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Home , 2021 in paleontology, Comparative biology, Ecomorphology, Late Miocene, Martin Brasier, Paleontology

SPECIAL FEATURE: INTRODUCTION The future of the record: in the 21st century David Jablonskia,1 and Neil H. Shubinb,1 ing the split between sharks and bony fishes, aDepartment of Geophysical Sciences and bDepartment of Organismal and but the fossil record shows that bone was , University of Chicago, Chicago, IL 60637 well below that evolutionary node, and that modern sharks represent a derived statefortheclade,havinglostbonystructures In the two decades, great progress in the fungi, and (5–14). The contributions widely distributed in their ancestors (30, 31). biological sciences has come from the in- of paleontology to the study of the rates and Paleontological data are invaluable for in- corporation of in understanding basic pattern of phenotypic are legion. ferring ancestral character states and the as- mechanisms in fields ranging from At the level, the fossil record has sembly of character complexes, and can now and to and famously shown that the evolutionary re- be used to test hypotheses drawn from de- . This conceptual ex- sponsiveness of local on decadal velopmental or phylogenetic analyses. pansion has been promoted in large part by or centennial timescales usually translates at The discovery and analysis of from theoretical, methodological, and empirical the 1- to 10-million-y timescale into stasis or keyintervalsinthehistoryoflifecaninform advances in two seemingly disparate fields. nondirectional random walks rather than the sequence, pattern, and phylogenetic The first field is , which sustained, directional evolutionary trans- dynamics underlying the origin of major opens powerful new windows on phyloge- formation (15, 16). For higher taxa, the functional and anatomical novelties. Such netic relationships, structure and quantification of form within a multidi- “intermediate forms” in the fossil record can , and developmental mechanisms. mensional morphospace was developed in serve as tests of genetic, developmental, and The second field is paleontology, which paleontology (17) and this rich literature affords a unique, direct, and expanding biomechanical hypotheses based on extant continues to find new ways to explore taxa. Indeed, some of the most fundamental source of information into the , evolutionary diversification, from formal , , and spatial and discoveries of fossil stem taxa have only visualizations of evolutionary convergence happened in recent decades. Among verte- temporal dynamics of past life. The fossil and parallelism (e.g., ref. 18) to direct record is certainly rich in incident and rife brates alone, fossils have illuminated evolu- analyses of the relation between ontogeny tionary pathways leading to the origin of with bizarre players, but an extensive body and phylogeny (19–21). of research now treats the fossil record as a (32), (33), turtles (34), The biological world we see around us snakes (35), (36, 37), (38), biological laboratory for rigorously framing today is a highly pruned version of a rich and and testing hypotheses at the intersection of (23), whales (39, 40), hominids (24), ancient . Consequently, reliance and many other groups. These fossils are paleontology with diverse disciplines across solely on recent taxa in analyses of origins i the full range of timescales encompassed valuable on several counts: ( ) they provide can definitively mislead. The diversity and data on the rate and pattern of character by the and life sciences. This Special disparity of many extant clades, from ele- Feature collects some of the exciting and acquisition, which in turn illuminates the phants (22) to horses (23), and for that factors underlying dramatic transformations important new directions and insights, matter hominins (24), has demonstrably from the beginnings of life on Earth to (e.g., feathers as insulation and display be- declined in the latest . Those clades ii the immediate precursor to the present-day fore flight in birds); ( ) they inform mech- were hardly unique, so that fossil data are biota (Fig. 1). anistic hypotheses on underlying changes essential for a fuller understanding of the Paleontology informs the natural sciences in development, both constraining and in- rates and patterns of phenotypic change by providing unique sources of data on spiring experimental tests of rival scenarios within and among many clades (e.g., refs. important phenotypes and on the spatial and (e.g., developmental hypotheses on the ori- 25 and 26). Of course, some clades are in- temporal dynamics of biological events and gin of the wrist and ankle joints of tetra- accessible or sparsely represented as fossils, iii processes. Accordingly, we organize these pods); and ( ) they place transitions in their but even in such groups, from onychoph- contributions in terms of the important environmental context (e.g., whales on the orans to ants to penguins, fossils alter our phenotypes contained in the fossil record, shoreline of a tropical sea (39) and hominids and the analysis of dynamics of species, picture of the timing and extent of mor- arising with bipedal gaits in woodland set- clades, and communities in both space phological diversification. Formal incorpo- tings (41). Moreover, many major transi- and . ration of sparse fossil morphologies in tions occurred in lacking close phylogeny-based analyses of extant species modern analogs, and so can be understood Phenotypes is a promising interdisciplinary growth area ecologically only by paleontological analysis At its most fundamental level, the fossil re- (e.g., ref. 27). of the peculiar ecosystems of their . cord is a narrative of changes to phenotypes can generate a false signal re- and their functions: the origin, persistence, garding the origin of evolutionary novelties Author contributions: D.J. and N.H.S. wrote the paper. – and demise of biological form (1 4), along when only extant taxa are analyzed (28, 29). The authors declare no conflict of interest. with changes in behavior, physiology, and life For example, phylogenetic analysis of extant 1To whom correspondence may be addressed. Email: djablons@ history of vertebrates, invertebrates, plants, chordates suggests that bone evolved follow- uchicago.edu or [email protected].

