Modelling the past: new generation approaches to understanding biological patterns in the fossil record

The history of life on this planet is gleaned from analysing how fossils are distributed through time and space. While these patterns are now rather securely known, at least for well-studied parts of the world, their interpretation remains far from simple. Fossils preserve only partial data from which to reconstruct their biology and the geological record is incomplete and biased, so that taxonomic ranges and palaeocommunity structure are imperfectly known. To better understand the often highly complex deep-time processes that gave rise to the empirical fossil record, palaeontologists have turned to modelling the past. Here, we summarize a series of 11 papers that showcase where modelling the past is being applied to advance our understanding across a wide spectrum of current palaeontological endeavours.     

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.     

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.     

Calibrating the Tree of Life: fossils, molecules and evolutionary timescales

Background

Molecular dating has gained ever-increasing interest since the molecular clock hypothesis was proposed in the 1960s. Molecular dating provides detailed temporal frameworks for divergence events in phylogenetic trees, allowing diverse evolutionary questions to be addressed. The key aspect of the molecular clock hypothesis, namely that differences in DNA or protein sequence between two species are proportional to the time elapsed since they diverged, was soon shown to be untenable. Other approaches were proposed to take into account rate heterogeneity among lineages, but the calibration process, by which relative times are transformed into absolute ages, has received little attention until recently. New methods have now been proposed to resolve potential sources of error associated with the calibration of phylogenetic trees, particularly those involving use of the fossil record.

Scope and Conclusions

The use of the fossil record as a source of independent information in the calibration process is the main focus of this paper; other sources of calibration information are also discussed. Particularly error-prone aspects of fossil calibration are identified, such as fossil dating, the phylogenetic placement of the fossil and the incompleteness of the fossil record. Methods proposed to tackle one or more of these potential error sources are discussed (e.g. fossil cross-validation, prior distribution of calibration points and confidence intervals on the fossil record). In conclusion, the fossil record remains the most reliable source of information for the calibration of phylogenetic trees, although associated assumptions and potential bias must be taken into account.     

Cladistics and the land plants: A response to Robinson

The reconstruction of phylogenetic relationships should be based not on belief but on an explicit and logical analysis of all available characters. Hennigian phylogenetic systematics (cladistics) provides a framework for evaluating putative homologies characterizing particular hierarchical levels, determining relationships of taxa sharing congruent patterns of homologies, and constructing a classification based on this information. Fossils can and should be included in the analysis if enough of the relevant characters are preserved; this is not currently possible for early land plants because of the fragmentary fossil record. To avoid circularity, adaptive and functional considerations should be addressed only after a phylogenetic hypothesis based on patterns on patterns of shared homologies is available.     

The importance of even highly incomplete fossil taxa in reconstructing the phylogenetic relationships of the tetraodontiformes (acanthomorpha: pisces)

The use of fossils in the phylogenetics of extant clades traditionallyhas been a contentious issue. Fossils usually are relativelyincomplete, and their use commonly leads to an increase in thenumber of equally most parsimonious trees and a decrease inthe resolution of phylogenies. Fossils alone, however, providecertain kinds of information about the biological history ofa clade, and computer simulations have shown that even highlyincomplete material can, under certain circumstances, increasethe accuracy of a phylogeny, rather than decrease it. Because empirical data are still scarce on the effects of theinclusion of fossils on phylogenetic reconstructions, we attemptedto investigate this problem by using a relatively well-knowngroup of acanthomorph fishes, the Tetraodontiformes (triggerfishes,pufferfishes, and ocean sunfishes), for which robust phylogeniesusing extant taxa already exist and that has a well-studiedfossil record. Adding incomplete fossil taxa of tetraodontiformsusually increases the number of equally most parsimonious treesand often decreases the resolution of consensus trees. However,adding fossil taxa may help to correctly establish relationshipsamong lineages that have experienced high degrees of morphologicaldiversification by allowing for a reinterpretation of homologousand homoplastic features, increasing the resolution rather thandecreasing it. Furthermore, taxa that were scored for 25% ormore of their characters did not cause a significant loss ofresolution, while providing unique biological information.     

