Amber microfossils: On the validity of species concept

Do terrestrial micro-organisms evolve morphologically? A recent concept suggests that morphological stasis over dozens of millions of years has persisted in microbial lineages. However, it is based on a weak fossil record. Indeed, it is already difficult to define a species with extant microbes, and this task is even harder when dealing with fossil micro-organisms. Based on research on fossils in amber, we highlighted the different problems that are raised when describing a new fossil species of micro-organisms and we discuss the concept of morphological stasis.     

Evidence of constrained phenotypic evolution in a cryptic species complex of agamid lizards

Lineages that exhibit little morphological change over time provide a unique opportunity to explore whether nonadaptive or adaptive processes explain the conservation of morphology over evolutionary time scales. We provide the most comprehensive evaluation to date of the evolutionary processes leading to morphological similarity among species in a cryptic species complex, incorporating two agamid lizard species (Diporiphora magna and D. bilineata). Phylogenetic analysis of mitochondrial (ND2) and nuclear (RAG-1) gene regions revealed the existence of eight deeply divergent clades. Analysis of morphological data confirmed the presence of cryptic species among these clades. Alternative evolutionary hypotheses for the morphological similarity of species were tested using a combination of phylogenetic, morphological, and ecological data. Likelihood model testing of morphological data suggested a history of constrained phenotypic evolution where lineages have a tendency to return to their medial state, whereas ecological data showed support for both Brownian motion and constrained evolution. Thus, there was an overriding signature of constrained evolution influencing morphological divergence between clades. Our study illustrates the utility of using a combination of phylogenetic, morphological, and ecological data to investigate evolutionary mechanisms maintaining cryptic species.     

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.     

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.     

Stasis of functionally versatile specialists

A classic hypothesis posits that lineages exhibiting long-term stasis are broadly adapted generalists that remain well-adapted despite environmental change. However, lacking constraints that steepen adaptive peaks and stabilize the optimum, generalists’ phenotypes might drift around a broad adaptive plateau. We propose that stasis would be likely for morphological specialists that behave as ecological generalists much of the time because specialists’ functional constraints stabilize the optimum, but those with a broad niche, such as generalists, can persist despite environmental change. Tree squirrels (Callosciurinae and Sciurini) exemplify ecologically versatile specialists, being extreme in adaptations for forceful biting that expand rather than limit niche breadth. Here, we examine the structure of disparity and the evolutionary dynamics of their trophic morphology (mandible size and shape) to determine if they exhibit stasis. In both lineages, a few dietary specialists disproportionately account for disparity; excluding them, we find compelling evidence for stasis of jaw shape but not size. The primary optima of these lineages diverge little, if at all over approximately 30 million years. Once their trophic apparatus was assembled, their morphological specialization steepened the slopes of their adaptive peak and constrained the position of the optima without limiting niche breadth.     

Evolution in fossil lineages: paleontology and The Origin of Species

Of all of the sources of evidence for evolution by natural selection, perhaps the most problematic for Darwin was the geological record of organic change. In response to the absence of species-level transformations in the fossil record, Darwin argued that the fossil record was too incomplete, too biased, and too poorly known to provide strong evidence against his theory. Here, this view of the fossil record is evaluated in light of 150 years of subsequent paleontological research. Although Darwin's assessment of the completeness and resolution of fossiliferous rocks was in several ways astute, today the fossil record is much better explored, documented, and understood than it was in 1859. In particular, a reasonably large set of studies tracing evolutionary trajectories within species can now be brought to bear on Darwin's expectation of gradual change driven by natural selection. An unusually high-resolution sequence of stickleback-bearing strata records the transformation of this lineage via natural selection. This adaptive trajectory is qualitatively consistent with Darwin's prediction, but it occurred much more rapidly than he would have guessed: almost all of the directional change was completed within 1,000 generations. In most geological sequences, this change would be too rapid to resolve. The accumulated fossil record at more typical paleontological scales (10(4)-10(6) years) reveals evolutionary changes that are rarely directional and net rates of change that are perhaps surprisingly slow, two findings that are in agreement with the punctuated-equilibrium model. Finally, Darwin's view of the broader history of life is reviewed briefly, with a focus on competition-mediated extinction and recent paleontological and phylogenetic attempts to assess diversity dependence in evolutionary dynamics.     

