When Earth started blooming: insights from the fossil record

Recent palaeobotanical studies have greatly increased the quantity and quality of information available about the structure and relationships of Cretaceous angiosperms. Discoveries of extremely well preserved Cretaceous flowers have been especially informative and, combined with results from phylogenetic analyses of extant angiosperms (based mainly on molecular sequence data), have greatly clarified important aspects of early angiosperm diversification. Nevertheless, many questions still persist. The phylogenetic origin of the group itself remains as enigmatic as ever and, in some cases, newly introduced techniques from molecular biology have given confusing results. In particular, relationships between the five groups of extant seed plants remain uncertain, and it has sometimes proved difficult to reconcile estimates of the time of divergence between extant lineages made using a 'molecular clock' with the fossil record. One result, however, is becoming increasingly clear: a great deal of angiosperm diversity is extinct. Some groups of angiosperms were evidently more diverse in the past than they are today. In other cases, fossils defy assignment to extant groups at the family level or below. This raises the possibility that evolutionary conclusions based solely upon extant taxa that are merely relics of groups that were once much more diverse might be misled by the effects of extinction. It also introduces the possibility that some early enigmatic fossils might represent lineages that diverged from the main line of angiosperm evolution below the most recent common ancestor of all extant taxa. These, and other questions, are among those that need to be addressed by future palaeobotanical research.     

Lemuriform origins as viewed from the fossil record

Fossils relevant to lemuriform origins are reviewed. Omanodon seems very close to the other early tooth-combed lemuriforms Karanisia, Wadilemur and Saharagalago, whereas Bugtilemur is rejected from the Lemuriformes. The Djebelemurinae, including Djebelemur and 'Anchomomys' milleri, are considered as stem lemuriforms preceding tooth comb differentiation; they are shown to be very distinct from European adapiforms. With tooth-combed lemuriforms present in Africa around 40 million years ago, and stem lemuriforms without tooth combs present on the same continent around 50-48 million years ago, a reasonable scenario can be proposed: tooth comb differentiation and lemuriform dispersal to Madagascar between 52-40 million years ago. The possible significance of Plesiopithecus for daubentoniid origins is raised. A critique of molecular dates is presented in the light of the fossil record. Azibiids are possibly early African prosimians. The timing of the dispersal of primates to Africa and the problem of strepsirhine origins are briefly examined.     

The evolutionary history of Fagus in western Eurasia: Evidence from genes, morphology and the fossil record

 Fagus (beech) is among the most abundant and economically important genera of broad-leaved trees in northern hemisphere temperate forests. The number of modern taxa present in Europe and Asia Minor has long been a matter of debate and up to five species have been recognised. To resolve taxonomic and phylogenetic relationships we conducted morphological and molecular genetic analyses in western Eurasiatic taxa and evaluated palaeontological evidence. To place our findings from western Eurasiatic populations in a broader context additional East Asiatic and North American species of the same subgenus Fagus as well as two species of the subgenus Engleriana were included in our study. The morphological features exhibited in western Eurasiatic populations of Fagus show a west-east gradient that is characterised by strongly overlapping variability between geographical races. Fagus populations from Asia Minor exhibit an even higher variability that is also reflected in their genetic variability of nuclear rDNA internal transcribed spacer (ITS) sequences. The intraspecific genetic variability recorded here is in conflict with previous ITS studies in Fagus. The high amount of ITS polymorphism within Fagus from western Eurasia along with the clinal variation observed for morphological characters suggest the presence of only a single species, Fagus sylvatica L., in Europe and Asia Minor. Previously recognised taxa such as F. orientalis Lipsky and Fagus moesiaca (Maly) Czeczott should therefore be treated as synonyms of Fagus sylvatica. Although species belonging to the subgenus Engleriana were genetically distinct from species of the subgenus Fagus, relationships within the subgenus Fagus could not be clearly resolved. A reason for this could be the low rate of diversification in Fagus during the early phase of range expansion of the genus in the Oligocene period as indicated by the uniformity of leaf and cupule/nut fossils. This may account for the low overall ITS divergence and the high degree of polymorphism encountered in the subgenus Fagus and points to a late differentiation of western Eurasiatic and eastern Asiatic species. Area disruptions during the Pleistocene and the post-glacial recolonisation of western Europe appear to have caused the west-east gradient that is apparent in modern Fagus of western Eurasia but absent in Late Tertiary ancestors of Fagus sylvatica. Received June 22, 2001 Accepted February 25, 2002     

