Fossils,phylogenies, and the challenge of preserving evolutionary history in the face of anthropogenic extinctions

Anthropogenic impacts are endangering many long-lived species and lineages, possibly leading to a disproportionate loss of existing evolutionary history (EH) in the future. However, surprisingly little is known about the loss of EH during major extinctions in the geological past, and thus we do not know whether human impacts are pruning the tree of life in a manner that is unique in the history of life. A major impediment to comparing the loss of EH during past and current extinctions is the conceptual difference in how ages are estimated from paleontological data versus molecular phylogenies. In the former case the age of a taxon is its entire stratigraphic range, regardless of how many daughter taxa it may have produced; for the latter it is the time to the most recent common ancestor shared with another extant taxon. To explore this issue, we use simulations to understand how the loss of EH is manifested in the two data types. We also present empirical analyses of the marine bivalve clade Pectinidae (scallops) during a major Plio–Pleistocene extinction in California that involved a preferential loss of younger species. Overall, our results show that the conceptual difference in how ages are estimated from the stratigraphic record versus molecular phylogenies does not preclude comparisons of age selectivities of past and present extinctions. Such comparisons not only provide fundamental insights into the nature of the extinction process but should also help improve evolutionarily informed models of conservation prioritization.Extinction of any species or higher taxon invariably results in some loss of existing evolutionary history (EH), but a major concern about extinctions driven by anthropogenic impacts is that they may remove a disproportionately large amount of such history (1–3). In groups as varied as birds, mammals, and plants, studies have shown that extinctions of species currently on the International Union for the Conservation of Nature Red List of Threatened Species would lead to a much larger loss of EH than expected under randomly distributed extinction of the same number of species (4–6). This disproportionate loss of EH stems from phylogenetic clustering of anthropogenic extinctions (1) with a bias toward the loss of species-poor and geologically old taxa (7–9). Such predictions, along with the realization that not all species currently threatened by human activities can be saved, have motivated the development of various strategies for minimizing the loss of EH (8, 10, 11). These approaches primarily target lineages that are old but species poor in an attempt to protect large amounts of EH and, presumably, also unique traits and functions that may affect future evolutionary potential (10, 12).Although the disproportionate loss of EH caused by anthropogenic extinctions is increasingly evident, surprisingly little is known about the loss of EH during extinctions in the geological past. The rich archive of extinctions preserved in the fossil record has been the main source of insights about the nature of the extinction process (13–15), and it provides the baseline against which the magnitude of the current crisis has been measured (16). Comparisons of ecological and biogeographic components of past and present extinctions also hold great potential for predicting the nature of future losses (17, 18). Although paleontological studies have tested for age-related bias in extinction vulnerability (19–22), such analyses have focused primarily on background extinctions rather than on selectivity across major extinction events (23). However, without a better understanding of patterns of loss of EH during major pulsed extinctions in the geological past, we cannot answer the fundamental question of whether we, as a species, are pruning the tree of life in a unique manner. Such an understanding requires developing a comparative framework that includes both paleontological and neontological data.A major impediment to comparing anthropogenic impacts on EH with those during past extinctions is that the methods used in each case differ. Analyses of future losses caused by anthropogenic extinctions primarily have used tree-based measures of EH (24, but see ref. 25) that are not easily applicable to extinct taxa for which large phylogenies are still lacking. More importantly, even when phylogenies of extinct taxa are available, the differences in the nature of paleontological and molecular phylogenies complicate direct comparisons. In paleontological phylogenies, a species maintains its identity over time as long as its traits remain relatively constant. This property allows “budding cladogenesis” in which a parent species remains unaffected while giving rise to a daughter (Fig. 1) (26, 27). In contrast, molecular (or cladistic) phylogenies allow only “bifurcating cladogenesis” in which the parent lineage is replaced by two daughters (or more daughters in the case of multifurcation), even for speciation events that were, in fact, budding (Fig. 1) (26). Thus, the discrepancy between the stratigraphic and cladistic representations depends on the frequency of budding versus bifurcating speciation, which remains unknown at present despite well-documented cases of budding cladogenesis in the fossil record (26–28).Open in a separate windowFig. 1.A simple tree showing how the full branching history of a clade can be reduced to either stratigraphic ranges or a bifurcating phylogeny. A clade undergoes speciation (assumed here to be budding, with survival of the parent) and extinction, with nine lineages (A–I) surviving to the focal time (t = 0). The stratigraphic range and absolute age of each surviving species are determined by the time of its first appearance in the fossil record, without reference to species relationships. The bifurcating phylogeny is determined by the divergence times of surviving species relative to one another, without regard for their original times of speciation. Colors illustrate the four scenarios of age-dependent extinction at the focal time. Note that the oldest species differ—in both identity and age—between the absolute and relative age definitions, as do the youngest species. Thus, stratigraphic and phylogenetic diversity are differently affected by the loss of species.Whether cladogenesis is viewed as budding or bifurcating has important consequences for assessing what the “age” of a species is and consequently for analyses of age selectivities as well as other aspects of evolutionary dynamics (29). For budding cladogenesis, the age of a taxon is its entire stratigraphic range (hereafter absolute age) regardless of daughter taxa it may have produced, whereas for bifurcating cladogenesis the age of the taxon is the time to the most recent common ancestor shared with another extant taxon (hereafter relative age) (Fig. 1) (26, 29). Comparing paleontological insights about evolutionary dynamics with those inferred from molecular phylogenies requires us to understand better the consequences of this difference for empirical analyses. For the question addressed here, the age definition used will affect empirical tests of age selectivity during extinctions. It also will affect simulation tests, such as when choosing taxa for removal during an age-biased extinction event (Fig. 1). We emphasize, however, that these two age definitions are simply different conceptualizations of a given biological history. Extinction selectivity is expected to be based on traits (e.g., geographic range, body size) rather than on age per se, so any signal of age-dependent extinction more likely reflects its relationship to other traits.Our goal here is to understand how the loss of EH is manifested in budding versus bifurcating phylogenies. We start with simulations to illustrate how a given extinction event erodes EH on each of these types of phylogenies. We then explore this issue empirically using a phylogeny of living and extinct marine scallops (Pectinidae) that experienced elevated extinction during the Plio–Pleistocene transition (30).     

