POTENTIAL PITFALLS OF RECONSTRUCTING DEEP TIME EVOLUTIONARY HISTORY WITH ONLY EXTANT DATA,A CASE STUDY USING THE CANIDAE (MAMMALIA,CARNIVORA)

Reconstructing evolutionary patterns and their underlying processes is a central goal in biology. Yet many analyses of deep evolutionary histories assume that data from the fossil record is too incomplete to include, and rely solely on databases of extant taxa. Excluding fossil taxa assumes that character state distributions across living taxa are faithful representations of a clade's entire evolutionary history. Many factors can make this assumption problematic. Fossil taxa do not simply lead‐up to extant taxa; they represent now‐extinct lineages that can substantially impact interpretations of character evolution for extant groups. Here, we analyze body mass data for extant and fossil canids (dogs, foxes, and relatives) for changes in mean and variance through time. AIC‐based model selection recovered distinct models for each of eight canid subgroups. We compared model fit of parameter estimates for (1) extant data alone and (2) extant and fossil data, demonstrating that the latter performs significantly better. Moreover, extant‐only analyses result in unrealistically low estimates of ancestral mass. Although fossil data are not always available, reconstructions of deep‐time organismal evolution in the absence of deep‐time data can be highly inaccurate, and we argue that every effort should be made to include fossil data in macroevolutionary studies.     

Developmental bias in the fossil record

The role of developmental bias and plasticity in evolution is a central research interest in evolutionary biology. Studies of these concepts and related processes are usually conducted on extant systems and have seen limited investigation in the fossil record. Here, I identify plasticity‐led evolution (PLE) as a form of developmental bias accessible through scrutiny of paleontological material. I summarize the process of PLE and describe it in terms of the environmentally mediated accumulation and release of cryptic genetic variation. Given this structure, I then predict its manifestation in the fossil record, discuss its similarity to quantum evolution and punctuated equilibrium, and argue that these describe macroevolutionary patterns concordant with PLE. Finally, I suggest methods and directions towards providing evidence of PLE in the fossil record and conclude that such endeavors are likely to be highly rewarding.     

INTEGRATING FOSSILS WITH MOLECULAR PHYLOGENIES IMPROVES INFERENCE OF TRAIT EVOLUTION

Comparative biologists often attempt to draw inferences about tempo and mode in evolution by comparing the fit of evolutionary models to phylogenetic comparative data consisting of a molecular phylogeny with branch lengths and trait measurements from extant taxa. These kinds of approaches ignore historical evidence for evolutionary pattern and process contained in the fossil record. In this article, we show through simulation that incorporation of fossil information dramatically improves our ability to distinguish among models of quantitative trait evolution using comparative data. We further suggest a novel Bayesian approach that allows fossil information to be integrated even when explicit phylogenetic hypotheses are lacking for extinct representatives of extant clades. By applying this approach to a comparative dataset comprising body sizes for caniform carnivorans, we show that incorporation of fossil information not only improves ancestral state estimates relative to those derived from extant taxa alone, but also results in preference of a model of evolution with trend toward large body size over alternative models such as Brownian motion or Ornstein–Uhlenbeck processes. Our approach highlights the importance of considering fossil information when making macroevolutionary inference, and provides a way to integrate the kind of sparse fossil information that is available to most evolutionary biologists.     

Fossil‐based comparative analyses reveal ancient marine ancestry erased by extinction in ray‐finned fishes

The marine‐freshwater boundary is a major biodiversity gradient and few groups have colonised both systems successfully. Fishes have transitioned between habitats repeatedly, diversifying in rivers, lakes and oceans over evolutionary time. However, their history of habitat colonisation and diversification is unclear based on available fossil and phylogenetic data. We estimate ancestral habitats and diversification and transition rates using a large‐scale phylogeny of extant fish taxa and one containing a massive number of extinct species. Extant‐only phylogenetic analyses indicate freshwater ancestry, but inclusion of fossils reveal strong evidence of marine ancestry in lineages now restricted to freshwaters. Diversification and colonisation dynamics vary asymmetrically between habitats, as marine lineages colonise and flourish in rivers more frequently than the reverse. Our study highlights the importance of including fossils in comparative analyses, showing that freshwaters have played a role as refuges for ancient fish lineages, a signal erased by extinction in extant‐only phylogenies.     