The shape of pterosaur evolution: evidence from the fossil record

Abstract Although pterosaurs are a well‐known lineage of Mesozoic flying reptiles, their fossil record and evolutionary dynamics have never been adequately quantified. On the basis of a comprehensive data set of fossil occurrences correlated with taxon‐specific limb measurements, we show that the geological ages of pterosaur specimens closely approximate hypothesized patterns of phylogenetic divergence. Although the fossil record has expanded greatly in recent years, collectorship still approximates a sigmoid curve over time as many more specimens (and thus taxa) still remain undiscovered, yet our data suggest that the pterosaur fossil record is unbiased by sites of exceptional preservation (lagerstätte). This is because as new species are discovered the number of known formations and sites yielding pterosaur fossils has also increased – this would not be expected if the bulk of the record came from just a few exceptional faunas. Pterosaur morphological diversification is, however, strongly age biased: rarefaction analysis shows that peaks of diversity occur in the Late Jurassic and Early Cretaceous correlated with periods of increased limb disparity. In this respect, pterosaurs appear unique amongst flying vertebrates in that their disparity seems to have peaked relatively late in clade history. Comparative analyses also show that there is little evidence that the evolutionary diversification of pterosaurs was in any way constrained by the appearance and radiation of birds.     

Paleoecology and coalescence: phylogeographic analysis of hypotheses from the fossil record

The application of principles from coalescence theory to genealogical relationships within species can provide insights into the process of diversification and the influence of biogeography on distributional patterns. There are several features that make some organisms more suitable for detailed studies of historical processes; in particular, limited dispersal, which serves to conserve the patterns of genetic variation that developed during colonization. We describe the potential benefits of studies that integrate analyses of genetic variation with information from the fossil pollen record and present recent examples of the application of quantitative methods of phylogeographic analysis.     

Thalloid organisms and the fossil record: New perspectives from the Transantarctic Mountains

