Susana Magallón

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.

Ferns diversified in the shadow of angiosperms

The rise of angiosperms during the Cretaceous period is often portrayed as coincident with a dramatic drop in the diversity and abundance of many seed-free vascular plant lineages, including ferns. This has led to the widespread belief that ferns, once a principal component of terrestrial ecosystems, succumbed to the ecological predominance of angiosperms and are mostly evolutionary holdovers from the late Palaeozoic/early Mesozoic era. The first appearance of many modern fern genera in the early Tertiary fossil record implies another evolutionary scenario; that is, that the majority of living ferns resulted from a more recent diversification. But a full understanding of trends in fern diversification and evolution using only palaeobotanical evidence is hindered by the poor taxonomic resolution of the fern fossil record in the Cretaceous. Here we report divergence time estimates for ferns and angiosperms based on molecular data, with constraints from a reassessment of the fossil record. We show that polypod ferns (> 80% of living fern species) diversified in the Cretaceous, after angiosperms, suggesting perhaps an ecological opportunistic response to the diversification of angiosperms, as angiosperms came to dominate terrestrial ecosystems.

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.

A metacalibrated time-tree documents the early rise of flowering plant phylogenetic diversity

The establishment of modern terrestrial life is indissociable from angiosperm evolution. While available molecular clock estimates of angiosperm age range from the Paleozoic to the Late Cretaceous, the fossil record is consistent with angiosperm diversification in the Early Cretaceous. The time-frame of angiosperm evolution is here estimated using a sample representing 87% of families and sequences of five plastid and nuclear markers, implementing penalized likelihood and Bayesian relaxed clocks. A literature-based review of the palaeontological record yielded calibrations for 137 phylogenetic nodes. The angiosperm crown age was bound within a confidence interval calculated with a method that considers the fossil record of the group. An Early Cretaceous crown angiosperm age was estimated with high confidence. Magnoliidae, Monocotyledoneae and Eudicotyledoneae diversified synchronously 135-130 million yr ago (Ma); Pentapetalae is 126-121 Ma; and Rosidae (123-115 Ma) preceded Asteridae (119-110 Ma). Family stem ages are continuously distributed between c. 140 and 20 Ma. This time-frame documents an early phylogenetic proliferation that led to the establishment of major angiosperm lineages, and the origin of over half of extant families, in the Cretaceous. While substantial amounts of angiosperm morphological and functional diversity have deep evolutionary roots, extant species richness was probably acquired later.

Dating Lineages: Molecular and Paleontological Approaches to the Temporal Framework of Clades

The recent proliferation of methodological advances in molecular phylogenetic and paleobiological research has resulted in powerful approaches to investigate the temporal framework of lineages. This article is a review of molecular and paleontological methods to estimate ages of clades. Inferring ages of clades is complicated by the nature of the process of molecular substitution and the uncertainties of the paleontological record. Some of the greatest problems associated with molecular methods include the stochastic nature of molecular substitution, the assumption of rate constancy among lineages when such constancy is absent, and the inextricable link between substitution rate and elapsed time on the branches of phylogeny. Molecular methods to estimate ages are ultimately based on the fact that as time elapses, molecular differences accumulate among sequences. Under rate constancy, methods to estimate ages include linear regression of molecular distance on elapsed time and maximum likelihood optimization of node ages under a single rate. Recently developed methods that allow rate heterogeneity are powerful approaches to estimate rates and divergence times under more realistic assumptions. Among‐lineage rate variation is introduced as a compound Poisson process or more frequently is guided by the principle of temporal rate autocorrelation. These methods are based on numerical, semiparametric, and Bayesian parametric approaches, and some allow incorporation of constraints on the ages of nodes (derived, e.g., from fossils), conferring additional realism to age estimates. The paleontological record provides times of first appearances of morphological traits but not of lineage divergences; nevertheless, it represents one of the few sources of absolute information to decouple rates and times in a phylogeny. Analytical methods applied to paleontological data provide an alternative source of information about lineage duration. Stratigraphic confidence intervals that contain the time of origin of a lineage under a known probability are based on the frequency and abundance of fossil finds through the lineage’s fossil record. Tests of postulated lineage durations, derived, for example, from a molecular age estimate, are available under probabilistic or likelihood frameworks. A powerful approach toward achieving more robust inferences about evolutionary rates and timing of lineage divergence lies in the complementary use of molecular‐ and paleontological‐based approaches. While incorporating fossil information as age constraints confers further realism to molecular‐estimated rates and ages, such estimates may be evaluated against expectations derived from paleontological information.

Land plant evolutionary timeline: Gene effects are secondary to fossil constraints in relaxed clock estimation of age and substitution rates

UNLABELLED PREMISE OF THE STUDY Land plants play an essential role in the evolution of terrestrial life. Their time of origin and diversification is fundamental to understanding the evolution of life on land. We investigated the timing and the rate of molecular evolution of land plants, evaluating the effects of different types of molecular data, including temporal information from fossils, and using different molecular clock methods. • METHODS Ages and absolute rates were estimated independently with two substitutionally different data sets: a highly conserved 4-gene data set and matK, a fast-evolving gene. The vascular plant backbone and the crown nodes of all major lineages were calibrated with fossil-derived ages. Dates and absolute rates were estimated while including or excluding the calibrations and using two relaxed clocks that differ in their implementation of temporal autocorrelation. • KEY RESULTS Land plants diverged from streptophyte alga 912 (870-962) million years ago (Mya) but diversified into living lineages 475 (471-480) Mya. Ages estimated for all major land-plant lineages agree with their fossil record, except for angiosperms. Different genes estimated very similar ages and correlated absolute rates across the tree. Excluding calibrations resulted in the greatest age differences. Different relaxed clocks provided similar ages, but different and uncorrelated absolute rates. • CONCLUSIONS Whole-genome rate accelerations or decelerations may underlie the similar ages and correlated absolute rates estimated with different genes. We suggest that pronounced substitution rate changes around the angiosperm crown node may represent a challenge for relaxed clocks to model adequately.