CONGRUENCE BETWEEN SUPERPOSITIONAL AND PHYLOGENETIC PATTERNS: COMPARING CLADISTIC PATTERNS WITH FOSSIL RECORDS

Abstract— As the only direct evidence of past organismic history, the fossil record has always figured importantly in the reconstruction of phylogeny. But the incomplete nature of the fossil record has also been cited as a basis for claiming that fossils play only a secondary role in developing phylogenetic hypotheses that encompass extant taxa. The reliability of fossil data in such applications is a function of the degree of fit between superpositional relationships and the sequence of phylogenetic events. Thirty-eight vertebrate cases are examined for the fit between age data based on fossil first occurrences and phylogenetic results based on cladistic analysis. A general correspondence between superpositional and cladistic information is observed, although the degree of fit varies widely among cases. Horses, certain other ungulates, synapsids and basal archosaurs, which show very high correlations, are taxa characterized by an abundance of superpositional and cladistic data. Other groups, such as primates, show very poor correlations because certain major clades have either unreasonably short fossil durations or no fossil record at all. Correlations are also diminished when either fossil records or cladistic sequences are poorly resolved. In most cases, cladistic resolution was observed to exceed superpositional resolution. Correlations can be enhanced by more precise (e.g. radiometric) age dates, but these also place a high expectation on the fit between fossil first occurrence and cladistic results. Stratigraphic occurrence does not always provide a precise reflection of independently derived phylogenies, but the correspondence between age and cladistic information is remarkably high in a notable number of vertebrate examples.     

Exploring macroevolution using modern and fossil data

Macroevolution, encompassing the deep-time patterns of the origins of modern biodiversity, has been discussed in many contexts. Non-Darwinian models such as macromutations have been proposed as a means of bridging seemingly large gaps in knowledge, or as a means to explain the origin of exquisitely adapted body plans. However, such gaps can be spanned by new fossil finds, and complex, integrated organisms can be shown to have evolved piecemeal. For example, the fossil record between dinosaurs and Archaeopteryx has now filled up with astonishing fossil intermediates that show how the unique plexus of avian adaptations emerged step by step over 60 Myr. New numerical approaches to morphometrics and phylogenetic comparative methods allow palaeontologists and biologists to work together on deep-time questions of evolution, to explore how diversity, morphology and function have changed through time. Patterns are more complex than sometimes expected, with frequent decoupling of species diversity and morphological diversity, pointing to the need for some new generalizations about the processes that lie behind such patterns.     

Taxonomic identification bias does not drive patterns of abundance and diversity in theropod dinosaurs

The ability of palaeontologists to correctly diagnose and classify new fossil species from incomplete morphological data is fundamental to our understanding of evolution. Different parts of the vertebrate skeleton have different likelihoods of fossil preservation and varying amounts of taxonomic information, which could bias our interpretations of fossil material. Substantial previous research has focused on the diversity and macroevolution of non-avian theropod dinosaurs. Theropods provide a rich dataset for analysis of the interactions between taxonomic diagnosability and fossil preservation. We use specimen data and formal taxonomic diagnoses to create a new metric, the Likelihood of Diagnosis, which quantifies the diagnostic likelihood of fossil species in relation to bone preservation potential. We use this to assess whether a taxonomic identification bias impacts the non-avian theropod fossil record. We find that the patterns of differential species abundance and clade diversity are not a consequence of their relative diagnosability. Although there are other factors that bias the theropod fossil record that are not investigated here, our results suggest that patterns of relative abundance and diversity for theropods might be more representative of Mesozoic ecology than often considered.     

Fossil moonseeds from the Paleogene of West Gondwana (Patagonia,Argentina)

Premise of the Study

The fossil record is critical for testing biogeographic hypotheses. Menispermaceae (moonseeds) are a widespread family with a rich fossil record and alternative hypotheses related to their origin and diversification. The family is well‐represented in Cenozoic deposits of the northern hemisphere, but the record in the southern hemisphere is sparse. Filling in the southern record of moonseeds will improve our ability to evaluate alternative biogeographic hypotheses.