Comprehensive phylogeny of apid bees reveals the evolutionary origins and antiquity of cleptoparasitism

Apidae is the most speciose and behaviorally diverse family of bees. It includes solitary, eusocial, socially parasitic, and an exceptionally high proportion of cleptoparasitic species. Cleptoparasitic bees, which are brood parasites in the nests of other bees, have long caused problems in resolving the phylogenetic relationships within Apidae based on morphological data because of the tendency for parasites to converge on a suite of traits, making it difficult to differentiate similarity caused by common ancestry from convergence. Here, we resolve the evolutionary history of apid cleptoparasitism by conducting a detailed, comprehensive molecular phylogenetic analysis of all 33 apid tribes (based on 190 species), including representatives from every hypothesized origin of cleptoparasitism. Based on Bayesian ancestral state reconstruction, we show that cleptoparasitism has arisen just four times in Apidae, which is fewer times than previously estimated. Our results indicate that 99% of cleptoparasitic apid bees form a monophyletic group. Divergence time estimates reveal that cleptoparasitism is an ancient behavior in bees that first evolved in the late Cretaceous 95 Mya [95% highest posterior density (HPD) = 87–103]. Our phylogenetic analysis of the Apidae sheds light on the macroevolution of a bee family that is of evolutionary, ecological, and economic importance.     

From the Cover: Dynamic evolutionary change in post-Paleozoic echinoids and the importance of scale when interpreting changes in rates of evolution

How ecological and morphological diversity accrues over geological time has been much debated by paleobiologists. Evidence from the fossil record suggests that many clades reach maximal diversity early in their evolutionary history, followed by a decline in evolutionary rates as ecological space fills or due to internal constraints. Here, we apply recently developed methods for estimating rates of morphological evolution during the post-Paleozoic history of a major invertebrate clade, the Echinoidea. Contrary to expectation, rates of evolution were lowest during the initial phase of diversification following the Permo-Triassic mass extinction and increased over time. Furthermore, although several subclades show high initial rates and net decreases in rates of evolution, consistent with “early bursts” of morphological diversification, at more inclusive taxonomic levels, these bursts appear as episodic peaks. Peak rates coincided with major shifts in ecological morphology, primarily associated with innovations in feeding strategies. Despite having similar numbers of species in today’s oceans, regular echinoids have accrued far less morphological diversity than irregular echinoids due to lower intrinsic rates of morphological evolution and less morphological innovation, the latter indicative of constrained or bounded evolution. These results indicate that rates of evolution are extremely heterogenous through time and their interpretation depends on the temporal and taxonomic scale of analysis.Assessing how rates of morphological evolution have changed over geological time has been a major research goal of evolutionary paleobiologists since Westoll’s classic study of lungfish evolution (1). A common pattern to emerge from the fossil record is that many clades reach maximal morphological diversity early in their evolutionary history (2–4). This sort of pattern could be the result of an “early burst” of morphological diversification as taxa diverge followed by a slow-down in rates as ecological space becomes filled (5, 6). Internal constraint or long-term selective pressures could also limit overall disparity, leading to a slowdown in the rate of new trait acquisition over time (7, 8). However, only a small proportion of fossil disparity studies have also assessed changes in rates of evolution within lineages (e.g., along phylogenetic branches) thereby providing a more nuanced understanding of how this disparity came about (e.g., refs. 9–13). Simultaneously, decreasing rates in trait evolution have been difficult to detect using phylogenetic comparative data of extant taxa, because of low statistical power (14, 15), loss of signal through extinction (16), and inaccuracies in reconstructing ancestral nodes (17). Here we take advantage of recently developed methods for directly estimating per-lineage-million-year rates of evolution from phylogenies with both fossil and living taxa to test whether declining rates characterize the evolutionary history of a major clade of marine invertebrates, the echinoids.Since originating some 265 million years ago (18, 19), crown group echinoids have evolved to become ecologically and morphologically diverse in today’s oceans, and are an important component of both past and present marine ecosystems (e.g., refs. 20–22). However, analysis of how this diversity arose has either been based on taxonomic counts (e.g., ref. 23) or has adopted a morphometric approach where the requirement of a homologous set of landmarks limits taxonomic, temporal, and geographic scope (e.g., ref. 24). We use a discrete-character-based approach and a recent taxonomically comprehensive analysis of post-Paleozoic echinoids as our phylogenetic framework (25). This tree is almost entirely resolved (SI Appendix, Fig. S1) and branches may be scaled using the first appearance of each taxon in the fossil record (SI Appendix, Table S1). We tabulated the number of character state changes that occurred along each branch within ∼10-million-year time intervals spanning the Permian and post-Paleozoic (SI Appendix, Table S2), and divided this by the summed duration of branch lengths to compute a time series of per-lineage-million-year rates of morphological evolution. We accounted for uncertainty in phylogenetic structure, uncertainty in the timing of the first appearance of taxa, and uncertainty in the timing of character changes along each branch using a randomization approach (12). We also estimated rates within subclades, corroborating our findings by using likelihoods tests to determine whether some branches had higher rates than expected given rates across the entire tree. Finally, we compared rates of evolution through time with the structure of diversification within a character-defined morphospace, and looked for evidence of differences in evolutionary modes among subclades. The pattern that emerges is one of dynamic evolutionary change through time: Both rates and patterns of evolution vary temporally and across subclades, such that the overall pattern depends highly on the temporal and taxonomic scale of the analysis.     

