Diversity Dynamics in Nymphalidae Butterflies: Effect of Phylogenetic Uncertainty on Diversification Rate Shift Estimates

The species rich butterfly family Nymphalidae has been used to study evolutionary interactions between plants and insects. Theories of insect-hostplant dynamics predict accelerated diversification due to key innovations. In evolutionary biology, analysis of maximum credibility trees in the software MEDUSA (modelling evolutionary diversity using stepwise AIC) is a popular method for estimation of shifts in diversification rates. We investigated whether phylogenetic uncertainty can produce different results by extending the method across a random sample of trees from the posterior distribution of a Bayesian run. Using the MultiMEDUSA approach, we found that phylogenetic uncertainty greatly affects diversification rate estimates. Different trees produced diversification rates ranging from high values to almost zero for the same clade, and both significant rate increase and decrease in some clades. Only four out of 18 significant shifts found on the maximum clade credibility tree were consistent across most of the sampled trees. Among these, we found accelerated diversification for Ithomiini butterflies. We used the binary speciation and extinction model (BiSSE) and found that a hostplant shift to Solanaceae is correlated with increased net diversification rates in Ithomiini, congruent with the diffuse cospeciation hypothesis. Our results show that taking phylogenetic uncertainty into account when estimating net diversification rate shifts is of great importance, as very different results can be obtained when using the maximum clade credibility tree and other trees from the posterior distribution.     

Different Diversification Rates Between Sexual and Asexual Organisms

Patterns of diversity reflect the balance between speciation and extinction over time. Here we estimate net diversification rates for samples of sexual and asexual rotifers using phylogenetic reconstructions from sequence data of one mtDNA locus, cytochrome oxidase c subunit I. All four clades of bdelloid rotifers, obligate asexuals, had higher number of species per clade and significantly higher accumulation of diversification events towards the root of the trees than the four clades of their sexual relatives, the monogonont rotifers. Such differences were robust to confounding effects of number of analysed sequences, haplotype diversity, overall genetic divergence, age of the clades or geographic coverage. Our results support the idea that differences in diversification rates could thus be ascribed to different mechanisms of speciation, with ecological speciation as the most plausible mechanism for asexual organisms.     

Estimating diversification rates from phylogenetic information

Patterns of species richness reflect the balance between speciation and extinction over the evolutionary history of life. These processes are influenced by the size and geographical complexity of regions, conditions of the environment, and attributes of individuals and species. Diversity within clades also depends on age and thus the time available for accumulating species. Estimating rates of diversification is key to understanding how these factors have shaped patterns of species richness. Several approaches to calculating both relative and absolute rates of speciation and extinction within clades are based on phylogenetic reconstructions of evolutionary relationships. As the size and quality of phylogenies increases, these approaches will find broader application. However, phylogeny reconstruction fosters a perceptual bias of continual increase in species richness, and the analysis of primarily large clades produces a data selection bias. Recognizing these biases will encourage the development of more realistic models of diversification and the regulation of species richness.     

ABSOLUTE DIVERSIFICATION RATES IN ANGIOSPERM CLADES

Abstract The extraordinary contemporary species richness and ecological predominance of flowering plants (angiosperms) are even more remarkable when considering the relatively recent onset of their evolutionary diversification. We examine the evolutionary diversification of angiosperms and the observed differential distribution of species in angiosperm clades by estimating the rate of diversification for angiosperms as a whole and for a large set of angiosperm clades. We also identify angiosperm clades with a standing diversity that is either much higher or lower than expected, given the estimated background diversification rate. Recognition of angiosperm clades, the phylogenetic relationships among them, and their taxonomic composition are based on an empirical compilation of primary phylogenetic studies. By making an integrative and critical use of the paleobotanical record, we obtain reasonably secure approximations for the age of a large set of angiosperm clades. Diversification was modeled as a stochastic, time‐homogeneous birth‐and‐death process that depends on the diversification rate (r) and the relative extinction rate (∈). A statistical analysis of the birth and death process was then used to obtain 95% confidence intervals for the expected number of species through time in a clade that diversifies at a rate equal to that of angiosperms as a whole. Confidence intervals were obtained for stem group and for crown group ages in the absence of extinction (∈= 0.0) and under a high relative extinction rate (∈= 0.9). The standing diversity of angiosperm clades was then compared to expected species diversity according to the background rate of diversification, and, depending on their placement with respect to the calculated confidence intervals, exceedingly species‐rich or exceedingly species‐poor clades were identified. The rate of diversification for angiosperms as a whole ranges from 0.077 (∈= 0.9) to 0.089 (∈= 0.0) net speciation events per million years. Ten clades fall above the confidence intervals of expected species diversity, and 13 clades were found to be unexpectedly species poor. The phylogenetic distribution of clades with an exceedingly high number of species suggests that traits that confer high rates of diversification evolved independently in different instances and do not characterize the angiosperms as a whole.     