Methods

Fossils were collected from the Salamanca (early Paleocene, Danian) and the Huitrera (early Eocene, Ypresian) formations in Chubut Province, Argentina. We photographed them using light microscopy, epifluorescence, and scanning electron microscopy and compared the fossils with similar extant and fossil Menispermaceae using herbarium specimens and published literature.

Key Results

We describe fossil leaves and endocarps attributed to Menispermaceae from Argentinean Patagonia. The leaves are identified to the family, and the endocarps are further identified to the tribe Cissampelideae. The Salamancan endocarp is assigned to the extant genus Stephania. These fossils significantly expand the known range of Menispermaceae in South America, and they include the oldest (ca. 64 Ma) unequivocal evidence of the family worldwide.

Conclusions

Our findings highlight the importance of West Gondwana in the evolution of Menispermaceae during the Paleogene. Currently, the fossil record does not discern between a Laurasian or Gondwanan origin; however, it does demonstrate that Menispermaceae grew well outside the tropics by the early Paleocene. The endocarps’ affinity with Cissampelideae suggests that diversification of the family was well underway by the earliest Paleocene.     

Palaeontology and Evolutionary Developmental Biology: A Science of the Nineteenth and Twenty–first Centuries

A wind of change has swept through palaeontology in the past few decades. Contrast Sir Peter Medawar’s dismissive: ‘palaeontology is a particularly undemanding branch of science’ (as recalled by John Maynard Smith in Sabbagh 1999, p. 158) with ‘Palaeontology: grasping the opportunities in the science of the twenty–first century’, the title of a contribution to a special issue of Geobios by the Cambridge palaeontologist, Simon Conway Morris (1998a). The winds of change have come partly from palaeontologists seeking to broaden the impact of their studies and partly from biologists (neontologists) realizing the contributions that palaeontology can make to their disciplines. Consequently, impressions of past life preserved in stone are coming alive. Fossils are being described and analyzed using new tools and languages as the static fossil record becomes a record of transitions in patterns that can be explained and related to biological, ecological, climatic and tectonic changes. The latest addition is evolutionary developmental biology, or ‘evo–devo’, whose language provides a new basis upon which to interpret anatomical change, both materially and mechanistically. In this review I examine the major contributions made by palaeontology, how palaeontology has been linked to evolution and to embryology in the past, and how links with evo–devo have enlivened and will continue to enliven both palaeontology and evo–devo. Closer links between the two fields should illuminate important unresolved issues related to the origin of the metazoans (e.g. Why is there a conflict between molecular clocks and the fossil record in timing the metazoan radiation; were Precambrian metazoan ancestors similar to extant larvae or to miniature adults?) and to diversification of the metazoans (e.g. How do developmental constraints bias the direction of evolution; how do microevolutionary developmental processes relate to macroevolutionary changes?).     

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.     

The evolutionary radiation of modern birds (Neornithes): reconciling molecules, morphology and the fossil record

The pattern, timing and extent of the evolutionary radiation of anatomically modern birds (Neornithes) remains contentious: dramatically different timescales for this major event in vertebrate evolution have been recovered by the 'clock-like' modelling of molecular sequence data and from evidence extracted from the known fossil record. Because current synthesis would lead us to believe that fossil and nonfossil evidence conflict with regard to the neornithine timescale, especially at its base, it is high time that available data are reconciled to determine more exactly the evolutionary radiation of modern birds. In this review we highlight current understanding of the early fossil history of Neornithes in conjunction with available phylogenetic resolution for the major extant clades, as well as recent advancements in genetic methods that have constrained time estimates for major evolutionary divergences. Although the use of molecular approaches for timing the radiation of Neornithes is emphasized, the tenet of this review remains the fossil record of the major neornithine subdivisions and better-preserved taxa. Fossils allowing clear phylogenetic constraint of taxa are central to future work in the production of accurate molecular calibrations of the neornithine evolutionary timescale.  © 2004 The Linnean Society of London, Zoological Journal of the Linnean Society , 2004, 141 , 153–177.     