Revising the recent evolutionary history of equids using ancient DNA

The rich fossil record of the family Equidae (Mammalia: Perissodactyla) over the past 55 MY has made it an icon for the patterns and processes of macroevolution. Despite this, many aspects of equid phylogenetic relationships and taxonomy remain unresolved. Recent genetic analyses of extinct equids have revealed unexpected evolutionary patterns and a need for major revisions at the generic, subgeneric, and species levels. To investigate this issue we examine 35 ancient equid specimens from four geographic regions (South America, Europe, Southwest Asia, and South Africa), of which 22 delivered 87–688 bp of reproducible aDNA mitochondrial sequence. Phylogenetic analyses support a major revision of the recent evolutionary history of equids and reveal two new species, a South American hippidion and a descendant of a basal lineage potentially related to Middle Pleistocene equids. Sequences from specimens assigned to the giant extinct Cape zebra, Equus capensis, formed a separate clade within the modern plain zebra species, a phenotypicically plastic group that also included the extinct quagga. In addition, we revise the currently recognized extinction times for two hemione-related equid groups. However, it is apparent that the current dataset cannot solve all of the taxonomic and phylogenetic questions relevant to the evolution of Equus. In light of these findings, we propose a rapid DNA barcoding approach to evaluate the taxonomic status of the many Late Pleistocene fossil Equidae species that have been described from purely morphological analyses.     

Contrasted patterns of hyperdiversification in Mediterranean hotspots

Dating the Tree of Life has now become central to relating patterns of biodiversity to key processes in Earth history such as plate tectonics and climate change. Regions with a Mediterranean climate have long been noted for their exceptional species richness and high endemism. How and when these biota assembled can only be answered with a good understanding of the sequence of divergence times for each of their components. A critical aspect of dating by using molecular sequence divergence is the incorporation of multiple suitable age constraints. Here, we show that only rigorous phylogenetic analysis of fossil taxa can lead to solid calibration and, in turn, stable age estimates, regardless of which of 3 relaxed clock-dating methods is used. We find that Proteaceae, a model plant group for the Mediterranean hotspots of the Southern Hemisphere with a very rich pollen fossil record, diversified under higher rates in the Cape Floristic Region and Southwest Australia than in any other area of their total distribution. Our results highlight key differences between Mediterranean hotspots and indicate that Southwest Australian biota are the most phylogenetically diverse but include numerous lineages with low diversification rates.     

Revisiting the sedimentary record of the rise of diatoms

Diatoms are a major primary producer in the modern oceans and play a critical role in the marine silica cycle. Their rise to dominance is recognized as one of the largest shifts in Cenozoic marine ecosystems, but the timing of this transition is debated. Here, we use a diagenetic model to examine the effect of sedimentation rate and temperature on the burial efficiency of biogenic silica over the past 66 million years (i.e., the Cenozoic). We find that the changing preservation potential of siliceous microfossils during that time would have overprinted the primary signal of diatom and radiolarian abundance. We generate a taphonomic null hypothesis of the diatom fossil record by assuming a constant flux of diatoms to the sea floor and having diagenetic conditions driven by observed shifts in temperature and sedimentation rate. This null hypothesis produces a late Cenozoic (∼5 Ma to 20 Ma) increase in the relative abundance of fossilized diatoms that is comparable to current empirical records. This suggests that the observed increase in diatom abundance in the sedimentary record may be driven by changing preservation potential. A late Cenozoic rise in diatoms has been causally tied to the rise of grasslands and baleen whales and to declining atmospheric CO₂ levels. Here we suggest that the similarity among these records primarily arises from a common driver—the cooling climate system—that drove enhanced diatom preservation as well as the rise of grasslands and whales, rather than a causal link among them.