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.     

Estimating diversification rates for higher taxa: BAMM can give problematic estimates of rates and rate shifts

Estimates of diversification rates are invaluable for many macroevolutionary studies. Recently, an approach called BAMM (Bayesian Analysis of Macro‐evolutionary Mixtures) has become widely used for estimating diversification rates and rate shifts. At the same time, several articles have concluded that estimates of net diversification rates from the method‐of‐moments (MS) estimators are inaccurate. Yet, no studies have compared the ability of these two methods to accurately estimate clade diversification rates. Here, we use simulations to compare their performance. We found that BAMM yielded relatively weak relationships between true and estimated diversification rates. This occurred because BAMM underestimated the number of rates shifts across each tree, and assigned high rates to small clades with low rates. Errors in both speciation and extinction rates contributed to these errors, showing that using BAMM to estimate only speciation rates is also problematic. In contrast, the MS estimators (particularly using stem group ages), yielded stronger relationships between true and estimated diversification rates, by roughly twofold. Furthermore, the MS approach remained relatively accurate when diversification rates were heterogeneous within clades, despite the widespread assumption that it requires constant rates within clades. Overall, we caution that BAMM may be problematic for estimating diversification rates and rate shifts.     

The shape and temporal dynamics of phylogenetic trees arising from geographic speciation

Phylogenetic trees often depart from the expectations of stochastic models, exhibiting imbalance in diversification among lineages and slowdowns in the rate of lineage accumulation through time. Such departures have led to a widespread perception that ecological differences among species or adaptation and subsequent niche filling are required to explain patterns of diversification. However, a key element missing from models of diversification is the geographical context of speciation and extinction. In this study, we develop a spatially explicit model of geographic range evolution and cladogenesis, where speciation arises via vicariance or peripatry, and explore the effects of these processes on patterns of diversification. We compare the results with those observed in 41 reconstructed avian trees. Our model shows that nonconstant rates of speciation and extinction are emergent properties of the apportioning of geographic ranges that accompanies speciation. The dynamics of diversification exhibit wide variation, depending on the mode of speciation, tendency for range expansion, and rate of range evolution. By varying these parameters, the model is able to capture many, but not all, of the features exhibited by birth-death trees and extant bird clades. Under scenarios with relatively stable geographic ranges, strong slowdowns in diversification rates are produced, with faster rates of range dynamics leading to constant or accelerating rates of apparent diversification. A peripatric model of speciation with stable ranges also generates highly unbalanced trees typical of bird phylogenies but fails to produce realistic range size distributions among the extant species. Results most similar to those of a birth-death process are reached under a peripatric speciation scenario with highly volatile range dynamics. Taken together, our results demonstrate that considering the geographical context of speciation and extinction provides a more conservative null model of diversification and offers a very different perspective on the phylogenetic patterns expected in the absence of ecology.     

净多样化速率和进化时间对虎耳草目科间物种多样性差异的影响

不同生物类群包含的物种数目常存在巨大差异,这是生态学和生物学研究中普遍观察到的现象。然而,这一现象产生的原因仍然是未解之谜。从宏观进化的角度,进化时间假说和多样化速率假说是两个比较流行的假说。进化时间假说认为类群的演化时间越长,积累的物种丰富度越高; 而多样化速率假说认为类群的净多样化速率越快,则其物种丰富度越高。为验证这两个假说,该文以一棵包含1 539个物种化石定年的虎耳草目系统发育树为基础,通过宏观进化分析获取了虎耳草目内15个科的物种形成和灭绝速率,并计算了每个科的平均多样化速率。结果表明:(1)虎耳草目的物种多样化速率有着增加的趋势,并且多样化速率的增加主要出现在温带和高山类群,如茶藨子科、景天科和芍药科等。(2)采用系统发育广义最小二乘模型(PGLS)和线性回归模型(LM)结果表明,虎耳草目15个科的物种丰富度与科的分化时间和科内物种的最近共同祖先年龄都没有显著相关关系,而与净多样化速率显著正相关(R² =0.380,P<0.05)。该研究支持了多样化速率假说,认为不同科的净多样化速率的差异是导致虎耳草目科间物种数目差异的主要原因之一。全球气候变冷可能为虎耳草目中草本、落叶乔木和灌木等能够适应寒冷环境的类群提供了分布范围扩张和物种快速多样化的机会。该研究表明在温带和高山扩张类群中,物种净多样化速率可能是导致不同类群物种数目差异的主要原因。     

