Tempo does not correlate with mode in the fossil record

The dominating view of evolution based on the fossil record is that established species remain more or less unaltered during their existence. Substantial evolution is on the other hand routinely reported for contemporary populations, and most quantitative traits show high potential for evolution. These contrasting observations on long‐ and short‐time scales are often referred to as the paradox of stasis, which rests on the fundamental assumption that periods of morphological stasis in the fossil record represent minimal evolutionary change. Investigating 450 fossil time series, I demonstrate that the nonaccumulating morphological fluctuations during stasis travel similar distances in morphospace compared to lineages showing directional change. Hence, lineages showing stasis are commonly undergoing considerable amounts of evolution, but this evolution does not accumulate to produce large net evolutionary changes over time. Rates of evolutionary change across modes in the fossil record may be more homogenous than previously assumed and advocated, supporting the claim that substantial evolution is not exclusively or causally linked to the process of speciation. Instead of exemplifying minimal evolution, stasis likely represents information on the dynamics of the adaptive landscape on macroevolutionary time scales, including the persistence of adaptive zones and ecological niches over millions of years.     

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.     

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.     

The role of Quaternary environmental change in plant macroevolution: the exception or the rule?

The Quaternary has been described as an important time for genetic diversification and speciation. This is based on the premise that Quaternary climatic conditions fostered the isolation of populations and, in some instances, allopatric speciation. However, the 'Quaternary Ice-Age speciation model' rests on two key assumptions: (i) that biotic responses to climate change during the Quaternary were significantly different from those of other periods in Earth's history; and (ii) that the mechanisms of isolation during the Quaternary were sufficient in time and space for genetic diversification to foster speciation. These assumptions are addressed by examining the plant fossil record for the Quaternary (in detail) and for the past 410 Myr, which encompasses previous intervals of icehouse Earth. Our examination of the Quaternary record indicates that floristic responses to climate changes during the past 1.8 Myr were complex and that a distinction has to be made between those plants that were able to withstand the extremes of glacial conditions and those that could not. Generation times are also important as are different growth forms (e.g. herbaceous annuals and arborescent perennials), resulting in different responses in terms of genetic divergence rates during isolation. Because of these variations in the duration of isolation of populations and genomic diversification rates, no canonical statement about the predominant floristic response to climatic changes during the Quaternary (i.e. elevated rates of speciation or extinction, or stasis) is currently possible. This is especially true because of a sampling bias in terms of the fossil record of tree species over that of species with non-arborescent growth forms. Nevertheless, based on the available information, it appears that the dominant response of arborescent species during the Quaternary was extinction rather than speciation or stasis. By contrast, our examination of the fossil record of vascular plants for the past 410 Myr indicates that speciation rates often increased during long intervals of icehouse Earth (spanning up to 50 Myr). Therefore, longer periods of icehouse Earth than those occurring during the Quaternary may have isolated plant populations for sufficiently long periods of time to foster genomic diversification and allopatric speciation. Our results highlight the need for more detailed study of the fossil record in terms of finer temporal and spatial resolution than is currently available to examine the significance of intervals of icehouse Earth. It is equally clear that additional and detailed molecular studies of extant populations of Quaternary species are required in order to determine the extent to which these 'relic' species have genomically diversified across their current populations.     

Extinction, ecological opportunity, and the origins of global snake diversity

Snake diversity varies by at least two orders of magnitude among extant lineages, with numerous groups containing only one or two species, and several young clades exhibiting exceptional richness (>700 taxa). With a phylogeny containing all known families and subfamilies, we find that these patterns cannot be explained by background rates of speciation and extinction. The majority of diversity appears to derive from a radiation within the superfamily Colubroidea, potentially stemming from the colonization of new areas and the evolution of advanced venom-delivery systems. In contrast, negative relationships between clade age, clade size, and diversification rate suggest the potential for possible bias in estimated diversification rates, interpreted by some recent authors as support for ecologically mediated limits on diversity. However, evidence from the fossil record indicates that numerous lineages were far more diverse in the past, and that extinction has had an important impact on extant diversity patterns. Thus, failure to adequately account for extinction appears to prevent both rate- and diversity-limited models from fully characterizing richness dynamics in snakes. We suggest that clade-level extinction may provide a key mechanism for explaining negative or hump-shaped relationships between clade age and diversity, and the prevalence of ancient, species-poor lineages in numerous groups.     