Diatoms—phytoplankton that construct their shells out of silica—are critical to marine food webs and geochemical cycles. They account for ∼40% of marine primary productivity today (1), but are a relatively recent contributor to ocean ecosystems (2). Diatoms first appear in the fossil record in the Jurassic (3) and become ecologically dominant among phytoplankton during the Cenozoic (4, 5). Hypothesized explanations for their middle to late Cenozoic rise include the decline in atmospheric CO₂ concentrations over the last 40 My, sea level change, an increase in bioavailable silica reaching the ocean due to elevated continental weathering and/or the expansion of grasslands, and changes in nutrient focusing due to cooler temperatures, among others (5–9).The timing and cause of diatoms'' ascension is important beyond simply reconstructing the history of marine primary producers—it represents a major shift in Earth''s silica and carbon cycles. Diatoms are believed to have drawn down ocean silica concentrations to their lowest levels in Earth''s history (10), which, studies suggest, could have fundamentally changed climate regulation by altering marine authigenic clay formation (11, 12). A shift from calcifying to silicifying plankton also partially decouples inorganic and organic carbon and leads to a tighter coupling of organic carbon (along with nitrogen and phosphorous) to silica (3, 13, 14). In addition, the evolution of relatively large, well-protected phytoplankton lineages including diatoms, coccolithophores, and dinoflagellates, and their subsequent rise in ecological significance, is hypothesized to be the bottom-up impetus for massive ocean ecosystem restructuring in the Mesozoic and Cenozoic (15).Recent work (16–18) has called into question the classic timeline of diatoms'' increase in abundance and diversity (Fig. 1A). It has been assumed, based on fossil databases, that diatom diversity and abundance were generally very low at the beginning of the Cenozoic and increased toward the present, with a rapid rise beginning around the middle Miocene (23 Ma to 5 Ma) (8, 19, 20). Diatom abundance has, for the most part, been inferred from diatom diversity (21–23), although there is a similar increase in the relative abundance of diatoms in deep-sea sediments (5). Punctuating this long-term trend, siliceous microfossil (and radiolarian) abundance peaks in the Middle Eocene (5, 24) and is followed by a peak in diatom diversity in the latest Eocene to early Oligocene (10, 20, 21, 25, 26). Prior to the ecological rise of diatoms, radiolarians, a group of heterotrophic to mixotrophic protists, were the dominant pelagic silicifiers. As diatoms expanded, seawater silica concentrations are believed to have declined more than tenfold, leading to range contractions, reduced silicification, and reduced abundance in radiolarians and other silicifiers (11, 22, 23, 27–30). However, paired sponge and radiolarian silicon isotope work suggests roughly constant surface water silica concentrations between the latest Paleocene (60 Ma) and the Oligocene (33 Ma), at levels equivalent to modern surface ocean concentrations (<60 µM) (17) (Fig. 1). The Si isotope proxy builds from the observations that the extent of fractionation in sponges is strongly dependent on ambient dissolved Si concentration, while fractionation in radiolarians is mostly Si concentration independent (17, 31–36). In other words, these Si isotope findings suggest that any diatom-driven drawdown of silica must have occurred prior to the late Paleocene. Consistent with this alternative, Si isotope hypothesis, sponge reefs and hypersilicification in neritic sponges (indicative of high silica concentrations) disappeared in the Cretaceous to lower Paleocene (37). However, changes in Si isotope values in the Southern Ocean suggest yet another chronology, with diatom abundance increasing to near modern levels during the Eocene (10).Open in a separate windowFig. 1.Evidence for changes in the silica cycle over the Cenozoic. (A) Trends in diatom diversity according to two calculations [dotted green line, Barron Diatom Catalogue; solid green line, Neptune Database (96); both as reported in ref. 20] roughly coincide with that of whales (blue line) (97). Similarly, the expansion of terrestrial grassland ecosystems (yellow bar) (98–100) and grazers (red dots, hypsodonty index from ref. 21) coincides with an increase in the relative abundance of diatoms (orange line is 1.5-My running median relative diatom to radiolarian abundances from ref. 5; orange envelope shows interquartile range; both begin at 48 Ma, before which data are too scarce). (B) Other normalized diatom diversity curves show a much earlier peak (and then drop) (21), and δ³⁰Si from radiolarians and sponges indicate consistent ocean [Si] as far back as 61 Ma, suggesting diatoms did not increase their ecological impact since that time (17). Taxon silhouettes are from Phylopic.Here we consider whether secular change in the preservation potential of biogenic silica could reconcile this apparently conflicting evidence on diatoms and the evolution of the modern silica cycle. Two of the main factors determining whether biogenic silica makes it into the rock record are bottom-water temperature and sedimentation rate. Sedimentation rate determines how quickly silica is removed from the (diagenetically active) reactive zone beneath the sediment−water interface, and temperature determines the rates of dissolution in that zone (38). Both have changed through the Cenozoic (39–44), with declining deep-sea temperatures and increasing sedimentation rates correlated to declining atmospheric CO₂ levels, global cooling, and evolving ocean basins (45–49). Here we use a diagenetic model to investigate the effect of secular changes in deep-sea sedimentation rate and porewater temperature over the Cenozoic on opal burial efficiency (i.e., the proportion of opal rain reaching the seafloor that is permanently sequestered), and how this relates to the apparent rise of diatoms over the same interval. We generate a taphonomic null hypothesis for the fossil record of diatom abundance that explicitly assumes that there is no change in the flux of diatoms to the seafloor through the Cenozoic, and thereby quantifies and constrains the potential effect of changing diagenetic conditions on the interpretation of the siliceous microfossil record.     

