Metabolically similar cohorts of bacteria exhibit strong cooccurrence patterns with diet items and eukaryotic microbes in lizard guts

Gut microbiomes perform essential services for their hosts, including helping them to digest food and manage pathogens and parasites. Performing these services requires a diverse and constantly changing set of metabolic functions from the bacteria in the microbiome. The metabolic repertoire of the microbiome is ultimately dependent on the outcomes of the ecological interactions of its member microbes, as these interactions in part determine the taxonomic composition of the microbiome. The ecological processes that underpin the microbiome's ability to handle a variety of metabolic challenges might involve rapid turnover of the gut microbiome in response to new metabolic challenges, or it might entail maintaining sufficient diversity in the microbiome that any new metabolic demands can be met from an existing set of bacteria. To differentiate between these scenarios, we examine the gut bacteria and resident eukaryotes of two generalist‐insectivore lizards, while simultaneously identifying the arthropod prey each lizard was digesting at the time of sampling. We find that the cohorts of bacteria that occur significantly more or less often than expected with arthropod diet items or eukaryotes include bacterial species that are highly similar to each other metabolically. This pattern in the bacterial microbiome could represent an early step in the taxonomic shifts in bacterial microbiome that occur when host lineages change their diet niche over evolutionary timescales.     

Saikosaponin-d,a novel SERCA inhibitor,induces autophagic cell death in apoptosis-defective cells

Autophagy is an important cellular process that controls cells in a normal homeostatic state by recycling nutrients to maintain cellular energy levels for cell survival via the turnover of proteins and damaged organelles. However, persistent activation of autophagy can lead to excessive depletion of cellular organelles and essential proteins, leading to caspase-independent autophagic cell death. As such, inducing cell death through this autophagic mechanism could be an alternative approach to the treatment of cancers. Recently, we have identified a novel autophagic inducer, saikosaponin-d (Ssd), from a medicinal plant that induces autophagy in various types of cancer cells through the formation of autophagosomes as measured by GFP-LC3 puncta formation. By computational virtual docking analysis, biochemical assays and advanced live-cell imaging techniques, Ssd was shown to increase cytosolic calcium level via direct inhibition of sarcoplasmic/endoplasmic reticulum Ca²⁺ ATPase pump, leading to autophagy induction through the activation of the Ca²⁺/calmodulin-dependent kinase kinase–AMP-activated protein kinase–mammalian target of rapamycin pathway. In addition, Ssd treatment causes the disruption of calcium homeostasis, which induces endoplasmic reticulum stress as well as the unfolded protein responses pathway. Ssd also proved to be a potent cytotoxic agent in apoptosis-defective or apoptosis-resistant mouse embryonic fibroblast cells, which either lack caspases 3, 7 or 8 or had the Bax-Bak double knockout. These results provide a detailed understanding of the mechanism of action of Ssd, as a novel autophagic inducer, which has the potential of being developed into an anti-cancer agent for targeting apoptosis-resistant cancer cells.     

Primary controls on species richness in higher taxa

The disparity in species richness across the tree of life is one of the most striking and pervasive features of biological diversity. Some groups are exceptionally diverse, whereas many other groups are species poor. Differences in diversity among groups are frequently assumed to result from primary control by differential rates of net diversification. However, a major alternative explanation is that ecological and other factors exert primary control on clade diversity, such that apparent variation in net diversification rates is a secondary consequence of ecological limits on clade growth. Here, I consider a likelihood framework for distinguishing between these competing hypotheses. I incorporate hierarchical modeling to explicitly relax assumptions about the constancy of diversification rates across clades, and I propose several statistics for a posteriori evaluation of model adequacy. I apply the framework to a recent dated phylogeny of ants. My results reject the hypothesis that net diversification rates exert primary control on species richness in this group and demonstrate that clade diversity is better explained by total time-integrated speciation. These results further suggest that it may not possible to estimate meaningful speciation and extinction rates from higher-level phylogenies of extant taxa only.     

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.     