To what extent do new fossil discoveries change our understanding of clade evolution? A cautionary tale from burying beetles (Coleoptera: Nicrophorus)

Divergence time estimates derived from phylogenies are crucial to infer historical biogeography and diversification dynamics. Yet, the impact of fossil record incompleteness on macroevolutionary reconstructions remains equivocal. Here, we investigate to what extent gaps in the fossil record can impinge downstream evolutionary inferences in the beetle family Silphidae. Recent discoveries have pushed back the fossil record of this group from the Eocene into the Jurassic. We estimated the divergence times of the family using both its currently understood fossil record and the fossil record known prior to these recent discoveries. All fossil calibrations were informed with different parametric distributions to investigate the weight of priors on posterior age estimates. Based on time‐calibrated trees, we assessed the impact of fossil calibrations on the inference of ancestral ranges and diversification rate dynamics in the genus Nicrophorus. Depending upon the selected sets of fossil constraints, the age discrepancies had a major impact on the macroevolutionary inferences: the biogeographic extrapolations relative to paleogeography are markedly contrasting, and the calculated rates at which species form or go extinct (and when they varied) are strikingly different. We show that soft prior distributions do not necessarily alleviate such shortcomings therefore preventing the inference of reliable macroevolutionary patterns in groups presenting a taphonomic bias in their fossil record.     

Early tetrapodomorph biogeography: Controlling for fossil record bias in macroevolutionary analyses

The fossil record provides direct empirical data for understanding macroevolutionary patterns and processes. Inherent biases in the fossil record are well known to confound analyses of this data. Sampling bias proxies have been used as covariates in regression models to test for such biases. Proxies, such as formation count, are associated with paleobiodiversity, but are insufficient for explaining species dispersal owing to a lack of geographic context. Here, we develop a sampling bias proxy that incorporates geographic information and test it with a case study on early tetrapodomorph biogeography. We use recently-developed Bayesian phylogeographic models and a new supertree of early tetrapodomorphs to estimate dispersal rates and ancestral habitat locations. We find strong evidence that geographic sampling bias explains supposed radiations in dispersal rate (potential adaptive radiations). Our study highlights the necessity of accounting for geographic sampling bias in macroevolutionary and phylogenetic analyses and provides an approach to test for its effect.     

Evolutionary innovations in the fossil record: the intersection of ecology, development, and macroevolution

The origins of evolutionary innovations have been intensively studied, but relatively little is known about their large-scale ecological patterns. For post-Paleozoic benthic marine invertebrates, which have the richest and most densely sampled fossil record, order-level taxa tend to appear first in onshore, disturbed habitats, even in groups that are now exclusively deep-water (so that present-day distributions are not reliable indicators of original environments). New results presented here show that the onshore-origination pattern is robust to shifts in taxonomic methods and to new paleontological discoveries, and the few available studies suggest that this pattern can also be seen in terms of excursions in morphospace or the acquisition of derived character states, without reference to taxonomic categories. The environmental pattern at high levels contrasts significantly with the origin of low-level novelties (such as defined genera and families) in crinoids, echinoids, and bryozoans, where first appearances tend to conform to their clade-specific bathymetric diversity gradients. This discordance seems to eliminate potential driving mechanisms that simply scale up within-population genetic or ecological processes. Little is known about the factors that promote the onshore-offshore expansion of orders across the continental shelf, or that drive some clades to abandon ancestral habitats for an exclusively deep-water distribution. The origin of evolutionary innovation must ultimately reside in developmental changes, but the onshore-origination bias could emerge from two different dynamics: the pattern could be primarily genetic and developmental, i.e., innovations truly arise onshore; or primarily ecological, i.e., innovations arise randomly but preferentially survive onshore. Whatever the ultimate driving mechanisms, these macroevolutionary patterns show that theories of large-scale evolutionary novelty must include an ecological dimension.     