Araceae from the Early Cretaceous of Portugal: evidence on the emergence of monocotyledons

A new species (Mayoa portugallica genus novum species novum) of highly characteristic inaperturate, striate fossil pollen is described from the Early Cretaceous (Barremian-Aptian) of Torres Vedras in the Western Portuguese Basin. Based on comparison with extant taxa, Mayoa is assigned to the tribe Spathiphylleae (subfamily Monsteroideae) of the extant monocotyledonous family Araceae. Recognition of Araceae in the Early Cretaceous is consistent with the position of this family and other Alismatales as the sister group to all other monocots except Acorus. The early occurrence is also consistent with the position of Spathiphylleae with respect to the bulk of aroid diversity. Mayoa occurs in the earliest fossil floras (from circa 110 to 120 million years ago) that contain angiosperm flowers, carpels, and stamens. The new fossil provides unequivocal evidence of monocots in early angiosperm assemblages that also include a variety of key "magnoliid" lineages (e.g., Chloranthaceae) but only a limited diversity of eudicots.     

Early evolution of the angiosperm clade Asteraceae in the Cretaceous of Antarctica

The Asteraceae (sunflowers and daisies) are the most diverse family of flowering plants. Despite their prominent role in extant terrestrial ecosystems, the early evolutionary history of this family remains poorly understood. Here we report the discovery of a number of fossil pollen grains preserved in dinosaur-bearing deposits from the Late Cretaceous of Antarctica that drastically pushes back the timing of assumed origin of the family. Reliably dated to ∼76–66 Mya, these specimens are about 20 million years older than previously known records for the Asteraceae. Using a phylogenetic approach, we interpreted these fossil specimens as members of an extinct early diverging clade of the family, associated with subfamily Barnadesioideae. Based on a molecular phylogenetic tree calibrated using fossils, including the ones reported here, we estimated that the most recent common ancestor of the family lived at least 80 Mya in Gondwana, well before the thermal and biogeographical isolation of Antarctica. Most of the early diverging lineages of the family originated in a narrow time interval after the K/P boundary, 60–50 Mya, coinciding with a pronounced climatic warming during the Late Paleocene and Early Eocene, and the scene of a dramatic rise in flowering plant diversity. Our age estimates reduce earlier discrepancies between the age of the fossil record and previous molecular estimates for the origin of the family, bearing important implications in the evolution of flowering plants in general.Flowering plants underwent a rapid ecological radiation and taxonomic diversification in the Early Cretaceous, about 121–99 Mya (1). Asterids, in particular, represent an extraordinarily diverse clade of extant angiosperms that includes more than 80,000 species. This clade contains the most species-rich angiosperm family, the Asteraceae, with 23,000 species, many of which are economically important taxa, such as sunflowers, lettuce, and gerberas. The origin and early diversification of family Asteraceae were important events in the history of life largely because this lineage has been a dominant component for the past several millions of years in numerous biomes around the world, primarily in open habitat ecosystems. Particularly, the evolution of Asteraceae, typically characterized by bearing attractive inflorescences (or capitula), may have promoted the radiation of insect pollinators (e.g., solitary bees) that heavily rely on this family to feed and reproduce (2). To date, the oldest fossil confidently assigned to Asteraceae is from the Middle Eocene of Patagonia. It consists of an inflorescence and associated pollen grains assigned to an extinct clade of Asteraceae, phylogenetically placed at a moderately derived position within the phylogenetic tree of the family (3). The discovery of these Eocene specimens indicated that the crucial split between subfamily Barnadesioideae, the earliest diverging branch of the family, and the rest of Asteraceae occurred even earlier, either during the early Paleogene or Late Cretaceous (4, 5). Recent molecular dating analyses support a Late Cretaceous origin for the crown group Asterales (4, 6), whereas the emergence of Asteraceae was estimated to have occurred in the Early Eocene (4).Here we report fossil pollen evidence from exposed Campanian/Maastrichtian sediments from the Antarctic Peninsula (Fig. 1, Fig. S1, and SI Materials and Methods, Fossiliferous Localities) (7) that radically changes our understanding of the early evolution of Asteraceae.Open in a separate windowFig. 1.Map showing distribution of Upper Cretaceous rocks of the Snow Hill Island and López de Bertodano Formations. The studied sections in Brandy Bay–Santa Marta Cove (James Ross Island) and Cape Lamb (Vega Island) are also indicated. Adapted from Olivero (7).Open in a separate windowFig. S1.Stratigraphic sections of the Upper Cretaceous Snow Hill Island and López de Bertodano Formations. (A) Stratigraphic section of the Snow Hill Island Formation at Santa Marta Cove, James Ross Island with the situation of the studied samples and Ammonite Assemblages [Assemblages 8–9, adapted from Olivero (7)]. (B) Stratigraphic section of the Snow Hill Island and López de Bertodano Formations at Cape Lamb, Vega Island with the situation of the studied samples. To highlight the stratigraphic continuity of the samples, the lower 100 m of the section includes the Gamma Member of the Snow Hill Island Formation exposed on Humps Island, which bear the same Ammonite Assemblages 8-2 and 9 (Assemblages 8-2 and 9) recorded in Santa Marta Cove area (see A).     