Macroevolutionary thermodynamics: Temperature and the tempo of evolution in the tropics

An influential hypothesis proposes that the tempo of evolution is faster in the tropics. Emerging evidence, including a study in this issue of PLOS Biology, challenges this view, raising new questions about the causes of Earth’s iconic latitudinal diversity gradient (LDG).

Biologists have long puzzled over the spectacular diversity of animals and plants from Earth’s tropical regions. It is true that some tropical environments are not especially rich in species, and some groups of organisms show contrarian patterns with diversity peaks that occur far outside of the warm, humid tropics. Nonetheless, the big picture is clear: A vastly disproportionate fraction of Earth’s terrestrial biodiversity is concentrated in tropical rainforests, and warm water reef environments similarly account for a large fraction of marine diversity. The extremes of tropical diversity transcend the ability of most humans to process it: Some Amazonian rainforests, for example, contain more species of trees in just a few hectares than are found in the entirety of Europe or North America [1]. In general, the most diverse tropical rainforests support order-of-magnitude increases in species richness relative to otherwise comparable temperate zone communities across a wide range of organisms. Despite decades of study, however, the causes of this latitudinal diversity gradient (LDG) remain elusive.One of the most prominent hypotheses for the LDG is, loosely speaking, the idea that biological processes speed up in the tropics, potentially due to the kinetic effects of temperature on the rates of organismal processes. It seems obvious that the pulse of life should be faster under a torrid tropical sun, and—to naturalists who’ve spent time in lowland rainforests in particular—such a view accords well with perceptions of the humid tropics as a raging, steamy mess of species interactions that collectively generate the tangled web that is tropical diversity. It is generally accepted that temperature can affect metabolic rate and many other biological processes, including those involving ecological interactions between species (e.g., competition, predation, and herbivory). The specific mechanisms connecting thermal energy to biodiversity remain unclear. For example, they might involve the influence of temperature on rates of molecular evolution, which might then influence rates of speciation [2]. Or, species in warmer environments might live closer to their optimal body temperatures, thus enabling them to allocate more resources to performance-associated functions and leading to a systematic upgrading in the intensity of antagonistic or coevolutionary interactions between species [3]. Regardless of the specific mechanism, the general idea is captured by Brown [4], who notes that “‘Diversity begets diversity’ in the tropics, because ‘the Red Queen runs faster when she is hot.’”Writing in PLOS Biology, Drury and colleagues [5] demonstrate that a central prediction of these “faster tropics” hypotheses fails to hold up. They predicted that, if certain types of ecological interactions between species are stronger in the tropics, then we should see a signal of those interactions in long-term patterns of trait evolution. In particular, the increased pressure to respond to species interactions in the tropics should result in faster overall rates of morphological evolution for tropical species. To test this hypothesis, the authors studied the rate of morphological evolution in birds, analyzing a large dataset on bill shape and body proportions from other recent studies [6] with a battery of sophisticated statistical models. These models allowed the rate of morphological change to differ systematically with latitude. Intriguingly, the models that best fit the data in some cases were those that allowed for strong interactions between species in driving patterns of divergence among closely related species that occupied that same biogeographic region (e.g., the neotropics). Thus, there is a partial signal of species interactions on the morphologies of species we see living together today, including those from both tropical and temperate regions. As suggested by the authors, these patterns might reflect a form of ecological character displacement, whereby morphologically similar species evolve differences that minimize their ecological overlap. But, surprisingly, the intensity of these effects shows no consistent relationship with latitude. The take-home message is that—at least for birds and the traits considered—species are not evolving more rapidly in the tropics.Drury and colleagues note that their results contradict recent articles that have documented differences in phenotypic evolutionary rates across latitude, although the studies referenced generally looked at different types of traits (e.g., birdsong). They suggest several potential reasons for the discrepancies between their results and those prior studies. But, critically, these earlier studies generally did not report faster evolution in the tropics, but faster evolution in the temperate zone. Hence, the results of Drury and colleagues and the earlier studies all converge to a similar and more general finding, which is that the warm tropics really aren’t so hot for macroevolution, at least as far as phenotypic evolutionary rates are concerned. By rejecting the simple explanations (faster evolution), new questions emerge about how and why tropical bird communities show such dramatic phenotypic and ecological diversity.Morphological evolution is not the only process that fails to show the expected pattern of “heating up” in the tropics. A number of recent studies have found that rates of species formation are either unrelated to latitude or slower in the tropics [7–9]. These results argue strongly against temperature kinetic models of biodiversity, whereby faster speciation emerges from the effects of warmer temperatures in the tropics on mutation and metabolic rates [10]. Many of the same causal pathways that predict increased rates of speciation as a function of temperature would also apply to rates of morphological evolution: Increased mutation rates in the tropics, for example, should accelerate the tempo of phenotypic evolution due to increased mutational variance in traits. But, regardless of whether we consider phenotypic evolution (as in Drury and colleagues) or lineage diversification, there is simply no evidence for faster evolutionary rates in the tropics.The results from Drury and colleagues [5] and other studies do not reject all possible causal pathways by which temperature or species interactions might facilitate high tropical diversity. Many phylogeny-based studies of species diversification and phenotypic evolution frame their interpretations through the lens of interspecific competition, ecological opportunity, and character displacement. Yet, numerous other types of interactions are relevant to global biodiversity patterns, and some of these interactions have scarcely been explored from a macroevolutionary perspective. Many such interactions have the potential to influence species richness and ecological diversity, perhaps through mechanisms that involve an indirect effect of temperature on equilibrium diversity levels. With more data on how host–pathogen, predator–prey, and other biotic interactions vary latitudinally, perhaps we will emerge with a greater understanding of the diverse mechanisms that contribute to the spectacular enrichment of tropical diversity.     