Thalloid body plans occur in several groups of organisms, including bryophytes, lichens and algae. While many aspects of the biology and ecology of extant thalloid organisms are well understood today, knowledge about the evolutionary history, palaeobiology and palaeoecology of these life forms remains limited. The recently discovered thalloid fossil Litothallus ganovex from the Triassic of Antarctica consists of fused vertical cell filaments forming a pseudoparenchymatous crust-like body, and most likely represents a freshwater macroalga. Other cuticle fragments from Antarctica are tentatively interpreted as remains of thallose liverworts. These unexpected new finds indicate that thalloid organisms are more frequent in the fossil record than previously assumed, and contribute to a better understanding of the palaeobiodiversity of ancient nonmarine ecosystems.Key words: Litothallus, Hildenbrandia, cuticles, thallus, Triassic, preservation, liverwortsBased on the seemingly simple organization of extant thalloid organisms (e.g., thalloid liverworts, lichens and algae), it has historically been believed that primitive thallophyte communities had colonized the terrestrial realm long before the first appearance of vascular land plants in the Silurian.^1,2 This hypothesis is continuously substantiated by an increasing number of reports of (crypto)spores, phytodebris and biogeochemical signals attributable to thalloid organisms that predate the earliest unequivocal axial land plant fossils by at least 40 million years.^3–7 However, with the exception of marine calcified algae, the macrofossil record of thalloid organisms is meagre throughout Earth history. This is commonly explained by the general absence of sclerified stabilizing and conducting tissues in thalloid bodies that drastically reduces the fossilization potential.We recently published an account on an exceptionally well-preserved non-marine thalloid organism from the Triassic of the Transantarctic Mountains.⁸ This organism, Litothallus ganovex, occurs as compressions of rosette-like thalli (Fig. 1A) with associated cellular sheets (Fig. 1C and D). The exquisite preservation of the fossils enabled a detailed study of the peculiar anatomy of the organism. The thallus of L. ganovex consists of densely spaced, vertical cellular filaments that are laterally fused to form a sheet- or crust-like structure (Fig. 1B). Thalloid bodies containing such pseudotissues only occur in certain algae and lichens. It appears most likely that L. ganovex represents a freshwater macroalga based on its striking resemblance to certain extant freshwater representatives of the red algal order Hildenbrandiales. We speculated that L. ganovex may have been a widespread constituent of certain Triassic freshwater ecosystems that was simply overlooked by earlier workers because of its inconspicuous appearance; Litothallus superficially resembles a coaly film on a sediment bedding plane. Recently we had the opportunity to study the large collection of Mesozoic plant fossils from various localities in Antarctica housed at the Natural History Museum and Biodiversity Research Center of the University of Kansas, Lawrence, KS. It appeared that many slabs with Triassic plant fossils also contain abundant Litothallus specimens, which demonstrates that this organism was in fact more common than we had originally envisaged. In some of the slabs large accumulations of thalli may even form thin coaly layers in the sediment.Open in a separate windowFigure 1The putative freshwater macroalga Litothallus ganovex (A–D) and other recently discovered enigmatic cuticular remains (E–I) from c. 225–195 million-year old sediments of the Transantarctic Mountains. (A) two thalli of L. ganovex. (B) UV epifluorescence-microscopic image of a thallus in cross section showing the (sub)vertical arrangement of cellular files. (C) SEM image of L. ganovex. (D) light-microscopic image of an isolated cellular sheet of L. ganovex. (E) Dorsal cuticle of a yet unidentified organism here interpreted as a liverwort. (F) SEM image of slit-like cavity in the dorsal cuticle surface, lined with papilla-like protrusions. (G) detail of several papilla-like protrusions at the bottom of a cavity, showing surface relief of helical ridges and furrows. (H) detached ventral cuticle showing the orthogonal cell pattern with intercalated pore-bearing cells. (I) detail showing intercalated roundish cells bearing tube-like pores with thickened rims. Scale bars: (A) = 1 cm; (B, D and I) = 50 µm; (E) = 500 µm; (C and F) = 100 µm; (G) = 20 µm; (H) = 200 µm.We have also discovered other enigmatic organic remains of putative thalloid organisms in a similar mode of preservation. For example, bulk macerations of Early Jurassic (c. 195–200 million-year old) sediments from Section Peak in North Victoria Land, Antarctica, have yielded a particularly interesting fossil that consists of a dorsiventally organized cuticle with upper and lower surfaces still in physical association. Neither of the surfaces shows stomata or indications of vein courses. Instead, the upper surface (Fig. 1E) bears slit-like cavities that are lined with large hollow protrusions of the epidermal cells (Fig. 1F). Some of these protrusions possess an interior microrelief of helical ridges and furrows (Fig. 1G). The lower cuticle is comparatively thin and displays an orthogonal pattern of rectangular cells with intercalated roundish cells bearing peculiar tube-like, thick-rimmed pores of about 25 µm diameter (Fig. 1H and I). Remotely similar cuticle-like remains of unknown affinity have been reported from Silurian and Devonian deposits.⁹ Graham et al. have attempted to clarify the identity of these enigmatic Palaeozoic fossils by comparing them with experimentally degraded liverwort thalli.¹⁰ Extant liverworts were therefore subjected to a series of degradation treatments simulating the effects of decay and burial. These treatments produced isolated ventral cuticles with thick-rimmed tubular pores, which represent the remnants of broken-off rhizoids.¹⁰ While the purported similarity between the artificially degraded liverwort remains and the Silurian/Devonian cuticle-like fossils has later been questioned, it is interesting to note that some of the liverwort fragments illustrated by Graham et al. are almost identical to the Jurassic cuticle from Section Peak. At present we can only speculate about the biological affinities of the Section Peak fossil, but we suggest that it may represent a fragment of a thallose liverwort. In this context it is worth to draw attention to the extant liverwort genus Monoclea. In contrast to most other complex thallose liverworts, Monoclea thalli lack air pores and a clearly defined midrib.¹¹ Rhizoids with diameters of 9 to 35 µm are scattered over the entire ventral surface.¹¹ Moreover, Monoclea produces archegonia embedded between mucilage hairs in flask-shaped archegonial cavities on the dorsal side.¹¹ Although highly speculative at present, the slit-like cavities of the Jurassic fossil may have had a similar function. We hope to obtain additional material from Section Peak that permits more detailed analyses and comparisons to further test our hypothesis regarding this highly remarkable Jurassic fossil.The current perception of thalloid organisms in the fossil record remains strongly biased for several reasons. Traditionally, intentional search for fossil thalloid organisms focuses almost exclusively on the Palaeozoic, and aims at resolving the earliest history of plant life on land. Reports on thalloid fossils from younger periods of Earth history are comparatively sporadic and often merely the result of incidental finds. Moreover, impression and compression fossils of thalloid organisms have often been misidentified (e.g., as fern aphlebiae, conifer twigs, arthropod cuticles or trace fossils), and consequently have been grouped together with superficially similar fossils that belong to entirely different organisms.¹² The general scarcity of uncalcified thalloid organisms in the fossil record may therefore to a certain degree also be a result of these strong biases in collecting, identifying and ultimately in studying these often inconspicuous fossils. The search for fossil thalloid organisms, especially from post-Palaeozoic deposits, can greatly contribute to a more accurate reconstruction of the diversity and functioning of ecosystems through time. We hope that our recent discoveries of Litothallus and other wellpreserved, yet enigmatic thalloid fossils provide a stimulus for a reappraisal of this largely disregarded segment of life in the past.     