Congruent phylogenetic and fossil signatures of mammalian diversification dynamics driven by Tertiary abiotic change

Computational methods for estimating diversification rates from extant species phylogenetic trees have become abundant in evolutionary research. However, little evidence exists about how their outcome compares to a complementary and direct source of information: the fossil record. Furthermore, there is virtually no direct test for the congruence of evolutionary rates based on these two sources. This task is only achievable in clades with both a well‐known fossil record and a complete phylogenetic tree. Here, we compare the evolutionary rates of ruminant mammals as estimated from their vast paleontological record—over 1200 species spanning 50 myr—and their living‐species phylogeny. Significantly, our results revealed that the ruminant's fossil record and phylogeny reflect congruent evolutionary processes. The concordance is especially strong for the last 25 myr, when living groups became a dominant part of ruminant diversity. We found empirical support for previous hypotheses based on simulations and neontological data: The pattern captured by the tree depends on how clade specific the processes are and which clades are involved. Also, we report fossil evidence for a postradiation speciation slowdown coupled with constant, moderate extinction in the Miocene. The recent deceleration in phylogenetic rates is connected to rapid extinction triggered by recent climatic fluctuations.     

Angiosperm diversification through time

The extraordinary diversity of angiosperms is the ultimate outcome of the interplay of speciation and extinction, which determine the net diversification of different lineages. We document the temporal trends of angiosperm diversification rates during their early history. Absolute diversification rates were estimated for order-level clades using ages derived from relaxed molecular clock analyses that included or excluded a maximal constraint to angiosperm age. Diversification rates for angiosperms as a whole ranged from 0.0781 to 0.0909 net speciation events per million years, with dates from the constrained analysis. Diversification through time plots show an inverse relationship between clade age and rate, where the younger clades tend to have the highest rates. Angiosperm diversity is found to have mixed origins: slightly less than half of the living species belong to lineages with low to moderate diversification rates, which appeared between 130 and 102 Mya (Barremian-uppermost Albian; Lower Cretaceous). Slightly over half of the living species belong to lineages with moderate to high diversification rates, which appeared between 102 and 77 Mya (Cenomanian-mid Campanian; Upper Cretaceous). Terminal lineages leading to living angiosperm species, however, may have originated soon or long after the phylogenetic differentiation of the clade to which they belong.     

Signatures of random and selective mass extinctions in phylogenetic tree balance

Current models of diversification with evolving speciation rates have trouble mimicking the extreme imbalance seen in estimated phylogenies. However, these models have not incorporated extinction. Here, we report on a simple simulation model that includes heritable and evolving speciation rates coupled with mass extinctions, Random (but not selective) mass extinctions, coupled with evolving among-lineage variation in speciation rates, increase imbalance of postrecovery clades. Thus, random mass extinctions are plausible contributors to the imbalance of modern clades. Paleontological evidence suggests that mass extinctions are often random with respect to ecological and morphological traits, consistent with our simulations. In contrast, evidence that the current anthropogenic mass extinction is phylogenetically selective suggests that the current extinction episode may be qualitatively different from past ones in the way it reshapes future biotas.     

A major shift in diversification rate helps explain macroevolutionary patterns in primate species diversity

Primates represent one of the most species rich, wide ranging, and ecologically diverse clades of mammals. What major macroevolutionary factors have driven their diversification and contributed to the modern distribution of primate species remains widely debated. We employed phylogenetic comparative methods to examine the role of clade age and evolutionary rate heterogeneity in the modern distribution of species diversity of Primates. Primate diversification has accelerated since its origin, with decreased extinction leading to a shift to even higher evolutionary rates in the most species rich family (Cercopithecidae). Older primate clades tended to be more diverse, however a shift in evolutionary rate was necessary to adequately explain the imbalance in species diversity. Species richness was also poorly explained by geographic distribution, especially once clade age and evolutionary rate shifts were accounted for, and may relate instead to other ecological factors. The global distribution of primate species diversity appears to have been strongly impacted by heterogeneity in evolutionary rates.     