From the Cover: Evidence for abrupt speciation in a classic case of gradual evolution

In contrast with speciation in terrestrial organisms, marine plankton frequently display gradual morphological change without lineage division (e.g., phyletic gradualism or gradual evolution), which has raised the possibility that a different mode of evolution dominates within pelagic environments. Here, we reexamine a classic case of putative gradual evolution within the Globorotalia plesiotumida–G. tumida lineage of planktonic foraminifera, and find both compelling evidence for the existence of a third cryptic species during the speciation event and the abrupt evolution of the descendant G. tumida. The third morphotype, not recognized in previous analyses, differs in shape and coiling direction from its ancestor, G. plesiotumida. This species dominates the globorotaliid population for 414,000 years just before the appearance of G. tumida. The first population of the descendant, G. tumida, evolves abruptly within a 44,000-year interval. A combination of morphological data and biostratigraphic evidence suggests that G. tumida evolved by cladogenesis. Our findings provide an unexpected twist on one of the best-documented cases of within-lineage phyletic gradualism and, in doing so, revisit the limitations and promise of the study of speciation in the fossil record.     

Organogenesis in deep time: A problem in genomics,development, and paleontology

The fossil record is a unique repository of information on major morphological transitions. Increasingly, developmental, embryological, and functional genomic approaches have also conspired to reveal evolutionary trajectory of phenotypic shifts. Here, we use the vertebrate appendage to demonstrate how these disciplines can mutually reinforce each other to facilitate the generation and testing of hypotheses of morphological evolution. We discuss classical theories on the origins of paired fins, recent data on regulatory modulations of fish fins and tetrapod limbs, and case studies exploring the mechanisms of digit loss in tetrapods. We envision an era of research in which the deep history of morphological evolution can be revealed by integrating fossils of transitional forms with direct experimentation in the laboratory via genome manipulation, thereby shedding light on the relationship between genes, developmental processes, and the evolving phenotype.Paleontologists in recent decades have discovered a host of new taxa that reveal transitional stages in the evolution of birds, whales, mammals, tetrapods, frogs, salamanders, and arthropods (1–9). This pulse of discovery is not an accident, but the result of an elaboration of our ability to identify likely sites for fossil recovery by using increasingly refined phylogenies, stratigraphic maps, and geological records. Likewise, imaging techniques, such as high-energy CT, have opened up old and understudied fossil collections as new vehicles for discovery. With advances in both fieldwork and imaging, the discovery of the phenotypic basis for morphological innovation is at a critical moment in its long history: Novel perspectives on classical questions of anatomical evolution are within our reach.Fossils, when placed in a phylogenetic context, can reveal taxa with novel combinations of characters that could not be predicted by studying extant creatures alone. If we lacked fossil evidence of mammal-like reptiles, for example, then the physiological and morphological similarities of birds and mammals would likely be interpreted as homologies rather than examples of parallel evolution (e.g., the discredited “Haemothermia” clade) (10, 11). In addition to identifying solid taxonomic groupings, these same fossils reveal transitional series in the origin of the mammalian dentition, ear, and cranium (3). Our understanding of numerous other transformations, from the origin of birds to the origin of tetrapods, is seriously limited without the knowledge of extinct stem taxa.A rich fossil record permits us to document robustly supported transformation series in the evolution of an anatomical feature, organ system, or body plan. However, to understand the pattern and process of evolutionary transitions, paleontologists have increasingly turned their attention to development. In recent years, the combination of technologies from developmental biology and abundant genomic resources for a multitude of model and nonmodel organisms has greatly enriched our understanding of the genetic and developmental processes underlying organogenesis. This broad set of tools provides a new framework for testing hypotheses derived from paleontological findings, thereby forming an interdisciplinary research program with comparative genomics as well as genetic manipulation of embryonic development (12–15).Here, we use the evolution and diversification of the vertebrate limb as an exemplar to reveal how discoveries in paleontology can leverage experimental and comparative work in molecular biology, genomics, and embryology. First, we review how fossil analyses of early gnathostomes, coupled with embryological studies, offer the foundation for hypotheses on the origin of paired appendages. Then, we discuss current research on model and nonmodel species that shed light on the origin of digits by comparing gene expression and regulatory mechanisms underlying fin and limb development. Next, we examine recent studies that identify the genetic and developmental basis for digit reduction in tetrapods. Finally, we highlight novel technologies that are enabling biologists to solve century-old evolutionary puzzles with state-of-the-art molecular approaches. The synthesis of modern technology with paleontological findings has been an ongoing topic of interest (16–18). Continued advances in technology now give morphologists an ever-expanding toolkit to test genome function and, ultimately, manipulate genomes in a phylogenetic framework. When these new technologies are coupled with paleontological discovery, new insights into classical questions in evolutionary morphology lie in the offing.     