4852–4858 | PNAS | April 21, 2015 | vol. 112 | no. 16 www.pnas.org/cgi/doi/10.1073/pnas.1505146112 Downloaded by guest on September 28, 2021 Kidwell much a document of clade failure as suc- INTRODUCTION Goswami et al. cess, and provides a direct observational SPECIAL FEATURE: Jackson & Blois window on a wide range of natural exper- White et al. iments, in and directly preceding S. Huang et al. the present biological moment. D. Huang et al. Atthesametime,anotherkeyfinding Slater from the fossil record is a lack of extinction Pieretti et al. where it might be expected. For example, one Pieretti et al. of the great contributions of fossil data is the Pieretti et al. demonstration that species tend to respond Hunt et al. to climate changes by individualistic range Droser & Gehling shifts, despite the web of positive and nega- Brasier et al. tive interactions seen in every present-day Brasier et al. site. Thus, biotic associations have been dis- banded and assembled during repeated gla- cial cycles without significant extinction or Protero- zoic Cenozoic evident disruption of flow through 3 1 500 50 5 2.5 105 novel (“non-analog”)systems(72).Thead- Ga Ma Ka dition of anthropogenic pressures—not the Geologic time least migration barriers in the form of high- Fig. 1. Distribution through geologic time of the contributions to this Special Feature. Ga, billion (109) y ago; Ka = ways, cultivated land, and cities and sub- thousand (103) y ago; Ma, million (106)yago. urbs—has the potential to overturn such resiliency, and paleontological data on what biotas “want to do” in response to climatic – Examples include the origin of vertebrates, traits, can change over time (e.g., refs. 56 59). and other drivers provide a valuable baseline , mollusks, and This paleontological access to long-term perspective from which to view the likely (among others) in late and evolutionary dynamics allows empirical acceleration of future species movements. seas with the initial establishment evaluation of multilevel evolutionary pro- Larger-scale biotic interchanges, which were of macrofaunal foodwebs (42), the Paleozoic- cesses, and the relative contribution of traits often asymmetric between donor and re- early Mesozoic diversification of major insect at organismic, species, and even clade level in cipient regions in the geologic past as they are clades in a world before flowering plants (43), the waxing and waning of clades through today (73), further allow comparative evalu- and the protracted evolution of oceanic eco- time (2, 7, 60, 61). A major area of ongoing ation of the major determinants and long- systems lacking the mineralized phytoplank- work on this general topic involves the in- term consequences of successful range shifts ton that only became major factors in the tegration of paleontological and molecular of different magnitudes. At least one marine late Mesozoic and Cenozoic (44). phylogenetic data, particularly when one or interchange through an ice-free Arctic Ocean the other is sparse, and many new ap- has already occurred (74), and further anal- Time proaches and results are coming online yses of that event in advance of its likely re- – Rates and timing of taxonomic diversification (e.g., refs. 27 and 62 66). enactment in the near future (75) would within and among lineages can sometimes Regarding extinction, the fossil record re- be valuable. be inferred using data on extant veals that complex, seemingly robust eco- The temporal perspective afforded by the alone, and the vast lit- logical systems can collapse and take millions fossil record has additional applications for erature has detected many linkages between of to recover. It also shows that when predicting change and managing . intrinsic biological traits and diversification major extinction events occur on a global For example, biological baselines used to set rates in phylogenies of extant taxa (reviewed scale, recoveries are far more heterogeneous conservation or restoration targets generally in refs. 45 and 46). However, decomposing than expected: some surviving clades redi- rely on the earliest sustained record-keeping diversification rate into its origination and versify prolifically, whereas others linger at in a target region, but this approach is se- extinction components is crucial for a wide low diversities or slip into extinction long verely limited relative to the trajectory of range of issues, from niche conservatism to after the initial bottleneck (67, 68). Abrupt anthropogenic change at most locations. The – diversity-dependence (47 49). Such data biotic transitions also occur at regional scales, nascent field of conservation is are difficult to retrieve robustly from extant and far more frequently than the attention demonstrating more profound shifts in nat- species because, for example, correlations focused on the Big Five mass of ural systems from prior removal of key between rates and individual or clade-level the geologic past might suggest. The fossil species and disruption of and traits may undermine parameter estimates record associated with, for example, the late biogeochemical cycles by agriculture, fisher- from phylogenies (50, 51), and extinction can Cenozoic aridification of the North American ies, and industrialization (76, 77). In addition mask true evolutionary rates or trends rela- interior (69), the uplift of the Himalayas (70), to -level perspectives, close study tive to those inferred from extant species (e.g., and the uplift of Panama (71) provides op- of the environmental and biogeographic his- refs. 29 and 52–55). The fossil record can get portunities for comparative analyses of the tory of individual species is often feasible. For closer to the mechanistic underpinnings of biotic response to changing temperature, example, the European bison (Bison bonasus) present-day biodiversity by providing direct moisture, and regimes, quanti- has been managed as a forest specialist, but the observations on how and when clades differ fying timescales and among-clade dynamics fossil record suggests that its woodland dis- in origination and extinction rates, and how of diversity loss and recovery, and testing tribution was only recently created by the both variables, and their relation to intrinsic alternative drivers. The fossil record is as loss of its open grassland (78). As in