Quantitative traits and diversification

Quantitative traits have long been hypothesized to affect speciation and extinction rates. For example, smaller body size or increased specialization may be associated with increased rates of diversification. Here, I present a phylogenetic likelihood-based method (quantitative state speciation and extinction [QuaSSE]) that can be used to test such hypotheses using extant character distributions. This approach assumes that diversification follows a birth-death process where speciation and extinction rates may vary with one or more traits that evolve under a diffusion model. Speciation and extinction rates may be arbitrary functions of the character state, allowing much flexibility in testing models of trait-dependent diversification. I test the approach using simulated phylogenies and show that a known relationship between speciation and a quantitative character could be recovered in up to 80% of the cases on large trees (500 species). Consistent with other approaches, detecting shifts in diversification due to differences in extinction rates was harder than when due to differences in speciation rates. Finally, I demonstrate the application of QuaSSE to investigate the correlation between body size and diversification in primates, concluding that clade-specific differences in diversification may be more important than size-dependent diversification in shaping the patterns of diversity within this group.     

Causes of plant diversification in the Cape biodiversity hotspot of South Africa

The Cape region of South Africa is one of the most remarkable hotspots of biodiversity with a flora comprising more than 9000 plant species, almost 70% of which are endemic, within an area of only ± 90,000 km2. Much of the diversity is due to an exceptionally large contribution of just a few clades that radiated substantially within this region, but little is known about the causes of these radiations. Here, we present a comprehensive analysis of plant diversification, using near complete species-level phylogenies of four major Cape clades (more than 470 species): the genus Protea, a tribe of legumes (Podalyrieae) and two speciose genera within the iris family (Babiana and Moraea), representing three of the seven largest plant families in this biodiversity hotspot. Combining these molecular phylogenetic data with ecological and biogeographical information, we tested key hypotheses that have been proposed to explain the radiation of the Cape flora. Our results show that the radiations started throughout the Oligocene and Miocene and that net diversification rates have remained constant through time at globally moderate rates. Furthermore, using sister-species comparisons to assess the impact of different factors on speciation, we identified soil type shifts as the most important cause of speciation in Babiana, Moraea, and Protea, whereas shifts in fire-survival strategy is the most important factor for Podalyrieae. Contrary to previous findings in other groups, such as orchids, pollination syndromes show a high degree of phylogenetic conservatism, including groups with a large number of specialized pollination syndromes like Moraea. We conclude that the combination of complex environmental conditions together with relative climatic stability promoted high speciation and/or low extinction rates as the most likely scenario leading to present-day patterns of hyperdiversity in the Cape.     

A phylogenetic perspective on habitat shifts and diversity in the North American Enallagma damselflies

Community ecologists are increasingly aware that the regional history of taxon diversification can have an important influence on community structure. Likewise, systematists recognize that ecological context can have an important influence on the processes of speciation and extinction that create patterns of descent. We present a phylogenetic analysis of 33 species of a North American radiation of damselflies (Zygoptera: Coenagrionidae: Enallagma Selys), which have been well studied ecologically, to elucidate the evolutionary mechanisms that have contributed to differences in diversity between larval habitats (lakes with and without fish predators). Analysis of molecular variation in 842 bp of the mitochondrial cytochrome oxidase I and II subunit and of the intervening Leu-tRNA and 37 morphological characters resulted in three well-defined clades that are only partially congruent with previous phylogenetic hypotheses. Molecular and morphological data partitions were significantly incongruent (p < .01). Lack of haplotype monophyly within species and small amounts of sequence divergence (< 1%) between related species in three of the four clades suggest that recent, and parallel, speciation has been an important source of community diversity. Reconstruction of habitat preference over the phylogeny suggests that the greater species diversity in fish-containing lake habitats reflects the recency of shifts into the fishless lake habit, although a difference in speciation or extinction rates between the two habitats is difficult to exclude as an additional mechanism.     

Phylogenetically patterned speciation rates and extinction risks change the loss of evolutionary history during extinctions

If we are to plan conservation strategies that minimize the loss of evolutionary history through human-caused extinctions, we must understand how this loss is related to phylogenetic patterns in current extinction risks and past speciation rates. Nee & May (1997, Science 278, 692-694) showed that for a randomly evolving clade (i) a single round of random extinction removed relatively little evolutionary history, and (ii) extinction management (choosing which taxa to sacrifice) offered only marginal improvement. However, both speciation rates and extinction risks vary across lineages within real clades. We simulated evolutionary trees with phylogenetically patterned speciation rates and extinction risks (closely related lineages having similar rates and risks) and then subjected them to several biologically informed models of extinction. Increasing speciation rate variation increases the extinction-management pay-off. When extinction risks vary among lineages but are uncorrelated with speciation rates, extinction removes more history (compared with random trees), but the difference is small. When extinction risks vary and are correlated with speciation rates, history loss can dramatically increase (negative correlation) or decrease (positive correlation) with speciation rate variation. The loss of evolutionary history via human-caused extinctions may therefore be more severe, yet more manageable, than first suggested.     