Inferring social behavior from sexual dimorphism in the fossil record

Sexual dimorphism is commonly used as evidence of the behavior of extinct species. Even so, few analyses scrutinize whether extant comparative data support inferences of mating systems or behavior in extinct species. This analysis evaluates the relations between measures of dimorphism and several estimates of mating system and intrasexual competition. Dimorphism alone provides poor resolution for reconstructing behavior. Many behavioral inferences based on perceived dimorphism are not supported by extant comparative data. This reflects the large standard errors of relations between dimorphism estimates and behavioral classifications. Used with caution, dimorphism can provide a hint of the behavior of extinct species in some cases. However, in many cases inferred dimorphism allows little more than an inference of polygyny, without any indication of specific types of mating systems.     

Amphibian development in the fossil record

Ontogenetic series of extinct taxa are extremely rare and when preserved often incomplete and difficult to interpret. However, the fossil record of amphibians includes a number of well-preserved ontogenetic sequences for temnospondyl and lepospondyl taxa, which have provided valuable information about the development of these extinct groups. Here we summarize the current knowledge on fossil ontogenies of amphibians, their potential and limitations for relationship assessments, and discuss the insights they have provided for our understanding of the anatomy, life history, and ecology of extinct amphibians.     

Cladistics and the hominid fossil record

Cladistic methodology has become common in phylogenetic analyses of the hominid fossil record. Even though it has correctly placed emphasis on morphology for the primary determination of affinities between groups and on explicit statements regarding traits and methods employed in making phylogenetic assessments, cladistics nonetheless has limitations when applied to the hominid fossil record. These include 1) the uncritical assumption of parsimony, 2) uncertainties in the identification of homoplasies, 3) difficulties in the appropriate delimitation of samples for analysis, 4) failure to account for normal patterns of variation, 5) methodological problems with the appropriate identification of morphological traits involving issues of biological relevance, intercorrelation, primary versus secondary characters, and the use of continuous variables, 6) issues of polarity identification, and 7) problems in hypothesis testing. While cladistics has focused attention on alternative phylogenetic reconstructions in hominid paleontology and on explicit statements regarding their morphological and methodological underpinnings, its biological limitations are too abundant for it to be more than a heuristic device for the preliminary ordering of complex human paleontological and neonatological data.     