Jablonski and Shubin PNAS | April 21, 2015 | vol. 112 | no. 16 | 4853 Downloaded by guest on September 28, 2021 all of the topics touched upon here, the far in elucidating the mechanism and signif- problematic Eosphaera repre- exchange of methods, data, and ideas should icance of these patterns. sents a form unknown in modern biotas, be a two-way street, and conservation pa- Analyses that combine phenotypes with likely an extinct in microbial leobiology will benefit by the infusion of temporal dynamics in a spatially explicit multicellularity. molecular methods and the continuing de- context are rare but are likely to increase with Droser and Gehling (101) synthesize data velopment of ecological and evolutionary new methods and datasets. In a pathfinding on the assemblage of multicel- models (48, 79). study, Hellberg et al. (99) showed that pre- lular fossils known as the Ediacarian Biota. sent-day populations of a marine snail di- With a near-global distribution from >40 Space verged significantly in form from its late localities in rocks 575–541 My, these fossils Clades are dynamic not only over time but predecessors, generating a variety offer a picture of early multicellular life about through space. Although spatial variation in of novel shell forms with postglacial range 30 My before the famous Cambrian Explo- sampling can be as large a challenge in the expansion. This exemplary study combined sion. An enigmatic array of forms, the fossil record as it is for many components of phylogeographic analysis with comparative Ediacarian Biota have spawned numerous the modern biota (80), the fossil record of morphometric analyses within a single spe- controversial hypotheses about their rela- even sparsely preserved clades can signifi- cies before and after range expansion. Only tionship to extant clades, and their sig- cantly inform the biogeographic and envi- by coupling analyses of phenotypic diversi- nificance for understanding the rise of ronmental history of lineages and major fication in both space and time will we be multicellular life in general. Droser and groups. The geologically recent presence of in a position to achieve a mechanistic un- Gehling show that the forms, horses, proboscidians, and rhinos in the derstanding of ecological and evolutionary whatever their phylogenetic affinities, present New World (81) and, in the early Cenozoic, changes across scales, from local to global, many attributes of later animal life, including monotremes in (82), ratites in the and hierarchical levels, from mobility, heterotrophy, skeletonization, and Northern Hemisphere (83), hummingbirds through bodies to species and clades (2). participation in complex ecosystems, and so in the Old World (83), mousebirds in North these forms offer an informative comparator America (84), Acropora reef corals in Britain Introduction to the Papers in This to later animal evolution. Moreover, because (85), and the huge (up to 1 m) campaniloid Special Feature the biota includes, in addition to many phy- snails of southwest in California, The papers assembled in this Special Fea- logenetically problematic taxa, early relatives the Caribbean, Africa, and northwest Europe ture, which range in time from the earliest of cnidarians, poriferans, and bilaterians, it (86), are just a sampling that demonstrates vestiges of life in Archean to the sheds light on the roots of the metazoan ra- the pervasive history of biotic expansion and fossil record accumulating from extant spe- diations of the Cambrian and later times. regional extinction that would be difficult or cies communities (Fig. 1), can be roughly Pieretti et al. (102) demonstrate the power impossible to infer from present-day diversity organized as mainly concerned with origins of combining the growing morphological and and distributions. The paleontological data or dynamics. phylogenetic records from the fossil record can now feed into new models for the spatial with novel technologies in development and and temporal dynamics in their respective Origins. Brasier et al. (100) discuss the to provide a richer understanding clades, and the history of biodiversity hot- technical and conceptual advances in the of major evolutionary transitions. With con- spots and coldspots can become much clearer search for the earliest fossil traces of life. tinued discovery of new fossils and fresh (87–90). These data also suggest that mac- have long been reported from perspectives on others, and the expansion of roecological and macroevolutionary analyses the Archean Eon [3.5–2.5 Ga (= billion y)], developmental and genomic analyses beyond of present-day regional biotas may be better but new techniques for imaging and nano- standard model organisms, this multidisci- informed by incorporating geologically recent scale elemental analysis, growing knowl- plinary approach can be applied to many of extinction and origination into the equation edge of present-day prokaryote phylogeny the long-standing questions of anatomical rather than under an equilibrium assumption and diversity, and close attention to the en- evolution. Focusing on the evolution of ver- apriori(48,91–93). vironments and processes of tebrate appendages, Pieretti et al. first present Just as the fossil record has provided rich preservation are pushing this field forward. evidence that the origin of paired, lateral evidence for the highly clumped distribution Brasier et al. discuss refined criteria for sep- appendages in vertebrates involved a re- of originations and extinctions through geo- arating preservational artifacts from fossil- deployment of the developmental program logic time (e.g., refs. 42 and 47), spatially ized prokaryotes, and revisit three classic for a single median fin, initially generating a explicit