EARLY BURSTS OF BODY SIZE AND SHAPE EVOLUTION ARE RARE IN COMPARATIVE DATA

George Gaylord Simpson famously postulated that much of life's diversity originated as adaptive radiations—more or less simultaneous divergences of numerous lines from a single ancestral adaptive type. However, identifying adaptive radiations has proven difficult due to a lack of broad‐scale comparative datasets. Here, we use phylogenetic comparative data on body size and shape in a diversity of animal clades to test a key model of adaptive radiation, in which initially rapid morphological evolution is followed by relative stasis. We compared the fit of this model to both single selective peak and random walk models. We found little support for the early‐burst model of adaptive radiation, whereas both other models, particularly that of selective peaks, were commonly supported. In addition, we found that the net rate of morphological evolution varied inversely with clade age. The youngest clades appear to evolve most rapidly because long‐term change typically does not attain the amount of divergence predicted from rates measured over short time scales. Across our entire analysis, the dominant pattern was one of constraints shaping evolution continually through time rather than rapid evolution followed by stasis. We suggest that the classical model of adaptive radiation, where morphological evolution is initially rapid and slows through time, may be rare in comparative data.     

Speciation in the fossil record

It is easy to claim that the fossil record says nothing about speciation because the biological species concept (which relies on interbreeding) cannot be applied to it and genetic studies cannot be carried out on it. However, fossilized organisms are often preserved in sufficient abundance for populations of intergrading morphs to be recognized, which, by analogy with modern populations, are probably biological species. Moreover, the fossil record is our only reliable documentation of the sequence of past events over long time intervals: the processes of speciation are generally too slow to be observed directly, and permanent reproductive isolation can only be verified with hindsight. Recent work has shown that some parts of the fossil record are astonishingly complete and well documented, and patterns of lineage splitting can be examined in detail. Marine plankton appear to show gradual speciation, with subsequent morphological differentiation of lineages taking up to 500000 years to occur. Marine invertebrates and vertebrates more commonly show punctuated patterns, with periods of rapid speciation followed by long-term stasis of species lineages.     

Speciation and Bursts of Evolution

A longstanding debate in evolutionary biology concerns whether species diverge gradually through time or by rapid punctuational bursts at the time of speciation. The theory of punctuated equilibrium states that evolutionary change is characterised by short periods of rapid evolution followed by longer periods of stasis in which no change occurs. Despite years of work seeking evidence for punctuational change in the fossil record, the theory remains contentious. Further there is little consensus as to the size of the contribution of punctuational changes to overall evolutionary divergence. Here we review recent developments which show that punctuational evolution is common and widespread in gene sequence data.     

Paleontological Patterns, Macroecological Dynamics and the Evolutionary Process

Here we consider evolutionary patterns writ large in the fossil record. We argue that Darwin recognized but downgraded or de-emphasized several of these important patterns, and we consider what a renewed emphasis on these patterns can tell us about the evolutionary process. In particular, one of the key patterns we focus on is the role geographic isolation plays in fomenting evolutionary divergence; another one of the key patterns is stasis of species; the final pattern is turnovers, which exist at several hierarchical scales, including regional ecosystem replacement and pulses of speciation and extinction. We consider how each one of these patterns are related to the dynamic of changing ecological and environmental conditions over time and also investigate their significance in light of other concepts including punctuated equilibria and hierarchy theory. Ultimately, we tie each of these patterns into a framework involving macroecological dynamics and the important role environmental change plays in shaping evolution from the micro- to macroscale.     