Likelihood methods for detecting temporal shifts in diversification rates

Maximum likelihood is a potentially powerful approach for investigating the tempo of diversification using molecular phylogenetic data. Likelihood methods distinguish between rate-constant and rate-variable models of diversification by fitting birth-death models to phylogenetic data. Because model selection in this context is a test of the null hypothesis that diversification rates have been constant over time, strategies for selecting best-fit models must minimize Type I error rates while retaining power to detect rate variation when it is present. Here I examine model selection, parameter estimation, and power to reject the null hypothesis using likelihood models based on the birth-death process. The Akaike information criterion (AIC) has often been used to select among diversification models; however, I find that selecting models based on the lowest AIC score leads to a dramatic inflation of the Type I error rate. When appropriately corrected to reduce Type I error rates, the birth-death likelihood approach performs as well or better than the widely used gamma statistic, at least when diversification rates have shifted abruptly over time. Analyses of datasets simulated under a range of rate-variable diversification scenarios indicate that the birth-death likelihood method has much greater power to detect variation in diversification rates when extinction is present. Furthermore, this method appears to be the only approach available that can distinguish between a temporal increase in diversification rates and a rate-constant model with nonzero extinction. I illustrate use of the method by analyzing a published phylogeny for Australian agamid lizards.     

Clade age and species richness are decoupled across the eukaryotic tree of life

Explaining the dramatic variation in species richness across the tree of life remains a key challenge in evolutionary biology. At the largest phylogenetic scales, the extreme heterogeneity in species richness observed among different groups of organisms is almost certainly a function of many complex and interdependent factors. However, the most fundamental expectation in macroevolutionary studies is simply that species richness in extant clades should be correlated with clade age: all things being equal, older clades will have had more time for diversity to accumulate than younger clades. Here, we test the relationship between stem clade age and species richness across 1,397 major clades of multicellular eukaryotes that collectively account for more than 1.2 million described species. We find no evidence that clade age predicts species richness at this scale. We demonstrate that this decoupling of age and richness is unlikely to result from variation in net diversification rates among clades. At the largest phylogenetic scales, contemporary patterns of species richness are inconsistent with unbounded diversity increase through time. These results imply that a fundamentally different interpretative paradigm may be needed in the study of phylogenetic diversity patterns in many groups of organisms.