paleontological data have shown that microbiotas. The authors reject the bio- paired set of pectoral fins and only later evolutionary novelties and major clades genicity of many specimens from the Apex giving rise to the pelvic appendages. The preferentially originate at low latitudes (94, Chert (a controversial assemblage dated at transition from fins to limbs is well-docu- 95), and perhaps certain environments in 3.46 Ga), and document a microbiota from mented in the fossil record, and we can see both marine and terrestrial settings (95–97). the roughly contemporary Strelly Pool that the defining feature of limbs, the wrist, Large-scale diversity trends along latitudinal Sandstone (dated 3.43 Ga), unexpectedly and digits, arose in a of evolutionary and other environmental gradients are thus preserved between sand grains from the steps in an extinct lineage of sarcopterygian shaped not just by in situ origination and earliest known shoreline. These shore de- fishes. The wrist and digits have no clear extinction but also by the export of lineages posits seem unlikely hosts for cellular pres- morphological counterparts in extant fishes, into novel habitats, in violation of the general ervation, and so these finds open a new and the underlying developmental and ge- tendency toward evolutionary niche conser- search window for the early fossil record and netic transitions are obscured in model spe- vatism seen in most clades. This is an espe- expand our ecological picture of early cies of teleost fishes because of genome cially active area for interdisciplinary work: microbial life. High-resolution imaging in duplication and reorganization in that clade. spatially explicit phylogenetic analyses in- one of the classic younger microbiotas, the using gar (which separated from corporating fossil and extant taxa (98) will go Gunflint Chert (1.88 Ga), confirms that the the teleosts before the duplication event)

4854 | www.pnas.org/cgi/doi/10.1073/pnas.1505146112 Jablonski and Shubin Downloaded by guest on September 28, 2021 show that its regulatory enhancers can drive evolutionary modes in the simulated se- early bursts in phenotypic evolution could INTRODUCTION digit development in mice, suggesting that quences are quite similar to those in the real derive not only from an evolutionary slow- SPECIAL FEATURE: the wrist–digit complex and its regulatory data, suggesting that the bounded, often os- down in an increasingly crowded world, but pathways did indeed have homologs in the cillatory, of many physical environ- from constant evolutionary rate within a distal bones of early bony fishes. Changes in mental changes contributes significantly to bounded morphospace. Those bounds might gene regulation can also be traced through the nondirectional dynamic observed in many be set by intrinsic, developmental constraints, diversification of limb design, and analysis of fossil sequences. the presence of phylogenetically unrelated but mammalian digit reduction, a common evo- Goswami et al. (104) explore the ways that ecologically similar competitors, or by cli- lutionary theme, shows that convergence on morphological characters are integrated de- matic and other environmental changes that reduced digit number has occurred by two velopmentally into a unified, functioning continually shift the ecological space that can very different genetic and developmental , and how this integration influences accommodate different dietary groups over mechanisms, giving insight into the remark- and is influenced by evolution. The authors time. Diversity ceilings may exist but are able malleability of limbs. The next argue for the importance of a deep-time moving targets on macroevolutionary time- step in the integration of paleontology and perspective to the analysis of integration, scales, as others have suggested in various developmental biology may well be the ex- modularity, and the origins of morpho- contexts (e.g., refs. 47, 106, and 107). perimental modulation of gene expression to logical variation. Taking advantage of the Regional biotas are shaped by the in- test specific hypotheses on transitional forms large populations preserved in teraction of origination, extinction, and im- and their underlying genetic basis against Late Pleistocene tar pits, Goswami et al. migration, so that present-day diversity and fossil phenotypes close to those transitions. analyze the evolutionary signal of patterns its relation to current environmental factors White et al. (41) show that a priori as- of phenotypic integration in dire wolves can only tell part of the story. S. Huang et al. sumptions about what evolutionary ancestors and saber-toothed cats from different pits (108) use the rich record (2–5My should look like can be misleading in our spanning 27,000 y of evolution at Rancho ago) on the warm, temperate coasts of North understanding of evolution. La Brea. These samples reveal decreas- America to evaluate the dynamics leading up have long assumed that the immediate an- ing levels of phenotypic integration as to the modern distribution of marine bio- cestors of the human clade were - climate changed, indicating that devel- diversity. With marine bivalves as a model like. The discovery of challenges opmental interactions created—or failed , the authors show that overall regional these assumptions on multiple levels. By to damp—increasing phenotypic varia- diversities were shaped by extinction and revealing both unexpected morphological tion in responses to stresses associated subsequent recovery through origination and conditions and ecological , this with environmental change. immigration, with clades (here, taxonomic discovery reveals an informative complexity A long-standing issue in biodiversity dy- families) shared by the two coastlines show- to hypotheses of morphological transforma- namics is the potential operation of negative ing a variety of divergent, convergent, and tion and during the acquisition of feedbacks: Is the rate and level of taxonomic parallel trajectories in species richness. Thus, traits unique