Myxomycete diversity and distribution from the fossil record to the present

The myxomycetes (plasmodial slime molds or myxogastrids) are a group of eukaryotic microorganisms usually present and sometimes abundant in terrestrial ecosystems. Evidence from molecular studies suggests that the myxomycetes have a significant evolutionary history. However, due to the fragile nature of the fruiting body, fossil records of the group are exceedingly rare. Although most myxomycetes are thought to have very large distributional ranges and many species appear to be cosmopolitan or nearly so, results from recent studies have provided evidence that spatial distribution patterns of these organisms can be successfully related to (1) differences in climate and/or vegetation on a global scale and (2) the ecological differences that exist for particular habitats on a local scale. A detailed examination of the global distribution of four examples (Barbeyella minutissima, Ceratiomyxa morchella, Leocarpus fragilis and Protophysarum phloiogenum) demonstrates that these species have recognizable distribution patterns in spite of the theoretical ability of their spores to bridge continents. Special Issue: Protist diversity and geographic distribution. Guest editor: W. Foissner.     

Phylogeny of Schisandraceae based on morphological data: evidence from modern plants and the fossil record

Schisandraceae are traditionally subdivided in two genera, Schisandra and Kadsura, based on differences in the organisation of the floral receptacle, the carpels, and the presence or absence of a ``pseudostigma'. Recently, phylogenetic analyses utilizing ITS sequence data and morphological data resulted in incongruent tree topologies, with the morphological trees suggesting monophyly of the two genera, whereas ITS trees did not resolve Schisandra and Kadsura as monophyletic clades. In the present paper we study seed morphology and leaf epidermal features of 22 species of Schisandraceae in order to provide additional data for a morphological data matrix. Seed morphological characters are highly homoplastic and do not yield further evidence for monophyly of the two genera. Instead, a number of characters appear to support sister group relationships between taxa within the genera, such as, for instance, for K. coccinea and K. scandens, both of which have large seeds along with a multi-layered mesotesta. Considering leaf epidermal characteristics, species of Kadsura were found to be consistently amphistomatic, whereas species of Schisandra are always hypostomatic. Phylogenetic analysis using the extended data matrix resulted in weakly supported Kadsura and Schisandra clades with five and four synapomorphies indicating monophyly of Kadsura and Schisandra, respectively. Fossils ascribed to Schisandraceae date back to the Late Cretaceous. These are tri-and hexacolpate pollen types displaying a combination of features found in modern Schisandraceae and partly also in Illiciaceae. Leaf remains from this period are poorly preserved and difficult to ascribe to Schisandraceae because of the lack of synapomorphies for the family. In the Early Cainozoic, leaf and seed remains from North America and Europe unambiguously belong to the family. Seeds from the Eocene of North America show some similarities to the modern Schisandra glabra from North America, while fossils from Europe show more similarities to modern Asian species.     

Atomism, transformism and the fossil record

The modern debate between exponents of classical evolutionary classification and of cladistic analysis of phylogenetic relationships mirrors to some extent the arguments that were put forward in the debate between Cuvier and Geoffroy Saint-Hilaire in 1830. Put into a historical perspective the problems of comparative biology centre around two complementary traditions, atomism and transformism.     

Coupled evolutionary rates and the fossil record

A model for speciation is given in which a taxon’s phenotypic variation and concomitant variation in fitness are related to gradients within the environment. Phenotypic expressions within the population are shown to undergo abrupt transitions as a result of discontinuous fitness-functions. Evidence for rapid and abrupt phenotypic variation is explored by analyses of speciation (= origination) rates within the fossil record. In general, a high correlation exists among the area/volume changes of sedimentary rocks known for each geologic period and the apparent speciation rates seen in selected vascular/non-vascular plant groups. Regressions of speciation rates on rock area/volume plots indicate that the Devonian, Carboniferous, and Permian show significant divergences (= residual) rates from predicted origination rates. The Cretaceous shows the highest residual value as a consequence of the rapid appearance of angiosperm fossils. A similar pattern in diversity changes for the mandibulate terrestrial invertebrates is also apparent. The coupled evolution of the angiosperms with specific insect groups appears to be the most tenable explanation for the residual Cretaceous origination rate of the former group. It is postulated that the angiospems have evolved in part as the result of a phytochemical cost-function such that phytophagous insects are warded off, while potential pollinators are favored. Quantitative/qualitative differences observed in the distribution of secondary metabolites may be evidence for coupled evolution. A “predatorprey mediated co-existence” between phytophagous insects and angiosperms may have served as a factor in allowing the co-existence of less than optimal plant species providing an impetus for relatively rapid speciation turnover.     