Hotspots and the conservation of evolutionary history

Species diversity is unevenly distributed across the globe, with terrestrial diversity concentrated in a few restricted biodiversity hotspots. These areas are associated with high losses of primary vegetation and increased human population density, resulting in growing numbers of threatened species. We show that conservation of these hotspots is critical because they harbor even greater amounts of evolutionary history than expected by species numbers alone. We used supertrees for carnivores and primates to estimate that nearly 70% of the total amount of evolutionary history represented in these groups is found in 25 biodiversity hotspots.     

Fossil traces of the bone-eating worm Osedax in early Oligocene whale bones

Osedax is a recently discovered group of siboglinid annelids that consume bones on the seafloor and whose evolutionary origins have been linked with Cretaceous marine reptiles or to the post-Cretaceous rise of whales. Here we present whale bones from early Oligocene bathyal sediments exposed in Washington State, which show traces similar to those made by Osedax today. The geologic age of these trace fossils (∼30 million years) coincides with the first major radiation of whales, consistent with the hypothesis of an evolutionary link between Osedax and its main food source, although older fossils should certainly be studied. Osedax has been destroying bones for most of the evolutionary history of whales and the possible significance of this “Osedax effect” in relation to the quality and quantity of their fossils is only now recognized.     

Distribution history and climatic controls of the Late Miocene Pikermian chronofauna

The Late Miocene development of faunas and environments in western Eurasia is well known, but the climatic and environmental processes that controlled its details are incompletely understood. Here we map the rise and fall of the classic Pikermian fossil mammal chronofauna between 12 and 4.2 Ma, using genus-level faunal similarity between localities. To directly relate land mammal community evolution to environmental change, we use the hypsodonty paleoprecipitation proxy and paleoclimate modeling. The geographic distribution of faunal similarity and paleoprecipitation in successive timeslices shows the development of the open biome that favored the evolution and spread of the open-habitat adapted large mammal lineages. In the climate model run, this corresponds to a decrease in precipitation over its core area south of the Paratethys Sea. The process began in the latest Middle Miocene and climaxed in the medial Late Miocene, about 7–8 million years ago. The geographic range of the Pikermian chronofauna contracted in the latest Miocene, a time of increasing summer drought and regional differentiation of habitats in Eastern Europe and Southwestern Asia. Its demise at the Miocene-Pliocene boundary coincides with an environmental reversal toward increased humidity and forestation, changes inevitably detrimental to open-adapted, wide-ranging large mammals.     