A phylogeny of Cenozoic macroperforate planktonic foraminifera from fossil data

We present a complete phylogeny of macroperforate planktonic foraminifer species of the Cenozoic Era (∼65 million years ago to present). The phylogeny is developed from a large body of palaeontological work that details the evolutionary relationships and stratigraphic (time) distributions of species‐level taxa identified from morphology (‘morphospecies’). Morphospecies are assigned to morphogroups and ecogroups depending on test morphology and inferred habitat, respectively. Because gradual evolution is well documented in this clade, we have identified many instances of morphospecies intergrading over time, allowing us to eliminate ‘pseudospeciation’ and ‘pseudoextinction’ from the record and thereby permit the construction of a more natural phylogeny based on inferred biological lineages. Each cladogenetic event is determined as either budding or bifurcating depending on the pattern of morphological change at the time of branching. This lineage phylogeny provides palaeontologically calibrated ages for each divergence that are entirely independent of molecular data. The tree provides a model system for macroevolutionary studies in the fossil record addressing questions of speciation, extinction, and rates and patterns of evolution.     

Ghost Introgression: Spooky Gene Flow in the Distant Past

Evolution is a continuous trial and error process in which most lineages go extinct without leaving fossil remains. Many of these lineages would be closely related and occasionally hybridized with lineages that gave rise to extant species. Hence, it is likely that one can find genetic signatures of these ancient introgression events in present-day genomes, so-called ghost introgression. The increasing availability of high-quality genome assemblies for non-model organisms and the development of more sophisticated methods for detecting introgression will undoubtedly reveal more cases of ghost introgression, indicating that the Tree of Life is even more reticulated than assumed. The presence of ghost introgression has important consequences for the study of numerous evolutionary processes, including adaptation, speciation, and macroevolutionary patterns. In addition, detailed studies of introgressed regions could provide insights into the morphology of the extinct lineage, providing an unexpected link between genomics and the fossil record. Hence, new methods that take into account ghost introgression will need to be developed.     

Stickleback fishes: Bridging the gap between population biology and paleobiology

Integration of evolutionary mechanisms and phylogeny requires study of phenotypes that change in the fossil record and continue to evolve in extant populations. Pelvic reduction in the three-spined stickle-back has evolved rapidly in a Miocene fossil assemblage and in numerous extant isolated lake populations throughout its distribution. Although pelvic reduction is caused by selection, expression of reduced pelvic phenotypes is constrained by development and other factors. However, lineages with pelvis reduction rapidly go extinct while lineages that retain the fully formed pelvic girdle tend to persist. Existence of pelvic reduction since the Miocene has depended on an equilibrium between divergence and extinction. The phylogenetic topology resulting from this process differs greatly from the conventional view of evolutionary history, and could only be recognized by analysis of both extant populations and fossil material. If this phylogenetic topology is common, it may help to account for the different perceptions that population biologists and paleobiologists have of evolutionary tempo.     

Ancestral state reconstruction of body size in the Caniformia (Carnivora, Mammalia): the effects of incorporating data from the fossil record