Confrontation of morphological and molecular data: the Praomys group (Rodentia, Murinae) as a case of adaptive convergences and morphological stasis

Phylogenetic relationships in a group of 21 African rodent species designated as the Praomys group (Murinae) were investigated using morphological characters and sequence data from the complete mitochondrial cytochrome b gene and nuclear IRBP gene fragment (840bp). The molecular results confirm the monophyly of the Praomys group, including the species Malacomys verschureni, while the other Malacomys species appear very divergent. The basal relationships within the Praomys group are poorly resolved, suggesting a rapid radiation at about 7-9 million years ago based on genetic divergence rates calibrated from the fossil record. Discrepancies between molecular and morphological results probably reflect of numerous convergences as well as variations in the rates of morphological evolution among lineages. Reconstructions of the ancestral character states suggest a savannah origin for the Praomys group, along with some morphological traits conserved by stasis in savannah taxa. At the same time, forest taxa seem to be characterized by an accelerated morphological evolution, with acquisition of convergent adaptive characters.     

Using ecological niche modelling to evaluate niche stability in deep time

Aim To investigate relative niche stability in species responses to various types of environmental pressure (biotic and abiotic) on geological time‐scales using the fossil record. Location The case study focuses on Late Ordovician articulate brachiopods of the Cincinnati Arch in eastern North America. Methods Species niches were modelled for a suite of fossil brachiopod species based on five environmental variables inferred from sedimentary parameters using GARP and Maxent . Niche stability was assessed by comparison of (1) the degree of overlap of species distribution models developed for a time‐slice and those generated by projecting niche models of the previous time‐slice onto environmental layers of a second time‐slice using GARP and Maxent , (2) Schoener’s D statistic, and (3) the similarity of the contribution of each environmental parameter within Maxent niche models between adjacent time‐slices. Results Late Ordovician brachiopod species conserved their niches with high fidelity during intervals of gradual environmental change but responded to inter‐basinal species invasions through niche evolution. Both native and invasive species exhibited similar levels of niche evolution in the invasion and post‐invasion intervals. Niche evolution was related mostly to decreased variance within the former ecological niche parameters rather than to shifts to new ecospace. Main conclusions Although the species examined exhibited morphological stasis during the study interval, high levels of niche conservatism were observed only during intervals of gradual environmental change. Rapid environmental change, notably inter‐basinal species invasions, resulted in high levels of niche evolution among the focal taxa. Both native and invasive species responded with similar levels of niche evolution during the invasion interval and subsequent environmental reorganization. The assumption of complete niche conservatism frequently employed in ecological niche modelling (ENM) analyses to forecast or hindcast species geographical distributions is more likely to be accurate for climate change studies than for invasive species analyses over geological time‐scales.     

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. I. RATE TESTS FOR RANDOM CHANGE VERSUS SELECTION IN DIFFERENTIATION OF LIVING SPECIES

The possible roles of random genetic change and natural selection in bryozoan speciation were analyzed using quantitative genetic methods on breeding data for traits of skeletal morphology in two closely related species of the cheilostome Stylopoma. The hypothesis that morphologic differences between the species are caused entirely by mutation and genetic drift could not be rejected for reasonable rates of mutation maintained for as few as 10³ to 10⁴ generations. Divergence times this short or shorter are consistent with the abrupt appearances of many invertebrate species in the fossil record, commonly followed by millions of years of morphologic stasis. To produce these differences over 10³ generations or fewer, directional selection acting alone would require unrealistically high levels of minimum selective mortality throughout divergence. Thus, selection is unnecessary to explain the divergence of these species, except as a means of accelerating the effects of random genetic change on shorter time scales (directional selection), or decelerating them over longer ones (stabilizing selection). These results are consistent with a variety of models of phenotypic evolution involving random shifts between multiple adaptive peaks. Similar results were obtained by substituting trait heritabilities and genetic covariances reconstructed by partitioning within- and among-colony phenotypic variance in place of the values based on breeding data. Quantitative genetic analysis of speciation in fossil bryozoan lineages is thus justified.     