to . or phenotypic diversification itself diversity- similar diversities for a given clade in differ- dependent? This question is difficult to re- ent regions today is no guarantee of a shared Dynamics. The empirical analysis of evolu- solve definitively using comparative phylo- history or similar diversification rates, and tionary tempo and mode has been one of the genetic data on extant taxa because extinct differences might be geologically recent great contributions of paleontology. Pheno- species cannot enter into diversity or dis- rather than stemming from deep-seated typic stasis has proven to be far more prev- parity estimates through time. Slater (105) evolutionary differences. S. Huang et al. find alent than expected, and the challenge is now tests for diversity-dependent morphological that the contribution of regional extinction to to rigorously test alternative evolutionary diversification in the dog , , a today’s species-richness patterns can be pre- models for long-term phenotypic evolution group with an excellent fossil record that dicted by the geographic range sizes of spe- and seek explanatory mechanisms for the exhibits three sequential diversifications cies during the Pliocene, a variable difficult to different trajectories exhibited in fossil time- through their 40-My history in North extract from present-day data but likely to series. Hunt et al. (103) fit likelihood models America. Diversification slowdowns are gen- play a role in extinction risk with the onset of to a large compilation of evolutionary studies erally viewed in terms of declining ecological large-amplitude glacial cycles near the Plio- ranging in scope from 5,000 y to >50 My. opportunities as the “ecological barrel” gets Pleistocene transition. Past distributional The authors again find that stasis and filled, and fossil canids can be studied in shifts (i.e., local or regional extinction and random walks best account for temporal terms of dietary diversity based on dentition immigration) are crucial to interpreting patterns, rather than directional change, but and body size. Slater finds support for neither present-day . also show that more complex models—par- an early burst of evolution and subsequent Extinction does more than remove phe- ticularly stasis plus punctuational change, diversity-dependent slowdown, nor for un- notypes and their ecological roles: it erases and shifts from a random walk to stasis— constrained diversification fitting a Brownian evolutionary history (EH). This effect is of tend to be increasingly supported in a motion model. Instead, the North American interest in its own right; for example, the maximum-likelihood framework with in- canids best fit a multipeak Ornstein–Uhlen- marine extinctions that accompanied mid- creasing numbers of samples within a study. beck model, where clades gravitate toward Cenozoic polar cooling were more evenly Stasis is more prevalent in marine than in specific trait values, in this case three different distributed phylogenetically in the Arctic terrestrial settings, and in macroinvertebrates body-mass and -area values, one for than in the Antarctic, so that similar regional and vertebrates than in microfossils. Eval- each of the major dietary categories within extinction intensities removed significantly uating the role of external drivers, Hunt the Canidae. These results can thus be moreEHintheSouthernOceanthaninthe et al. simulate phenotypic sequences using interpreted as a set of replicated diversifi- Arctic (89). However, EH can also be a basis a model in which traits track an empirical cations, occurring in and among three stable, for conservation decisions, with regions or long-term climate curve. The frequencies of bounded adaptive zones. Thus, apparent clades prioritized in part by the amount of

Jablonski and Shubin PNAS | April 21, 2015 | vol. 112 | no. 16 | 4855 Downloaded by guest on September 28, 2021 EH they represent. D. Huang et al. (109) manifestations of ecological and biogeo- means, and argues that the interaction of address for the first time one of the major graphic processes in a world of ceaseless en- climatic with other human stressors, rather conceptual and methodological gaps between vironmental change” (110). Rates of change thanclimatechangealone,iscreatingthe molecular and phylogenetic approaches to have varied greatly over time and among apparently unique dynamics in today’sbiota. origination and extinction, and assess how communities through time the past 20,000 y, Analyses of shifts in abundance, diversity, these contrasting approaches affect estimates and the implications of these strong varia- and function in fossil records of EH and its loss. Molecular phylogenies, tions are only beginning to be explored and document unprecedented biological change which depict the splits created by differenti- appreciated. While highlighting the abundant within the last few centuries relative to the ation of gene pools in extant species, nec- paleoecological support for environmental past 2 My, linked to human expansion and essarily yield bifurcations. Paleontological drivers for community composition, Jackson technological advances. Kidwell calls for an phylogenies, which reflect the phenotypic and Blois emphasize that even the broadest integration of paleontological data on the stasis and nondirectional change that per- spatial patterns are spatial aggregations of dynamics of extant species, communities, and vades the fossil record, often incorporate a local interactions among populations of ecosystems on recent decadal to millennial budding evolutionary topology, with line- competitors, predators, mutualists, and par- timescales, which had once been viewed as ages persisting after new species have split asites. Such interactions govern community outside the paleontologist’s purview, with from ancestral populations or clades. Using outcomes of environmental change, and ecological theory and management of the simulations, D. Huang et al. find that esti- more work is needed that takes into account biological