A recent molecular phylogeny of the mammalian order Carnivora implied large body size as the ancestral condition for the caniform subclade Arctoidea using the distribution of species mean body sizes among living taxa. "Extant taxa-only" approaches such as these discount character state observations for fossil members of living clades and completely ignore data from extinct lineages. To more rigorously reconstruct body sizes of ancestral forms within the Caniformia, body size and first appearance data were collected for 149 extant and 367 extinct taxa. Body sizes were reconstructed for four ancestral nodes using weighted squared-change parsimony on log-transformed body mass data. Reconstructions based on extant taxa alone favored large body sizes (on the order of 10 to 50 kg) for the last common ancestors of both the Caniformia and Arctoidea. In contrast, reconstructions incorporating fossil data support small body sizes (< 5 kg) for the ancestors of those clades. When the temporal information associated with fossil data was discarded, body size reconstructions became ambiguous, demonstrating that incorporating both character state and temporal information from fossil taxa unambiguously supports a small ancestral body size, thereby falsifying hypotheses derived from extant taxa alone. Body size reconstructions for Caniformia, Arctoidea, and Musteloidea were not sensitive to potential errors introduced by uncertainty in the position of extinct lineages relative to the molecular topology, or to missing body size data for extinct members of an entire major clade (the aquatic Pinnipedia). Incorporating character state observations and temporal information from the fossil record into hypothesis testing has a significant impact on the ability to reconstruct ancestral characters and constrains the range of potential hypotheses of character evolution. Fossil data here provide the evidence to reliably document trends of both increasing and decreasing body size in several caniform clades. More generally, including fossils in such analyses incorporates evidence of directional trends, thereby yielding more reliable ancestral character state reconstructions.     

Phylogenetic Distribution of Extant Richness Suggests Metamorphosis Is a Key Innovation Driving Diversification in Insects

Insects and their six-legged relatives (Hexapoda) comprise more than half of all described species and dominate terrestrial and freshwater ecosystems. Understanding the macroevolutionary processes generating this richness requires a historical perspective, but the fossil record of hexapods is patchy and incomplete. Dated molecular phylogenies provide an alternative perspective on divergence times and have been combined with birth-death models to infer patterns of diversification across a range of taxonomic groups. Here we generate a dated phylogeny of hexapod families, based on previously published sequence data and literature derived constraints, in order to identify the broad pattern of macroevolutionary changes responsible for the composition of the extant hexapod fauna. The most prominent increase in diversification identified is associated with the origin of complete metamorphosis, confirming this as a key innovation in promoting insect diversity. Subsequent reductions are recovered for several groups previously identified as having a higher fossil diversity during the Mesozoic. In addition, a number of recently derived taxa are found to have radiated following the development of flowering plant (angiosperm) floras during the mid-Cretaceous. These results reveal that the composition of the modern hexapod fauna is a product of a key developmental innovation, combined with multiple and varied evolutionary responses to environmental changes from the mid Cretaceous floral transition onward.     

Molecular evolution of pteridophytes and their relationship to seed plants: Evidence from complete 18S rRNA gene sequences

Complete 18S ribosomal RNA sequence data from representatives of all extant pteridophyte lineages together with RNA sequences from different seed plants were used to infer a molecular phylogeny of vascular plants that included all major land plant lineages. The molecular data indicate that lycopsids are monophyletic and are the earliest diverging group within the vascular land plants, whereasPsilotum nudum is more closely related to the seed plants than to other pteridophyte lineages. The phylogenetic trees based on maximum likelihood, parsimony and distance analyses show substantial agreement with the evolutionary relationships of land plants as interpreted from the fossil record.     

Macroevolutionary Dynamics and Historical Biogeography of Primate Diversification Inferred from a Species Supermatrix

Phylogenetic relationships, divergence times, and patterns of biogeographic descent among primate species are both complex and contentious. Here, we generate a robust molecular phylogeny for 70 primate genera and 367 primate species based on a concatenation of 69 nuclear gene segments and ten mitochondrial gene sequences, most of which were extracted from GenBank. Relaxed clock analyses of divergence times with 14 fossil-calibrated nodes suggest that living Primates last shared a common ancestor 71–63 Ma, and that divergences within both Strepsirrhini and Haplorhini are entirely post-Cretaceous. These results are consistent with the hypothesis that the Cretaceous-Paleogene mass extinction of non-avian dinosaurs played an important role in the diversification of placental mammals. Previous queries into primate historical biogeography have suggested Africa, Asia, Europe, or North America as the ancestral area of crown primates, but were based on methods that were coopted from phylogeny reconstruction. By contrast, we analyzed our molecular phylogeny with two methods that were developed explicitly for ancestral area reconstruction, and find support for the hypothesis that the most recent common ancestor of living Primates resided in Asia. Analyses of primate macroevolutionary dynamics provide support for a diversification rate increase in the late Miocene, possibly in response to elevated global mean temperatures, and are consistent with the fossil record. By contrast, diversification analyses failed to detect evidence for rate-shift changes near the Eocene-Oligocene boundary even though the fossil record provides clear evidence for a major turnover event (“Grande Coupure”) at this time. Our results highlight the power and limitations of inferring diversification dynamics from molecular phylogenies, as well as the sensitivity of diversification analyses to different species concepts.     