Rates of speciation in the fossil record

Data from palaeontology and biodiversity suggest that the global biota should produce an average of three new species per year. However, the fossil record shows large variation around this mean. Rates of origination have declined through the Phanerozoic. This appears to have been largely a function of sorting among higher taxa (especially classes), which exhibit characteristic rates of speciation (and extinction) that differ among them by nearly an order of magnitude. Secular decline of origination rates is hardly constant, however; many positive deviations reflect accelerated speciation during rebounds from mass extinctions. There has also been general decline in rates of speciation within major taxa through their histories, although rates have tended to remain higher among members in tropical regions. Finally, pulses of speciation appear sometimes to be associated with climate change, although moderate oscillations of climate do not necessarily promote speciation despite forcing changes in species' geographical ranges.     

Glutoxylon Chowdhury (Anacardiaceae): the first record of fossil wood from Bangladesh

This paper documents the first record of silicified fossil wood from a previously undescribed wood-rich horizon in the Sitakund Anticline, Eastern Bangladesh. The outcrop is composed of cross-stratified, fine-medium grained sandstones with bidirectional cross stratification indicative of a tidal environment, deposited ca. 5-5.2 million years before present (Miocene/Pliocene). The wood is characterised by large solitary vessels with alternate intervascular pits, banded parenchyma, uniseriate rays, and multiseriate rays with one radial canal per ray. This character combination closely resembles the wood of extant Gluta L. of the Anacardiaceae. This specimen has been assigned to the organ genus Glutoxylon Chowdhury erected for fossil woods with anatomical similarity to Gluta (including Melanorrhoea Wall.). The excellent preservation of this mature wood specimen illustrates the potential for using fossil wood from the Sitakund locality for palaeoecological studies in terms of biodiversity and adaptational response to climate change. Moreover such investigations of fossil woods from Bangladesh will compliment studies undertaken on fossil plants in other parts of Central and Southeastern Asia which will further the understanding of plant migration routes between India and Southeast Asia during the Tertiary.     

Patterns of heterochrony in the fossil record

Recent analyses of the fossil record have revealed that heterochrony has played a significant role in the evolution of most marine invertebrate groups. Recognition of several different heterochronic processes has allowed their influence under different ecological regimes to be assessed. Furthermore, recent research has demonstrated significant differences in frequencies of these processes between groups and at their different stages of phylogenetic development. The fossil record shows that heterochron y has been an important component in the generation of evolutionary trends. Heterochrony is an important factor in macroevolution because it can result in relatively abrupt morphological change with only minimum alteration of the genome.     

First Quaternary fossil record of Polyplacophorans from southern South America

A diverse assemblages of well-preserved polyplacophoran shell plates is present in Holocene marine deposits along the Beagle Channel, Tierra del Fuego (54°S). They represent the first fossil Quaternary report of polyplacophorans from southern South America. The taxa include Callochiton puniceus (Couthouy MS, Gould), Plaxiphora aurata (Spalowsky), Plaxiphora sp., Tonicia atrata (Sowerby), Tonicia calbucensis Plate, Tonicia chilensis (Frembly), and Tonicia lebruni de Rochebrune. The presence of these taxa in a transitory area between the Atlantic and the Pacific oceans suggests that, in the recent past, the Beagle Channel acted as a path that facilitated faunal dispersion between the two oceans. These records also show an apparent stability of these faunas over a period of several thousand years (from ca. 7500 years BP to present).