetidae, Bovidae+Moschidae+Cervidae, Simiiformes, Echimyidae, Odontoceti (excluding Physeteridae+Kogiidae+Platanistidae), Macropodidae, and Vespertilionidae. Moderate to high extinction rates from background and boreoeutherian diversification patterns indicate the important role of turnovers in shaping the heterogeneous taxonomic richness observed among extant mammalian groups. Furthermore, the present results emphasize the key role of extinction on erasing unusual diversification signals, and suggest that further studies are needed to clarify the historical radiation of some mammalian groups for which MEDUSA did not detect exceptional diversification rates.