Spatiotemporal sampling patterns in the 230 million year fossil record of terrestrial crocodylomorphs and their impact on diversity

The 24 extant crocodylian species are the remnants of a once much more diverse and widespread clade. Crocodylomorpha has an approximately 230 million year evolutionary history, punctuated by a series of radiations and extinctions. However, the group's fossil record is biased. Previous studies have reconstructed temporal patterns in subsampled crocodylomorph palaeobiodiversity, but have not explicitly examined variation in spatial sampling, nor the quality of this record. We compiled a dataset of all taxonomically diagnosable non‐marine crocodylomorph species (393). Based on the number of phylogenetic characters that can be scored for all published fossils of each species, we calculated a completeness value for each taxon. Mean average species completeness (56%) is largely consistent within subgroups and for different body size classes, suggesting no significant biases across the crocodylomorph tree. In general, average completeness values are highest in the Mesozoic, with an overall trend of decreasing completeness through time. Many extant taxa are identified in the fossil record from very incomplete remains, but this might be because their provenance closely matches the species’ present‐day distribution, rather than through autapomorphies. Our understanding of nearly all crocodylomorph macroevolutionary ‘events’ is essentially driven by regional patterns, with no global sampling signal. Palaeotropical sampling is especially poor for most of the group's history. Spatiotemporal sampling bias impedes our understanding of several Mesozoic radiations, whereas molecular divergence times for Crocodylia are generally in close agreement with the fossil record. However, the latter might merely be fortuitous, i.e. divergences happened to occur during our ephemeral spatiotemporal sampling windows.     

Phylogeny and evolutionary history of diplobathrid crinoids (Echinodermata)

Order Diplobathrida is a major clade of camerate crinoids spanning the Ordovician–Mississippian, yet phylogenetic relationships have only been inferred for Ordovician taxa. This has hampered efforts to construct a comprehensive tree of life for crinoids and develop a classification scheme that adequately reflects diplobathrid evolutionary history. Here, I apply maximum parsimony and Bayesian phylogenetic approaches to the fossil record of diplobathrids to infer the largest tree of fossil crinoids to date, with over 100 genera included. Recovered trees provide a framework for evaluating the current classification of diplobathrids. Notably, previous suborder divisions are not supported, and superfamily divisions will require significant modification. Although numerous revisions are required for families, most can be retained through reassignment of genera. In addition, recovered trees were used to produce phylogeny‐based estimates of diplobathrid lineage diversity. By accounting for ghost lineages, phylogeny‐based richness estimates offer greater insight into diversification and extinction dynamics than traditional taxonomy‐based approaches alone and provide a detailed summary of the ~150 million‐year evolutionary history of Diplobathrida. This study constitutes a major step toward producing a phylogeny of the Crinoidea and documenting crinoid diversity dynamics. In addition, it will serve as a framework for subsequent phylogeny‐based investigations of macroevolutionary questions.     

BOOM AND BUST: ANCIENT AND RECENT DIVERSIFICATION IN BICHIRS (POLYPTERIDAE: ACTINOPTERYGII), A RELICTUAL LINEAGE OF RAY‐FINNED FISHES