Using fossils to break long branches in molecular dating: a comparison of relaxed clocks applied to the origin of angiosperms.

Long branches are potentially problematic in molecular dating because they can encompass a vast number of combinations of substitution rate and time. A long branch is suspected to have biased molecular clock estimates of the age of flowering plants (angiosperms) to be much older than their earliest fossils. This study explores the effect of the long branch subtending angiosperms in molecular dating and how different relaxed clocks react to it. Fossil angiosperm relatives, identified through a combined morphological and molecular phylogenetic analysis for living and fossil seed plants, were used to break the long angiosperm stem branch. Nucleotide sequences of angiosperm fossil relatives were simulated using a phylogeny and model parameters from living taxa and incorporated in molecular dating. Three relaxed clocks, which implement among-lineage rate heterogeneity differently, were used: penalized likelihood (using 2 different rate smoothing optimization criteria), a Bayesian rate-autocorrelated method, and a Bayesian uncorrelated method. Different clocks provided highly correlated ages across the tree. Breaking the angiosperm stem branch did not result in major age differences, except for a few sensitive nodes. Breaking the angiosperm stem branch resulted in a substantially younger age for crown angiosperms only with 1 of the 4 methods, but, nevertheless, the obtained age is considerably older than the oldest angiosperm fossils. The origin of crown angiosperms is estimated between the Upper Triassic and the early Permian. The difficulty in estimating crown angiosperm age probably lies in a combination of intrinsic and extrinsic complicating factors, including substantial molecular rate heterogeneity among lineages and through time. A more adequate molecular dating approach might combine moderate background rate heterogeneity with large changes in rate at particular points in the tree.

Relationships among seed plants inferred from highly conserved genes: sorting conflicting phylogenetic signals among ancient lineages

Phylogenetic studies based on different types and treatment of data provide substantially conflicting hypotheses of relationships among seed plants. We conducted phylogenetic analyses of sequences of two highly conserved chloroplast genes, psaA and psbB, for a comprehensive taxonomic sample of seed plants and land plants. Parsimony analyses of two different codon position partitions resulted in well-supported, but significantly conflicting, phylogenetic trees. First and second codon positions place angiosperms and gymnosperms as sister clades and Gnetales as sister to Pinaceae. Third positions place Gnetales as sister to all other seed plants. Maximum likelihood trees for the two partitions are also in conflict. Relationships among the main seed plant clades according to first and second positions are similar to those found in parsimony analysis for the same data, but the third position maximum likelihood tree is substantially different from the corresponding parsimony tree, although it agrees partially with the first and second position trees in placing Gnetales as the sister group of Pinaceae. Our results document high rate heterogeneity among lineages, which, together with the greater average rate of substitution for third positions, may reduce phylogenetic signal due to long-branch attraction in parsimony reconstructions. Whereas resolution of relationships among major seed plant clades remains pending, this study provides increased support for relationships within major seed plant clades.

Use of simultaneous analyses to guide fossil-based calibrations of Pinaceae phylogeny

Uncertainties in the age and phylogenetic position of Pinaceae fossils present significant obstacles to our understanding of the timing of diversification in the family. We demonstrate that simultaneous phylogenetic analyses of chloroplast DNA (matK and rbcL) and nonmolecular characters that include both extant genera and a limited number of fossil taxa provide useful hypotheses for calibrating molecular trees. Root placements varied for Pinaceae, with Bayesian analyses recovering mutually monophyletic subfamilies Pinoideae and Abietoideae and parsimony analyses recovering Abietoideae as paraphyletic by placing the root between Cedrus and the remaining genera. The inferred phylogenetic positions of fossil taxa Pityostrobus bernissartensis as the sister group to Pinus and Pseudolarix erensis as the sister group to extant Pseudolarix were used to guide divergence‐time calibrations; these calibrations yielded an Early Cretaceous and an Early Jurassic age for crown‐group Pinaceae, respectively. The older age estimates based on Pseudolarix erensis are supported by weaker evidence from the fossil record but are consistent with recent reports of Early Cretaceous leaf fossils that appear to coincide with extant genera. There remains a great need to characterize the anatomy of extant and fossil species and to code additional nonmolecular characters.

Evolutionary biology in biodiversity science, conservation, and policy: A call to action

Evolutionary biologists have long endeavored to document how many species exist on Earth, to understand the processes by which biodiversity waxes and wanes, to document and interpret spatial patterns of biodiversity, and to infer evolutionary relationships. Despite the great potential of this knowledge to improve biodiversity science, conservation, and policy, evolutionary biologists have generally devoted limited attention to these broader implications. Likewise, many workers in biodiversity science have underappreciated the fundamental relevance of evolutionary biology. The aim of this article is to summarize and illustrate some ways in which evolutionary biology is directly relevant. We do so in the context of four broad areas: (1) discovering and documenting biodiversity, (2) understanding the causes of diversification, (3) evaluating evolutionary responses to human disturbances, and (4) implications for ecological communities, ecosystems, and humans. We also introduce bioGENESIS, a new project within DIVERSITAS launched to explore the potential practical contributions of evolutionary biology. In addition to fostering the integration of evolutionary thinking into biodiversity science, bioGENESIS provides practical recommendations to policy makers for incorporating evolutionary perspectives into biodiversity agendas and conservation. We solicit your involvement in developing innovative ways of using evolutionary biology to better comprehend and stem the loss of biodiversity.