HOW DID LIFE BECOME SO DIVERSE? THE DYNAMICS OF DIVERSIFICATION ACCORDING TO THE FOSSIL RECORD AND MOLECULAR PHYLOGENETICS

Abstract: The long‐term diversification of life probably cannot be modelled as a simple equilibrial process: the time scales are too long, the potential for exploring new ecospace is too large and it is unlikely that ecological controls can act at global scales. The sum of many clade expansions and reductions, each of which happens according to its own dynamic, probably approximates more a damped exponential curve when translated into a global‐scale species diversification curve. Unfortunately, it is not possible to plot such a meaningful global‐scale species diversification curve through time, but curves at higher taxonomic levels have been produced. These curves are subject to the vagaries of the fossil record, but it is unlikely that the sources of error entirely overwhelm the biological signal. Clades radiate when the external and internal conditions are right: a new territory or ecospace becomes available, and the lineage has acquired a number of characters that open up a new diet or mode of life. Modern high levels of diversity in certain speciose clades may depend on such ancient opportunities taken. Dramatic climatic changes through the Quaternary must have driven extinctions and originations, but many species responded simply by moving to more favourable locations. Ecological communities appear to be no more than merely chance associations of species, but there may be real interactions among species. Ironically, high species diversity may lead to more speciation, not, as had been assumed, less: more species create more opportunities and selective pressures for other species to respond to, rather than capping diversity at a fixed equilibrium level. Studies from the scale of modern ecosystems to global long‐term patterns in the fossil record support a model for the exponential diversification of life, and one explanation for a pattern of exponential diversification is that as diversity increases, new forms become ever more refinements of existing forms. In a sense the world becomes increasingly divided into finer niche space. Organisms have a propensity to speciate freely, species richness within ecosystems appears to generate opportunities for more speciation, clades show all kinds of patterns from sluggish speciation rates and constant diversity through time to apparently explosive speciation, and there is no evidence that rapidly speciating clades have reached a limit, nor that they are driving other clades to extinction. A corollary of this view is that current biodiversity must be higher than it has ever been. Limits to infinite growth are clearly local, regional, and global turnover and extinction events, when climate change and physical catastrophes knock out species and whole clades, and push the rising exponential curve down a notch or two.     

Phylogenetic fields through time: temporal dynamics of geographical co-occurrence and phylogenetic structure within species ranges

Species co-occur with different sets of other species across their geographical distribution, which can be either closely or distantly related. Such co-occurrence patterns and their phylogenetic structure within individual species ranges represent what we call the species phylogenetic fields (PFs). These PFs allow investigation of the role of historical processes—speciation, extinction and dispersal—in shaping species co-occurrence patterns, in both extinct and extant species. Here, we investigate PFs of large mammalian species during the last 3 Myr, and how these correlate with trends in diversification rates. Using the fossil record, we evaluate species'' distributional and co-occurrence patterns along with their phylogenetic structure. We apply a novel Bayesian framework on fossil occurrences to estimate diversification rates through time. Our findings highlight the effect of evolutionary processes and past climatic changes on species'' distributions and co-occurrences. From the Late Pliocene to the Recent, mammal species seem to have responded in an individualistic manner to climate changes and diversification dynamics, co-occurring with different sets of species from different lineages across their geographical ranges. These findings stress the difficulty of forecasting potential effects of future climate changes on biodiversity.     