Understanding the history that underlies patterns of species richness across the Tree of Life requires an investigation of the mechanisms that not only generate young species‐rich clades, but also those that maintain species‐poor lineages over long stretches of evolutionary time. However, diversification dynamics that underlie ancient species‐poor lineages are often hidden due to a lack of fossil evidence. Using information from the fossil record and time calibrated molecular phylogenies, we investigate the history of lineage diversification in Polypteridae, which is the sister lineage of all other ray‐finned fishes (Actinopterygii). Despite originating at least 390 million years (Myr) ago, molecular timetrees support a Neogene origin for the living polypterid species. Our analyses demonstrate polypterids are exceptionally species depauperate with a stem lineage duration that exceeds 380 million years (Ma) and is significantly longer than the stem lineage durations observed in other ray‐finned fish lineages. Analyses of the fossil record show an early Late Cretaceous (100.5–83.6 Ma) peak in polypterid genus richness, followed by 60 Ma of low richness. The Neogene species radiation and evidence for high‐diversity intervals in the geological past suggest a “boom and bust” pattern of diversification that contrasts with common perceptions of relative evolutionary stasis in so‐called “living fossils.”     

Green algae to land plants: An evolutionary transition

Studies focused upon the evolutionary transition from ancestral green algae to the earliest land plants are important from a range of ecological, molecular and evolutionary perspectives. A substantial suite of ultrastructural, biochemical and molecular data supports the concept that land plants (embryophytes) are monophyletically derived from an ancestral charophycean alga. However, the details of phylogenetic branching patterns linking extant charophytes and seedless embryophytes are currently unclear. Moreover, the fossil record has so far been mute regarding the algae-land plant transition. Nevertheless, an accurate reflection of major evolutionary events in the history of the earliest land plants can be obtained by comparative paleontological-neontological studies, and comparative molecular, cellular and developmental investigations of extant charophytes and bryophytes. This review focuses upon research progress toward understanding three clade-specific adaptations that were important in the successful colonization of land by plants: the histogenetic apical meristem, the matrotrophic embryo, and decay-resistant cell wall polymers.     

The origins of Dinosauria: much ado about nothing

Research this century has greatly improved our knowledge of the origin and early radiation of dinosaurs. The unearthing of several new dinosaurs and close outgroups from Triassic rocks from various parts of the world, coupled with improved phylogenetic analyses, has set a basic framework in terms of timing of events and macroevolutionary patterns. However, important parts of the early dinosauromorph evolutionary history are still poorly understood, rendering uncertain the phylogenetic position of silesaurids as either non‐dinosaur Dinosauriformes or ornithischians, as well as that of various early saurischians, such as Eoraptor lunensis and herrerasaurs, as either noneusaurischians or members of the sauropodomorph or theropod lineages. This lack of agreement in part derives from a patchy distribution of traits among early members of the main dinosauromorph lineages and requires a more meticulous assessment of characters and homologies than those recently conducted. Presently, the oldest uncontroversial dinosaur records come from Late Triassic (Carnian) rocks of South America, southern Africa and India, hinting at a south‐western Pangaea origin of the group. Besides, macroevolutionary approaches suggest that the rise of dinosaurs was a more gradual process than previously understood. Obviously, these tentative scenarios need to be tested by new fossil finds, which should also help close the major gaps recognized in the fossil record of Triassic dinosauromorphs.     

Fossils and living taxa agree on patterns of body mass evolution: a case study with Afrotheria

Most of life is extinct, so incorporating some fossil evidence into analyses of macroevolution is typically seen as necessary to understand the diversification of life and patterns of morphological evolution. Here we test the effects of inclusion of fossils in a study of the body size evolution of afrotherian mammals, a clade that includes the elephants, sea cows and elephant shrews. We find that the inclusion of fossil tips has little impact on analyses of body mass evolution; from a small ancestral size (approx. 100 g), there is a shift in rate and an increase in mass leading to the larger-bodied Paenungulata and Tubulidentata, regardless of whether fossils are included or excluded from analyses. For Afrotheria, the inclusion of fossils and morphological character data affect phylogenetic topology, but these differences have little impact upon patterns of body mass evolution and these body mass evolutionary patterns are consistent with the fossil record. The largest differences between our analyses result from the evolutionary model, not the addition of fossils. For some clades, extant-only analyses may be reliable to reconstruct body mass evolution, but the addition of fossils and careful model selection is likely to increase confidence and accuracy of reconstructed macroevolutionary patterns.