Ardipithecus ramidus and the evolution of the human cranial base

The early Pliocene African hominoid Ardipithecus ramidus was diagnosed as a having a unique phylogenetic relationship with the Australopithecus + Homo clade based on nonhoning canine teeth, a foreshortened cranial base, and postcranial characters related to facultative bipedality. However, pedal and pelvic traits indicating substantial arboreality have raised arguments that this taxon may instead be an example of parallel evolution of human-like traits among apes around the time of the chimpanzee–human split. Here we investigated the basicranial morphology of Ar. ramidus for additional clues to its phylogenetic position with reference to African apes, humans, and Australopithecus. Besides a relatively anterior foramen magnum, humans differ from apes in the lateral shift of the carotid foramina, mediolateral abbreviation of the lateral tympanic, and a shortened, trapezoidal basioccipital element. These traits reflect a relative broadening of the central basicranium, a derived condition associated with changes in tympanic shape and the extent of its contact with the petrous. Ar. ramidus shares with Australopithecus each of these human-like modifications. We used the preserved morphology of ARA-VP 1/500 to estimate the missing basicranial length, drawing on consistent proportional relationships in apes and humans. Ar. ramidus is confirmed to have a relatively short basicranium, as in Australopithecus and Homo. Reorganization of the central cranial base is among the earliest morphological markers of the Ardipithecus + Australopithecus + Homo clade.As the confluence of the neural, locomotor, and masticatory systems, the cranial base has been the site of profound structural change in human evolution. The modern human basicranium differs from that of our closest living relatives, the great apes, in numerous aspects of shape and morphological detail (1–4). In humans, the foramen magnum and occipital condyles are more anteriorly located, the midline basicranial axis is relatively short anteroposteriorly and strongly “flexed” internally, and the bilateral structures marking vascular and neural pathways through the central part of the base are more widely separated. This organization alters the relationships between the petrous and tympanic parts of the temporal bone. These phylogenetically derived features are already seen in the earliest known skulls of Australopithecus, ca. 3.0–3.4 Ma (5, 6).The cranium of Ardipithecus ramidus, an early Pliocene (4.4 Ma) hominoid from Ethiopia, was shown to have a relatively anterior foramen magnum on a short basicranium, corroborating evidence of nonhoning canine teeth and terrestrial bipedality for phylogenetic attribution of this taxon. These sets of derived characters are shared uniquely with the Australopithecus + Homo clade (7–10). At the same time, pelvic and pedal characters indicate that Ar. ramidus also retained considerable arboreal capabilities (11–14). Despite the evidence for a unique phylogenetic relationship with the Australopithecus + Homo clade, it has been argued that Ar. ramidus may be an example of putatively widespread parallel evolution (homoplasy) of human-like traits among great apes around the time of the split between the chimpanzee and human lineages (15–17).We report here results of a metrical and morphological study of the Ar. ramidus basicranium as another test of its hypothesized phylogenetic affinity with Australopithecus and Homo. We analyzed the length and breadth of the external cranial base and the structural relationship between the petrous and tympanic elements of the temporal bone in Ar. ramidus, Australopithecus (including Paranthropus of some authors), and mixed-sex samples of extant African hominoid (Gorilla gorilla, Pan troglodytes, Pan paniscus) and modern human skulls (SI Text, Note 1). The finding of additional shared basicranial modifications would support the hypothesis of phylogenetic affinity and weaken the alternative hypothesis of homoplasy as an explanation for human-like basicranial morphology. The outcome has important implications for understanding the functional-adaptive foundations of basicranial evolution in Australopithecus and Homo.The best-preserved basicranial specimen of Ar. ramidus, ARA-VP 1/500, comprises two nonarticulating temporo-occipital portions spanning the skull’s midline. This preservation permits reconstruction of distances between bilateral landmarks, including the carotid canal and the lateral margins of the tympanic elements (7, 10) (Fig. 1 and SI Text, Note 2). The petrous elements are incomplete but their articulation with the tympanics is preserved. The margin of the foramen magnum includes the anterior midline point (basion), constituting the posterior end of the external basicranial length. The specimen is insufficiently complete to permit direct measurement of external cranial base length, from basion forward to hormion (the posterior midline point of the vomer’s intersection with the basisphenoid). Suwa et al. (10) estimated the position of the foramen ovale to reconstruct the anterior terminus of a relatively short basicranial length in ARA-VP 1/500. Here, we present results of evaluations of cranial base breadths and previously unpublished estimates of cranial base length for ARA-VP 1/500 using a different methodology that allows more comprehensive comparisons between of Ar. ramidus and Australopithecus. All measurements were size-standardized by the external basicranial breadth, the distance spanning the base between the indentations just above the external auditory openings (biauricular breadth), which can be measured on ARA-VP 1/500.Open in a separate windowFig. 1.Basal view of Ar. ramidus cranium ARA-VP 1/500. Dotted line indicates midline. cf, carotid foramen; ba, basion, the midline point on the anterior margin of foramen magnum. At natural size, the distance between the centers of the carotid foramina is 50.3 cm.     

Colloquium paper: extinction as the loss of evolutionary history

Current plant and animal diversity preserves at most 1-2% of the species that have existed over the past 600 million years. But understanding the evolutionary impact of these extinctions requires a variety of metrics. The traditional measurement is loss of taxa (species or a higher category) but in the absence of phylogenetic information it is difficult to distinguish the evolutionary depth of different patterns of extinction: the same species loss can encompass very different losses of evolutionary history. Furthermore, both taxic and phylogenetic measures are poor metrics of morphologic disparity. Other measures of lost diversity include: functional diversity, architectural components, behavioral and social repertoires, and developmental strategies. The canonical five mass extinctions of the Phanerozoic reveals the loss of different, albeit sometimes overlapping, aspects of loss of evolutionary history. The end-Permian mass extinction (252 Ma) reduced all measures of diversity. The same was not true of other episodes, differences that may reflect their duration and structure. The construction of biodiversity reflects similarly uneven contributions to each of these metrics. Unraveling these contributions requires greater attention to feedbacks on biodiversity and the temporal variability in their contribution to evolutionary history. Taxic diversity increases after mass extinctions, but the response by other aspects of evolutionary history is less well studied. Earlier views of postextinction biotic recovery as the refilling of empty ecospace fail to capture the dynamics of this diversity increase.     

Reconstructing the evolutionary history of multiple myeloma

Multiple myeloma is the second most common lymphoproliferative disorder, characterized by aberrant expansion of monoclonal plasma cells. In the last years, thanks to novel next generation sequencing technologies, multiple myeloma has emerged as one of the most complex hematological cancers, shaped over time by the activity of multiple mutational processes and by the acquisition of key driver events. In this review, we describe how whole genome sequencing is emerging as a key technology to decipher this complexity at every stage of myeloma development: precursors, diagnosis and relapsed/refractory. Defining the time windows when driver events are acquired improves our understanding of cancer etiology and paves the way for early diagnosis and ultimately prevention.