Prolonging the past counteracts the pull of the present: protracted speciation can explain observed slowdowns in diversification

Phylogenetic trees show a remarkable slowdown in the increase of number of lineages towards the present, a phenomenon which cannot be explained by the standard birth-death model of diversification with constant speciation and extinction rates. The birth-death model instead predicts a constant or accelerating increase in the number of lineages, which has been called the pull of the present. The observed slowdown has been attributed to nonconstancy of the speciation and extinction rates due to some form of diversity dependence (i.e., species-level density dependence), but the mechanisms underlying this are still unclear. Here, we propose an alternative explanation based on the simple concept that speciation takes time to complete. We show that this idea of "protracted" speciation can be incorporated in the standard birth-death model of diversification. The protracted birth-death model predicts a realistic slowdown in the rate of increase of number of lineages in the phylogeny and provides a compelling fit to four bird phylogenies with realistic parameter values. Thus, the effect of recognizing the generally accepted fact that speciation is not an instantaneous event is significant; even if it cannot account for all the observed patterns, it certainly contributes substantially and should therefore be incorporated into future studies.     

Continental faunal exchange and the asymmetrical radiation of carnivores

Lineages arriving on islands may undergo explosive evolutionary radiations owing to the wealth of ecological opportunities. Although studies on insular taxa have improved our understanding of macroevolutionary phenomena, we know little about the macroevolutionary dynamics of continental exchanges. Here we study the evolution of eight Carnivora families that have migrated across the Northern Hemisphere to investigate if continental invasions also result in explosive diversification dynamics. We used a Bayesian approach to estimate speciation and extinction rates from a substantial dataset of fossil occurrences while accounting for the incompleteness of the fossil record. Our analyses revealed a strongly asymmetrical pattern in which North American lineages invading Eurasia underwent explosive radiations, whereas lineages invading North America maintained uniform diversification dynamics. These invasions into Eurasia were characterized by high rates of speciation and extinction. The radiation of the arriving lineages in Eurasia coincide with the decline of established lineages or phases of climate change, suggesting differences in the ecological settings between the continents may be responsible for the disparity in diversification dynamics. These results reveal long-term outcomes of biological invasions and show that the importance of explosive radiations in shaping diversity extends beyond insular systems and have significant impact at continental scales.     

EXTINCTION RATES SHOULD NOT BE ESTIMATED FROM MOLECULAR PHYLOGENIES

Molecular phylogenies contain information about the tempo and mode of species diversification through time. Because extinction leaves a characteristic signature in the shape of molecular phylogenetic trees, many studies have used data from extant taxa only to infer extinction rates. This is a promising approach for the large number of taxa for which extinction rates cannot be estimated from the fossil record. Here, I explore the consequences of violating a common assumption made by studies of extinction from phylogenetic data. I show that when diversification rates vary among lineages, simple estimators based on the birth–death process are unable to recover true extinction rates. This is problematic for phylogenetic trees with complete taxon sampling as well as for the simpler case of clades with known age and species richness. Given the ubiquity of variation in diversification rates among lineages and clades, these results suggest that extinction rates should not be estimated in the absence of fossil data.     

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.”     

Nested biological variation and speciation

The modes of speciation that are thought to have contributed most to the generation of biodiversity require population differentiation as the initial stage in the speciation process. Consequently, a complete understanding of the mechanisms of speciation requires that the process be examined not just after speciation is complete, or nearly so, but also much earlier. Because reproductive isolation defines biological species, and it evolves slowly, study of the process may require a prohibitive span of time. Even if speciation could be observed directly, selection of populations in the process of speciation is typically difficult or impossible, because those that will ultimately undergo speciation cannot be distinguished from those that will differentiate but never assume the status of new biological species. One means of circumventing this problem is to study speciation in taxa comprising several sibling species, at least one of which exhibits extensive population differentiation. We illustrate this approach by exploring patterns of population variation in the post-glacial radiation of the threespine stickleback, Gasterosteus aculeatus. We focus on lacustrine populations and species within this complex, demonstrating parallel axes of divergence within populations, among populations and among species. The pattern that emerges is one of parallel relationships between phenotype and fitness at all three hierarchical levels, a pattern that facilitates exploration of the causes and consequences of speciation and secondary contact. A second outcome of this exploration is the observation that speciation can be the consequence of a cascade of effects, beginning with selection on trophic or other characteristics that in turn force the evolution of other population characteristics that precipitate speciation. Neither of these conclusions could have been reached without comparative studies of wild populations at several hierarchical levels, a conclusion reinforced by a brief survey of similar efforts to elucidate the process of speciation. We address the issues most likely to be resolved using this approach, and suggest that comparisons of natural variation within taxa at several hierarchical levels may substantially increase our understanding of the speciation process.     