world. mated losses of EH in major extinction interactions—and the traits that mediate events are qualitatively similar when ex- them—in relation to environmental drivers. The Future of the Fossil Record tinctions are random with respect to clade Still unclear, for example, is whether com- The future of the fossil record is as many- , although EH is lost more rapidly with munities can display stability in the func- faceted as the disciplines that it impacts. A increasing extinction intensity in paleonto- tional attributes of their components even wide range of research questions involving logical data than in molecular trees. When as species composition ebbs and flows. In- biological systems can benefit greatly by in- extinction focuses on older lineages, as tegrated study of paleoecological case studies corporating data from the fossil record. Many appears to be happening today, both ap- would test fundamental ecological theory and exciting directions could not be included in proaches capture the disproportionate provide insights for how and where anthro- this Special Feature, from ancient DNA (112, of EH, although the molecular signal pogenically driven activities might be over- 113) to (114–116), to positive is damped relative to the paleontological one. riding past controls on community dynamics. and negative feedbacks among clades (117– Usingaphylogenyoflivingandextinctscallops In our final paper, Kidwell (111) examines 119) and between biological systems and the from California, which have an exceptional the many ways in which very young fossil global environment (5, 42, 120). By bringing fossil record, the authors find a preferential records from the last few decades to millen- together papers at the forefront of the in- loss of young species in the Plio-Pleistocene nia can provide unique insights into the tegration of paleontology with other disci- extinction pulse, although this signal proves current status of extant species, communities, plines,wehopethisSpecialFeaturewillhelp difficult to retrieve from molecular data, and biomes, emphasizing marine and coastal define a future agenda for work at these consistent with simulation results. Nonethe- systems. The fossil record of the Anthro- scientific interfaces. less, the encouraging outcome of this study is pocene—the informal term encompassing Sadly, as this volume went to press we that extinction selectivity measured by these the human domination of a majority of learned of the tragic death of one of our different approaches to EH are broadly natural processes on a global scale—includes contributors, . Martin was an comparable, indicating that the fossil record information from still-unburied organic re- integrative paleobiologist par excellence,who can provide a useful natural laboratory for mainsaswellasshallow-cores,thuslinking made fundamental contributions to many anticipating future losses of EH caused by directly to older fossil records. Such ap- aspects of paleontology, most recently re- anthropogenic extinctions. proaches provide baseline ecological data garding the early evolution of life, from the At a finer scale, ecological communities are otherwise inaccessible by direct observations interpretation of the oldest fossil evidence of also shaped by origination, local extinction, and written records, and permit the roles of living things to the biology of the enigmatic and immigration. Jackson and Blois (110) natural and anthropogenic drivers to be as- . He will be missed. consider how these factors shape terrestrial sessed in situations both outside and within ACKNOWLEDGMENTS. We thank D. Bapst, S. Huang, community composition and how an under- the timeframe of diverse human impacts. S. Kidwell, and G. Slater for valuable reviews of this standing of the incessant change in com- Kidwell notes that virtually all biological introduction; the authors and reviewers of the contribu- munities documented in the systems, even in the most remote areas, today tions to this Special Feature; and John Westlund for as- — — sistance with Fig. 1. Support was provided by the Brinson fossil record the past 2.6 My can inform operate around anthropogenically driven Foundation (N.H.S.) and the National Aeronautics and both ecological theory and the management environmental trends rather than stationary Space Administration (D.J.). and conservation of terrestrial biodiversity. Climate changes can be gradual and di- rectional, but are often punctuated by epi- 1 Erwin DH (2007) Disparity: Morphological pattern and 6 Jablonski D, Hunt G (2006) Larval ecology, geographic range, and developmental context. Palaeontology 50(1):57–73. species survivorship in mollusks: Organismic versus sodic events and by rapid-state transitions, 2 Jablonski D (2007) Scale and hierarchy in . species-level explanations. Am Nat 168(4):556–564. and detailed records show that some Palaeontology 50(1):87–109. 7 Schmidt DN, Lazarus D, Young JR, Kucera M (2006) Biogeography communities accordingly disassemble gradu- 3 Wagner PJ (2010) Paleontological perspectives on morphological and evolution of body size in marine plankton. Earth Sci Rev 78(3): evolution. Evolution Since : The First 150 Years, eds Bell M, 239–266. ally via decline and replacement of dominant et al. (Sinauer, Sunderland, MA), pp 451–478. 8 Carbone C, et al. (2009) Parallels between playbacks and species, whereas others undergo rapid col- 4 Seilacher A, Gishlick AD (2014) Morphodynamics (CRC, Boca Pleistocene tar seeps suggest sociality in an extinct sabretooth cat, lapse and turnover. Similar data for insects Raton, FL). Smilodon. Biol Lett 5(1):81–85. 5 Boyce CK, et al. (2010) Angiosperms helped put the rain in the 9 Raichlen DA, Gordon AD, Harcourt-Smith WE, Foster AD, Haas WR and vertebrates reinforce this perspective, rainforests: The impact of plant physiological evolution on tropical (2010) Laetoli footprints preserve earliest direct evidence of human- that local biological communities are “passing biodiversity. Ann Mo Bot Gard 97(4):527–540. like bipedal biomechanics. PLoS ONE 5(3):e9769.