Early vertebrate evolution

Debate over the origin and evolution of vertebrates has occupied biologists and palaeontologists alike for centuries. This debate has been refined by molecular phylogenetics, which has resolved the place of vertebrates among their invertebrate chordate relatives, and that of chordates among their deuterostome relatives. The origin of vertebrates is characterized by wide‐ranging genomic, embryologic and phenotypic evolutionary change. Analyses based on living lineages suggest dramatic shifts in the tempo of evolutionary change at the origin of vertebrates and gnathostomes, coincident with whole‐genome duplication events. However, the enriched perspective provided by the fossil record demonstrates that these apparent bursts of anatomical evolution and taxic richness are an artefact of the extinction of phylogenetic intermediates whose fossil remains evidence the gradual assembly of crown gnathostome characters in particular. A more refined understanding of the timing, tempo and mode of early vertebrate evolution rests with: (1) better genome assemblies for living cyclostomes; (2) a better understanding of the anatomical characteristics of key fossil groups, especially the anaspids, thelodonts, galeaspids and pituriaspids; (3) tests of the monophyly of traditional groups; and (4) the application of divergence time methods that integrate not just molecular data from living species, but also morphological data and extinct species. The resulting framework will provide for rigorous tests of rates of character evolution and diversification, and of hypotheses of long‐term trends in ecological evolution that themselves suffer for lack of quantitative functional tests. The fossil record has been silent on the nature of the transition from jawless vertebrates to the jawed vertebrates that have dominated communities since the middle Palaeozoic. Elucidation of this most formative of episodes likely rests with the overhaul of early vertebrate systematics that we propose, but perhaps more fundamentally with fossil grades that await discovery.     

Phylogenetic relationships within the class Anthozoa (phylum Cnidaria) based on nuclear 18S rDNA sequences

Taxonomic relationships within the corals and anemones (Phylum Cnidaria: Class Anthozoa) are based upon few morphological characters. The significance of any given character is debatable, and there is little fossil record available for deriving evolutionary relationships. We analyzed complete 18S ribosomal sequences to examine subclass-level and ordinal-level organization within the Anthozoa. We suggest that the Subclass Ceriantipatharia is not an evolutionarily relevant grouping. The Order Corallimorpharia appears paraphyletic and closely related to the Order Scleractinia. The 18S rRNA gene may be insufficient for establishing robust phylogenetic hypotheses concerning the specific relationships of the Corallimorpharia and the Ceriantharia and the branching sequence for the orders within the Hexacorallia. The 18S rRNA gene has sufficient phylogenetic signal, however, to distinguish among the major groupings within the Class Anthozoa, and we use this information to suggest relationships for the enigmatic taxa Dactylanthus and Dendrobrachia.     

Determining climate change impacts on ecosystems: the role of palaeontology

Climate change is projected to change the ecosystems on land and in the sea at rates that are unprecedented for millions of years. The most commonly used approach to derive projections of how ecosystems will look in the future are experiments on living organisms. By their nature, experiments are unlike the real world and cannot capture the ability of organisms to migrate, select and evolve. They are often limited to a select few species and drivers of environmental change and hence cannot represent the complexity of interactions in ‘real’ ecosystems. The fossil record is an archive of responses to climate change at a global ecosystem scale. If, and only if, fossil assemblage variation is combined with independent information of environmental changes, sensitives of species or higher taxa to a specific magnitude of change of an environmental driver can be determined and used to inform future vulnerabilities of this species to the same driver. While records are often fragmented, there are time intervals which, when thoroughly analysed with quantitative data, can provide valuable insights into the future of biodiversity on this planet. This review provides an overview of projected impacts on marine ecosystems including: (1) the range of neontological methods, observations and their challenges; and (2) the complementary information that palaeontologists can contribution to this global challenge. I advocate that, in collaborations with other disciplines, we should aim for a strong visibility of our field and the knowledge it can provide for policy relevant assessments of the future.     