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.     

Did insect pollination cause increased seed plant diversity?

The dominant paradigm for the disproportionate number of flowering plants is the unique coevolution that they underwent with pollinating insects. The theory underlying this biotic pollination hypothesis contradicts more generally accepted evolutionary theory. Furthermore, various lines of empirical evidence falsify the biotic pollination hypothesis: (a) several lineages of plants were insect pollinated – angiosperms, Gnetales, Bennettitales, Cheiro-lepidiaceae, Medullosales, and Cycadales - yet only the first four were ever diverse or underwent radiations; (b) the predicted rise in insect diversity, which was coupled with angiosperm radiation, does not appear in the fossil record; (c) the family Poaceae (grasses) are wind pollinated, yet are exceptionally diverse and species-rich; and (d) the family Formicidae (ants) were not pollinators, yet are exceptionally species-rich and ecologically dominant. I enumerate many alternate (and seldom investigated) hypotheses for these patterns of seed plant diversity, keeping in mind that although I show that insect pollination was neither a necessary nor sufficient condition for large numbers of species, it may have played a substantial role in both plant and insect speciation. Alternatively, existing theory regarding the biotic pollination hypothesis can be refined in an attempt to eliminate the aforementioned empirical anomalies and theoretical inconsistencies.     

EXTINCTION DURING EVOLUTIONARY RADIATIONS: RECONCILING THE FOSSIL RECORD WITH MOLECULAR PHYLOGENIES

Recent application of time‐varying birth–death models to molecular phylogenies suggests that a decreasing diversification rate can only be observed if there was a decreasing speciation rate coupled with extremely low or no extinction. However, from a paleontological perspective, zero extinction rates during evolutionary radiations seem unlikely. Here, with a more comprehensive set of computer simulations, we show that substantial extinction can occur without erasing the signal of decreasing diversification rate in a molecular phylogeny. We also find, in agreement with the previous work, that a decrease in diversification rate cannot be observed in a molecular phylogeny with an increasing extinction rate alone. Further, we find that the ability to observe decreasing diversification rates in molecular phylogenies is controlled (in part) by the ratio of the initial speciation rate (Lambda) to the extinction rate (Mu) at equilibrium (the LiMe ratio), and not by their absolute values. Here we show in principle, how estimates of initial speciation rates may be calculated using both the fossil record and the shape of lineage through time plots derived from molecular phylogenies. This is important because the fossil record provides more reliable estimates of equilibrium extinction rates than initial speciation rates.     

The evolution of body size in extant groups of North American freshwater fishes: speciation,size distributions,and Cope's rule

Change in body size within an evolutionary lineage over time has been under investigation since the synthesis of Cope's rule, which suggested that there is a tendency for mammals to evolve larger body size. Data from the fossil record have subsequently been examined for several other taxonomic groups to determine whether they also displayed an evolutionary increase in body size. However, we are not aware of any species-level study that has investigated the evolution of body size within an extant continental group. Data acquired from the fossil record and data derived from the evolutionary relationships of extant species are not similar, with each set exhibiting both strengths and weaknesses related to inferring evolutionary patterns. Consequently, expectation that general trends exhibited in the fossil record will correspond to patterns in extant groups is not necessarily warranted. Using phylogenetic relationships of extant species, we show that five of nine families of North American freshwater fishes exhibit an evolutionary trend of decreasing body size. These trends result from the basal position of large species and the more derived position of small species within families. Such trends may be caused by the invasion of small streams and subsequent isolation and speciation. This pattern, potentially influenced by size-biased dispersal rates and the high percentage of small streams in North America, suggests a scenario that could result in the generation of the size-frequency distribution of North American freshwater fishes.     