DISENTANGLING THE EFFECTS OF KEY INNOVATIONS ON THE DIVERSIFICATION OF BROMELIOIDEAE (BROMELIACEAE)

The evolution of key innovations, novel traits that promote diversification, is often seen as major driver for the unequal distribution of species richness within the tree of life. In this study, we aim to determine the factors underlying the extraordinary radiation of the subfamily Bromelioideae, one of the most diverse clades among the neotropical plant family Bromeliaceae. Based on an extended molecular phylogenetic data set, we examine the effect of two putative key innovations, that is, the Crassulacean acid metabolism (CAM) and the water‐impounding tank, on speciation and extinction rates. To this aim, we develop a novel Bayesian implementation of the phylogenetic comparative method, binary state speciation and extinction, which enables hypotheses testing by Bayes factors and accommodates the uncertainty on model selection by Bayesian model averaging. Both CAM and tank habit were found to correlate with increased net diversification, thus fulfilling the criteria for key innovations. Our analyses further revealed that CAM photosynthesis is correlated with a twofold increase in speciation rate, whereas the evolution of the tank had primarily an effect on extinction rates that were found five times lower in tank‐forming lineages compared to tank‐less clades. These differences are discussed in the light of biogeography, ecology, and past climate change.     

EXTINCTION RATES SHOULD NOT BE ESTIMATED FROM MOLECULAR PHYLOGENIES

Molecular phylogenies contain information about the tempo and mode of species diversification through time. Because extinction leaves a characteristic signature in the shape of molecular phylogenetic trees, many studies have used data from extant taxa only to infer extinction rates. This is a promising approach for the large number of taxa for which extinction rates cannot be estimated from the fossil record. Here, I explore the consequences of violating a common assumption made by studies of extinction from phylogenetic data. I show that when diversification rates vary among lineages, simple estimators based on the birth–death process are unable to recover true extinction rates. This is problematic for phylogenetic trees with complete taxon sampling as well as for the simpler case of clades with known age and species richness. Given the ubiquity of variation in diversification rates among lineages and clades, these results suggest that extinction rates should not be estimated in the absence of fossil data.     

Bats, clocks, and rocks: diversification patterns in Chiroptera

Identifying nonrandom clade diversification is a critical first step toward understanding the evolutionary processes underlying any radiation and how best to preserve future phylogenetic diversity. However, differences in diversification rates have not been quantitatively assessed for the majority of groups because of the lack of necessary analytical tools (e.g., complete species-level phylogenies, estimates of divergence times, and robust statistics which incorporate phylogenetic uncertainty and test appropriate null models of clade growth). Here, for the first time, we investigate diversification rate heterogeneity in one of the largest groups studied thus far, the bats (Mammalia: Chiroptera). We use a recent, robust statistical approach (whole-tree likelihood-based relative rate tests) on complete dated species-level supertree phylogenies. As has been demonstrated previously for most other groups, among-lineage diversification rate within bats has not been constant. However, we show that bat diversification is more heterogeneous than in other mammalian clades thus far studied. The whole-tree likelihood-based relative rates tests suggest that clades within the families Phyllostomidae and Molossidae underwent a number of significant changes in relative diversification rate. There is also some evidence for rate shifts within Pteropodidae, Emballonuridae, Rhinolophidae, Hipposideridae, and Vespertilionidae, but the significance of these shifts depends on polytomy resolution within each family. Diversification rate in bats has also not been constant, with the largest diversification rate shifts occurring 30-50 million years ago, a time overlapping with the greatest number of shifts in flowering plant diversification rates.     

Larger brains spur species diversification in birds

Evidence is accumulating that species traits can spur their evolutionary diversification by influencing niche shifts, range expansions, and extinction risk. Previous work has shown that larger brains (relative to body size) facilitate niche shifts and range expansions by enhancing behavioral plasticity but whether larger brains also promote evolutionary diversification is currently backed by insufficient evidence. We addressed this gap by combining a brain size dataset for >1900 avian species worldwide with estimates of diversification rates based on two conceptually different phylogenetic‐based approaches. We found consistent evidence that lineages with larger brains (relative to body size) have diversified faster than lineages with relatively smaller brains. The best supported trait‐dependent model suggests that brain size primarily affects diversification rates by increasing speciation rather than decreasing extinction rates. In addition, we found that the effect of relatively brain size on species‐level diversification rate is additive to the effect of other intrinsic and extrinsic factors. Altogether, our results highlight the importance of brain size as an important factor in evolution and reinforce the view that intrinsic features of species have the potential to influence the pace of evolution.