Simplification as a trend in synapsid cranial evolution

The prevalence and meaning of morphological trends in the fossil record have undergone renewed scrutiny in recent years. Studies have typically focused on trends in body size evolution, which have yielded conflicting results, and have only rarely addressed the question as to whether other morphological characteristics show persistent directionality over long time scales. I investigated reduction in number of skull and lower jaw bones (through loss or fusion) over approximately 150 million years of premammalian synapsid history. The results of a new skull simplification metric (SSM), which is defined as a function of the number of distinct elements, show that pronounced simplification is evident on both temporal (i.e., stratigraphic) and phylogenetic scales. Postcranial evolution exhibits a similar pattern. Skull size, in contrast, bears little relationship with the number of distinct skull bones present. Synapsid skulls carried close to their observed maximum number of elements for most of the Late Carboniferous and Early Permian. The SSM decreased in the Late Permian but, coincident with the radiation of early therapsids, the range of observed SSM values widened during this interval. From derived nonmammalian cynodonts in the Early Triassic through the earliest mammals in the Early Jurassic, both the minimum and maximum SSM decreased. Data from three representative modern mammals (platypus, opossum, and human) suggest that this trend continues through the Cenozoic. In a phylogenetic context, the number of skull elements present in a taxon shows a significant negative relationship with the number of branching events passed from the root of the tree; more deeply embedded taxa have smaller SSM scores. This relationship holds for various synapsid subgroups as well. Although commonly ascribed to the effects of long-term selection, evolutionary trends can alternatively reflect an underlying intrinsic bias in morphological change. In the case of synapsid skull bones (and those of some other tetrapods lineages), the rare production of novel, or neomorphic, elements may have contributed to the observed trend toward skeletal simplification.     

Évolution « graduelle » à l’échelle géologique chez les rongeurs fossiles du Cénozoïque européen

Cases of gradualism in rodent evolution during the Cainozoic in Europe. Since several decades, conflicting interpretations of the fossil record are well known when the latter is used to understand mechanisms and modes of biological evolution. Once recalled peculiarities of the paleontological material and approach, several cases studies conducted by teams of the laboratory of Montpellier are presented. It clearly appears that Theridomyidae, Gliridae and Murinae rodents illustrate gradual evolution at the geological time scale. At the same time scale, these groups do not give obvious examples of stasis. The understanding in terms of mechanisms of morphological evolution illustrated by fossils will remain a long running debate. And this despite consideration of the time scales involved in Earth History on the one hand, and in Biology and Ecology on the other hand, as well as of the gap between morphological change in individuals and genetic change within populations. To cite this article: M. Vianey-Liaud, J. Michaux, C. R. Palevol 2 (2003).     

Eutherians experienced elevated evolutionary rates in the immediate aftermath of the Cretaceous–Palaeogene mass extinction

The effect of the Cretaceous–Palaeogene (K–Pg) mass extinction on the evolution of many groups, including placental mammals, has been hotly debated. The fossil record suggests a sudden adaptive radiation of placentals immediately after the event, but several recent quantitative analyses have reconstructed no significant increase in either clade origination rates or rates of character evolution in the Palaeocene. Here we use stochastic methods to date a recent phylogenetic analysis of Cretaceous and Palaeocene mammals and show that Placentalia likely originated in the Late Cretaceous, but that most intraordinal diversification occurred during the earliest Palaeocene. This analysis reconstructs fewer than 10 placental mammal lineages crossing the K–Pg boundary. Moreover, we show that rates of morphological evolution in the 5 Myr interval immediately after the K–Pg mass extinction are three times higher than background rates during the Cretaceous. These results suggest that the K–Pg mass extinction had a marked impact on placental mammal diversification, supporting the view that an evolutionary radiation occurred as placental lineages invaded new ecological niches during the Early Palaeocene.     