Gaps in fossil teeth: Saltations or sampling errors?

All evolutionists accept that there are gaps in the fossil record. To some, gaps are data: they mark sudden transitions, unlikely to be preserved, between one species and its descendants that have arisen by a brief genetic revolution within an otherwise stable lineage. However, recent studies of sediment gain and loss show that few fossil beds can be complete enough to give details of the process of speciation, so that most gaps are gaps, and nothing more. Differences in the perception of time and sampling completeness mean that paleontologists and geneticists see the rate and pattern of evolution in different ways. Just how misleading each view may be is seen by analysing the laws of life governing change in living populations using the limitations intrinsic to studies of past times; and by a new insight into the details of species formation now emerging from some remarkably complete primate fossil sequences.     

Developmental bias,macroevolution, and the fossil record

A fuller understanding of the role of developmental bias in shaping large‐scale evolutionary patterns requires integrating bias (the probability distribution of variation accessible to an ancestral phenotype) with clade dynamics (the differential survival and production of species and evolutionary lineages). This synthesis could proceed as a two‐way exchange between the developmental data available to neontologists and the strictly phenotypic but richly historical and dynamic data available to paleontologists. Analyses starting in extant populations could aim to predict macroevolution in the fossil record from observed developmental bias, while analyses starting in the fossil record, particularly the record of extant species and lineages, could aim to predict developmental bias from macroevolutionary patterns, including the broad range of extinct phenotypes. Analyses in multivariate morphospaces are especially effective when coupled with phylogeny, theoretical and developmental models, and diversity–disparity plots. This research program will also require assessing the “heritability” of an ancestral bias across phylogeny, and the tendency for bias change in strength and orientation over evolutionary time. Such analyses will help find a set of general rules for the macroevolutionary effects of developmental bias, including its impact on and interactions with the other intrinsic and extrinsic factors governing the movement, expansion, and contraction of clades in morphospace.     

The demonstration of speciation in fossil molluscs and living fishes

Contrary to a recent assertion, freshwater (and marine) prosobranch gastropods and freshwater bivalves are subject to considerable variability. This, and the lack of a detailed understanding of the taxonomy of the forms involved, makes it difficult to accept that the changes documented by Williamson (1981) in a fossil sequence from Lake Turkana (Africa) represent speciation events. That 10 lineages, involving gastropods and bivalves, should change simultaneously, and the deviant forms should then simultaneously become extinct, can, we believe, be more plausibly attributed to ecophenotypic responses to environmental changes than to speciation. In revealing the pattern and process of evolution, both fossil and living forms are helpful, but in demonstrating the fine-scale events during and after speciation in living animals one can utilize techniques and observations that cannot be applied to fossil material. African cichlid fishes are particularly informative in this respect. Their current explosive radiation can be interpreted as a punctuational event in evolution.     

Parapatric divergence of sympatric morphs in a salamander: incipient speciation on Long Island?

Speciation is often categorized based on geographic modes (allopatric, parapatric or sympatric). Although it is widely accepted that species can arise in allopatry and then later become sympatrically or parapatrically distributed, patterns in the opposite direction are also theoretically possible (e.g. sympatric lineages or ecotypes becoming parapatric), but such patterns have not been shown at a macrogeographic scale. Here, we analyse genetic, climatic, ecological and morphological data and show that two typically sympatric colour morphs of the salamander Plethodon cinereus (redback and leadback) appear to have become parapatrically distributed on Long Island, New York, with pure‐redback populations in the west and pure‐leadback populations in the east (and polymorphic populations in between and on the mainland). In addition, the pure‐leadback populations in eastern Long Island are genetically, ecologically and morphologically divergent from both mainland and other Long Island populations, suggesting the possibility of incipient speciation. This parapatric separation seems to be related to the different ecological preferences of the two morphs, preferences which are present on the mainland and across Long Island. These results potentially support the idea that spatial segregation of sympatric ecotypes may sometimes play an important part in parapatric speciation.