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Variation in species richness across the tree of life, accompanied by the incredible variety of ecological and morphological characteristics found in nature, has inspired many studies to link traits with species diversification. Angiosperms are a highly diverse group that has fundamentally shaped life on earth since the Cretaceous, and illustrate how species diversification affects ecosystem functioning. Numerous traits and processes have been linked to differences in species richness within this group, but we know little about how these interact and their relative importance. Here, we synthesized data from 152 studies that used state-dependent speciation and extinction (SSE) models on angiosperm clades. Intrinsic traits related to reproduction and morphology were often linked to diversification but a set of universal drivers did not emerge as traits did not have consistent effects across clades. Importantly, dataset properties were correlated to SSE model results - trees that were larger, older, or less well-sampled tended to yield trait-dependent outcomes. We compared these properties to recommendations for SSE model use and provide a set of best practices to follow when designing studies and reporting results. Finally, we argue that SSE model inferences should be considered in a larger context incorporating species’ ecology, demography and genetics.

The present-day ubiquity of angiosperm-insect pollination has led to the hypothesis that these two groups coevolved early in their evolutionary history. However, recent fossil discoveries and fossil-calibrated molecular dating analyses challenge the notion that early diversifications of angiosperms and insects were inextricably linked. In this article, we examine (i) the discrepancies between dates of emergence for angiosperms and major clades of insects; (ii) the long history of gymnosperm-insect pollination modes, which likely shaped early angiosperm-insect pollination mutualisms; and (iii) how the K-Pg (Cretaceous-Paleogene) mass extinction event was vital in propelling modern angiosperm-insect mutualisms. We posit that the early diversifications of angiosperms and their insect pollinators were largely decoupled until the end of the Cretaceous.

SummaryPollination is a fundamental process driving the speciation of angiosperms (flowering plants). Most contemporary angiosperms are insect pollinated, but abiotic pollination by wind or water and vertebrate pollination by birds or mammals occurs in many lineages. We model the evolution of pollination across angiosperms and quantify the timing and environmental associations of pollination shifts.We use a robust dated phylogeny and trait-independent species-level sampling across all families of angiosperms to model the evolution of pollination modes. Data on the pollination system or syndrome of 1160 species were collated from primary literature.Angiosperms were ancestrally insect pollinated, and insects have pollinated angiosperms for approximately 86% of angiosperm evolutionary history. Wind pollination evolved at least 42 times, with few reversals back to animal pollination. Transitions between insect and vertebrate pollination were more frequent: vertebrate pollination evolved at least 39 times from an insect pollinated ancestor with at least 26 reversals. The probability of wind pollination increases with habitat openness (measured by Leaf Area Index) and with distance from the equator.Our reconstruction of pollination across angiosperms sheds light on a key question in angiosperm macroevolution, highlighting the long history of interactions between insect pollinators and angiosperms still vital to global biodiversity today.

Premise of the StudyRecent studies of floral disparity in the asterid order Ericales have shown that flowers vary strongly among families and that disparity is unequally distributed between the three flower modules (perianth, androecium, gynoecium). However, it remains unknown whether these patterns are driven by heterogeneous rates of morphological evolution or other factors.MethodsHere, we compiled a dataset of 33 floral characters scored for 414 extant ericalean species sampled from 346 genera and all 22 families. We conducted ancestral state reconstructions using an equal rates Markov models for each trait. We used the rates estimated during the ancestral state reconstruction for comparing evolutionary rates between flower modules, creating a “rate profile” of ericalean flowers.Key ResultsThe androecium exhibits the highest evolutionary rates across most characters, whereas most perianth and gynoecium characters evolve slower. High and low rates of morphological evolution can result in high floral disparity in Ericales. Analyses of an angiosperm-wide floral dataset reveal that this pattern appears to be conserved across most major angiosperm clades.ConclusionsElevated rates of morphological evolution in the androecium of Ericales may explain the higher disparity reported for this floral module. We discuss the implications of heterogenous morphological rates of evolution among floral modules from a functional perspective. Comparing rates of morphological evolution through rate profiles proves to be a powerful tool in understanding floral evolution.

Determining the link between genomic and phenotypic evolution is a fundamental goal in evolutionary biology. Insights into this link can be gained by using a phylogenetic approach to test for correlations between rates of molecular and morphological evolution. However, there has been persistent uncertainty about the relationship between these rates, partly because conflicting results have been obtained using various methods that have not been examined in detail. We carried out a simulation study to evaluate the performance of five statistical methods for detecting correlated rates of evolution. Our simulations explored the evolution of molecular sequences and morphological characters under a range of conditions. Of the methods tested, Bayesian relaxed-clock estimation of branch rates was able to detect correlated rates of evolution correctly in the largest number of cases. This was followed by correlations of root-to-tip distances, Bayesian model selection, independent sister-pairs contrasts, and likelihood-based model selection. As expected, the power to detect correlated rates increased with the amount of data, both in terms of tree size and number of morphological characters. Likewise, the performance of all five methods improved when there was greater rate variation among lineages. We then applied these methods to a data set from flowering plants and did not find evidence of a correlation in evolutionary rates between genomic data and morphological characters. The results of our study have practical implications for phylogenetic analyses of combined molecular and morphological data sets, and highlight the conditions under which the links between genomic and phenotypic rates of evolution can be evaluated quantitatively.

Fossil flowers are essential to infer past angiosperm evolutionary processes. The assignment of fossil flowers to extant clades has traditionally relied on morphological similarity and on apomorphies shared with extant taxa. The use of explicit phylogenetic analyses to establish their affinity has so far remained limited. In this study, we built a comprehensive framework to investigate the phylogenetic placement of 24 exceptionally preserved fossil flowers. For this, we assembled a new species-level dataset of 30 floral traits for 1201 extant species that were sampled to represent the stem and crown nodes of all angiosperm families. We explored multiple analytical approaches to integrate the fossils into the phylogeny, including different phylogenetic estimation methods, topological-constrained analyses, and a total evidence approach combining molecular and morphological data of extant and fossil species. Our results were widely consistent across approaches, with minor differences in the support of fossils at different phylogenetic positions. The placement of some fossils is in agreement with previously suggested relationships, but for others, a new placement is indicated. We also identified fossils that are well constrained within particular extant families, whereas others showed high phylogenetic uncertainty. Finally, we present recommendations for future total evidence analyses, regarding the selection of fossils and appropriate methodologies, and provide some perspectives on how to integrate fossils into the investigation of divergence times and the temporal evolution of morphological traits.