4856 | www.pnas.org/cgi/doi/10.1073/pnas.1505146112 Jablonski and Shubin Downloaded by guest on September 28, 2021 10 Buatois L, Mángano G (2011) Ichnology: Organism-Substrate 42 Erwin DH, Valentine JW (2013) The 73 Vermeij GJ (2005) Invasion as expectation: A historical fact of life. INTRODUCTION

Interactions in Space and Time (Cambridge Univ Press, Cambridge, UK). (Roberts, Greenwood Village, CO). Species Invasion, eds Sax DF, Stachowicz JS, Gaines SD (Sinauer, SPECIAL FEATURE: 11 Clementz MA (2012) New insight from old bones: Stable isotope 43 Labandeira CC, Currano ED (2013) The fossil record of plant- Sunderland, MA), pp 315–339. analysis of fossil mammals. J Mammal 93(2):368–380. insect dynamics. Annu Rev Earth Sci 41:287–311. 74 Vermeij GJ (1991) Anatomy of an invasion: The trans-Arctic 12 De Baets K, Klug C, Korn D, Landman NH (2012) Early 44 Falkowski P, Knoll AH, eds (2011) Evolution of Primary Producers interchange. Paleobiology 17(3):281–307. evolutionary trends in ammonoid embryonic development. Evolution in the Sea (Elsevier Academic, Burlington, MA). 75 Wang M, Overland JE (2012) A sea ice free summer Arctic within 66(6):1788–1806. 45 Pennell MW, Harmon LJ (2013) An integrative view of 30 years: An update from CMIP5 models. Geophys Res Lett 39(18): 13 Sims HJ (2012) The evolutionary diversification of seed size: Using phylogenetic comparative methods: Connections to L18501. the past to understand the present. Evolution 66(5):1636–1649. , community ecology, and paleobiology. Ann N Y Acad Sci 76 Willis KJ, Birks HJD (2006) What is natural? The need for a long- 14 Kimura Y, et al. (2013) Fossil mice and rats show isotopic 1289:90–105. term perspective in biodiversity conservation. Science 314(5803): evidence of niche partitioning and change in dental ecomorphology 46 Morlon H (2014) Phylogenetic approaches for studying 1261–1265. related to dietary shift in Late of Pakistan. PLoS ONE 8(8): diversification. Ecol Lett 17(4):508–525. 77 Dietl GP, Flessa KW (2011) Conservation paleobiology: Putting e69308. 47 Foote M (2010) The geological history of biodiversity. Evolution the dead to work. Trends Ecol Evol 26(1):30–37. 15 Gould SJ (2002) The Structure of Evolutionary Theory (Harvard Since Darwin: The First 150 Years, eds Bell M, et al. (Sinauer, 78 Kerley GIH, Kowalczyk R, Cromsigt JPGM (2012) Conservation Univ Press, Cambridge, MA). Sunderland, MA), pp 479–510. implications of the refugee and the European bison: 16 Hunt G (2007) The relative importance of directional change, 48 Fritz SA, et al. (2013) Diversity in time and space: Wanted dead King of the forest or refugee in a marginal habitat? Ecography 35(6): random walks, and stasis in the evolution of fossil lineages. Proc Natl and alive. Trends Ecol Evol 28(9):509–516. 519–529. Acad Sci USA 104(47):18404–18408. 49 Rabosky DL (2013) Diversity-dependence, ecological , 79 Lawling AM, Matzke NJ (2014) Conservation paleobiology 17 Foote M (1997) The evolution of morphological diversity. Annu and the role of competition in macroevolution. Annu Rev Ecol Evol needs phylogenetic methods. Ecography 37(11):1109–1122. Rev Ecol Syst 28:129–152. Syst 44:481–502. 80 Valentine JW, et al. (2013) The sampling and estimation of 18 Pearce T (2012) Convergence and parallelism in evolution: A 50 Maddison WP, FitzJohn RG (2015) The unsolved challenge to marine paleodiversity patterns: Implications of a Pliocene model. Neo-Gouldian account. Br J Philos Sci 63(2):429–448. phylogenetic correlation tests for categorical characters. Syst Biol Paleobiology 39(1):1–20. 19 Gerber S, Neige P, Eble GJ (2007) Combining ontogenetic and 64(1):127–136. 