Morphology, fossils, divergence timing, and the phylogenetic relationships of Gavialis

Although morphological data have historically favored a basal position for the Indian gharial (Gavialis gangeticus) within Crocodylia and a Mesozoic divergence between Gavialis and all other crocodylians, several recent molecular data sets have argued for a sister-group relationship between Gavialis and the Indonesian false gharial (Tomistoma schlegelii) and a divergence between them no earlier than the Late Tertiary. Fossils were added to a matrix of 164 discrete morphological characters and subjected to parsimony analysis. When morphology was analyzed alone, Gavialis was the sister taxon of all other extant crocodylians whether or not fossil ingroup taxa were included, and a sister-group relationship between Gavialis and Tomistoma was significantly less parsimonious. In combination with published sequence and restriction site fragment data, Gavialis was the sister taxon of all other living crocodylians, but the position of Tomistoma depended on the inclusion of fossil ingroup taxa; with or without fossils, preferred morphological and molecular topologies were not significantly different. Fossils closer to Gavialis than to Tomistoma can be recognized in the Late Cretaceous, and fossil relatives of Tomistoma are known from the basal Eocene, strongly indicating a divergence long before the Late Tertiary. Comparison of minimum divergence time from the fossil record with different measures of molecular distance indicates evolutionary rate heterogeneity within Crocodylia. Fossils strongly contradict a post-Oligocene divergence between Gavialis and any other living crocodylian, but the phylogenetic placement of Gavialis is best viewed as unresolved.     

Fossil Records in the Lythraceae

The Lythraceae (Myrtales) are a family of 28 genera and ca. 600 species constituting with the Combretaceae and sister family Onagraceae a major lineage of the Myrtales and including the former Sonneratiaceae, Duabangaceae, Punicaceae, and Trapaceae. The fossil record of the family is extensive and significant new discoveries have been added to the record in recent years. This review provides a vetted summary of fossils attributed to the Lythraceae, their geographic distributions, and their stratigraphic ranges. It anticipates the use of the information to generate robustly dated molecular phylogenies to accurately reconstruct the evolutionary and biogeographic history of the family. Fossils of 44 genera or form genera have been attributed to the Lythraceae; 24 are accepted here as lythracean. Fourteen of the 28 modern genera have fossil representatives: Adenaria, Crenea, Cuphea, Decodon, Duabanga, Lafoensia, Lagerstroemia, Lawsonia, Lythrum, Pemphis, Punica, Sonneratia, Trapa, and Woodfordia. Ten extinct genera are recognized. The most common kinds of fossil remains are seeds and pollen. The only fossil flower confidently accepted in the family is the extinct genus Sahnianthus from the Early Paleocene of India. The oldest confirmed evidence of the Lythraceae is pollen of Lythrum/Peplis from the Late Cretaceous (early Campanian, 82?81 Ma) of Wyoming. Seeds of Decodon from the late Campanian (73.5 Ma) of northern Mexico are next oldest. Sonneratia, Lagerstroemia, and extinct Sahnianthus first appear in the Paleocene of the Indian subcontinent; extinct Hemitrapa fruits first occur in the Paleocene of northwestern North America. Diversification of the Lythraceae occurred primarily during two major periods of global temperature change, during the Paleocene-Eocene Thermal Maximum and from the middle Miocene forward when temperatures decreased markedly and seasonality and dry-adapted vegetation types became more prominent. Fossils of the Lythraceae from South America and Africa are limited in number. The few dates available for South American genera are comparatively young and diversification of the largest genus, Cuphea (ca. 240 species), was mainly a Quaternary event. A phylogeny of the family is briefly explored and examples of specialized characters occurring in the oldest known genera are noted. The fossil record of the Lythraceae is presently too fragmentary to confidently reconstruct the early history of the family. The record indicates, however, that the family was well-diversified and widely dispersed globally over a wide latitudinal range by the end of the Paleocene.     

Written in stone: fossils, genes and evo-devo

Fossils give evo-devo a past. They inform phylogenetic trees to show the direction of evolution of developmental features, and they can reveal ancient body plans. Fossils also provide the primary data that are used to date past events, including divergence times needed to estimate molecular clocks, which provide rates of developmental evolution. Fossils can set boundaries for hypotheses that are generated from living developmental systems, and for predictions of ancestral development and morphologies. Finally, although fossils rarely yield data on developmental processes directly, informative examples occur of extraordinary preservation of soft body parts, embryos and genomic information.