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.”     

Evolution and development of the primate limb skeleton

The order Primates is composed of many closely related lineages, each having a relatively well established phylogeny supported by both the fossil record and molecular data. 1 Primate evolution is characterized by a series of adaptive radiations beginning early in the Cenozoic era. Studies of these radiations have uncovered two major trends. One is that substantial amounts of morphological diversity have been produced over short periods of evolutionary time. 2 The other is that consistent and repeated patterns (variational tendencies 3 ) are detected. Taxa within clades, such as the strepsirrhines of Madagascar and the platyrrhines of the Neotropics, have diversified in body size, substrate preference, and diet. 2 , 4 - 6 The diversification of adaptive strategies within such clades is accompanied by repeated patterns of change in cheiridial proportions 7 , 8 (Fig. 1) and tooth‐cusp morphology. 9 There are obvious adaptive, natural‐selection based explanations for these patterns. The hands and feet are in direct contact with a substrate, so their form would be expected to reflect substrate preference, whereas tooth shape is related directly to the functional demands of masticating foods having different mechanical properties. What remains unclear, however, is the role of developmental and genetic processes that underlie the evolutionary diversity of the primate body plan. Are variational tendencies a signature of constraints in developmental pathways? What is the genetic basis for similar morphological transformations among closely related species? These are a sampling of the types of questions we believe can be addressed by future research integrating evidence from paleontology, comparative morphology, and developmental genetics.     

Bird evolution in the Eocene: climate change in Europe and a Danish fossil fauna

The pattern of the evolutionary radiation of modern birds (Neornithes) has been debated for more than 10 years. However, the early fossil record of birds from the Paleogene, in particular, the Lower Eocene, has only recently begun to be used in a phylogenetic context to address the dynamics of this major vertebrate radiation. The Cretaceous-Paleogene (K-P) extinction event dominates our understanding of early modern bird evolution, but climate change throughout the Eocene is known to have also played a major role. The Paleocene and Lower Eocene was a time of avian diversification as a result of favourable global climatic conditions. Deteriorations in climate beginning in the Middle Eocene appear to be responsible for the demise of previously widespread avian lineages like Lithornithiformes and Gastornithidae. Other groups, such as Galliformes display replacement of some lineages by others, probably related to adaptations to a drier climate. Finally, the combination of slowly deteriorating climatic conditions from the Middle Eocene onwards, appears to have slowed the evolutionary rate in Europe, as avian faunas did not differentiate markedly until the Oligocene. Taking biotic factors in tandem with the known Paleogene fossil record of Neornithes has recently begun to illuminate this evolutionary event. Well-preserved fossil taxa are required in combination with ever-improving phylogenetic hypotheses for the inter-relationships of modern birds founded on morphological characters. One key avifauna of this age, synthesised for the first time herein, is the Lower Eocene Fur Formation of Denmark. The Fur birds represent some of the best preserved (often in three dimensions and with soft tissues) known fossil records for major clades of modern birds. Clear phylogenetic assessment of these fossils will prove critical for future calibration of the neornithine evolutionary timescale. Some early diverging clades were clearly present in the Paleocene as evidenced directly by new fossil material alongside the phylogenetically constrained Lower Eocene taxa. A later Oligocene radiation of clades other than Passeriformes is not supported by available fossil data.     

There's something afoot in the evolution of ontogenies

Allometry, the association between size and shape, has long been considered an evolutionary constraint because of its ability to channel variation in particular directions in response to evolution of size. Several recent studies, however, have demonstrated that allometries themselves can evolve. Therefore, constraints based on these allometries are not constant over long evolutionary time scales. The changes in ontogeny appear to have a clear adaptive basis, which establishes a feedback loop from adaptive change of ontogeny through the altered developmental constraints to the potential for further evolutionary change. Altogether, therefore, this new evidence underscores the tight interactions between developmental and ecological factors in the evolution of morphological traits.