81 Tomiya S (2013) Body size and extinction risk in terrestrial evolutionary scales of morphological disparity: a study of early 51 Rabosky DL, Goldberg EE (2015) Model inadequacy and mammals above the species level. Am Nat 182(6):E196–E214. ammonites. Evol Dev 9(5):472–482. mistaken inferences of trait-dependent speciation. Syst Biol 64(2): 82 Pascual R, Goin FJ, Balarino L, Udrizar Sauthier DE (2002) New 20 Bhullar BA, et al. (2012) Birds have paedomorphic 340–355. data on the monotreme Monotrematum sudamericanum, skulls. Nature 487(7406):223–226. 52 Finarelli JA (2007) Mechanisms behind active trends in body size and the of triangulate molars. Acta Palaeontol 21 De Baets K, Klug C, Monnet C (2013) Intraspecific variability evolution of the Canidae (Carnivora: Mammalia). Am Nat 170(6): Pol 47(3):487–492. through ontogeny in early ammonoids. Paleobiology 39(1):75–94. 876–885. 83 Mayr G (2009) Fossil Birds (Springer, Berlin). 22 Shoshani J (1998) Understanding proboscidean evolution: A 53 Liow LH, Quental TB, Marshall CR (2010) When can decreasing 84 Ksepka DT, Clarke JA (2010) New fossil mousebird (Aves: formidable task. Trends Ecol Evol 13(12):480–487. diversification rates be detected with molecular phylogenies and the Coliiformes) with feather preservation provides insight into the 23 MacFadden BJ (1994) Fossil Horses (Cambridge Univ Press, fossil record? Syst Biol 59(6):646–659. ecological diversity of an North American avifauna. Zool J Cambridge, UK). 54 Quental TB, Marshall CR (2010) Diversity dynamics: Molecular Linn Soc 160(4):685–706. 24 Tuttle RH (2014) and (Harvard Univ Press, phylogenies need the fossil record. Trends Ecol Evol 25(8):434–441. 85 Wallace CC, Rosen BR (2006) Diverse staghorn corals (Acropora) Cambridge, MA). 55 Rabosky DL (2010) Extinction rates should not be estimated from in high-latitude Eocene assemblages: Implications for the evolution of 25 Polly PD (2001) Paleontology and the comparative method: molecular phylogenies. Evolution 64(6):1816–1824. modern diversity patterns of reef corals. Proc Biol Sci 273(1589): Ancestral node reconstructions versus observed node values. Am Nat 56 Jablonski D (2008) Species selection: Theory and data. Annu Rev 975–982. 157(6):596–609. Ecol Evol Syst 39:501–524. 86 Squires RL (1993) New reports of the large gastropod Campanile 26 Finarelli JA, Goswami A (2013) Potential pitfalls of reconstructing 57 Crampton JS, et al. (2010) Factors that influence species dura- from the Paleocene and Eocene of the Pacific coast of North deep time evolutionary history with only extant data, a case study tion—Interactions between traits in marine molluscs. Paleobiology America. Veliger 36(4):323–331. using the Canidae (mammalia, carnivora). Evolution 67(12): 36(2):204–223. 87 Renema W, et al. (2008) Hopping hotspots: Global shifts in 3678–3685. 58 Ezard THG, Aze T, Pearson PN, Purvis A (2011) Interplay between marine biodiversity. Science 321(5889):654–657. 27 Slater GJ, Harmon LJ, Alfaro ME (2012) Integrating fossils with changing climate and species’ ecology drives macroevolutionary 88 Kiel S, Nielsen SN (2010) Quaternary origin of the inverse molecular phylogenies improves inference of trait evolution. dynamics. Science 332(6027):349–351. latitudinal diversity gradient among southern Chilean mollusks. Evolution 66(12):3931–3944. 59 Wagner PJ, Estabrook GF (2014) Trait-based diversification shifts 38(10):955–958. 28 Donoghue PCJ, Purnell MA (2005) Genome duplication, reflect differential extinction among fossil taxa. Proc Natl Acad Sci 89 Krug AZ, Jablonski D, Roy K, Beu AG (2010) Differential extinction and vertebrate evolution. Trends Ecol Evol 20(6):312–319. USA 111(46):16419–16424. extinction and the contrasting structure of polar marine . PLoS 29 Ruta M, Wagner PJ, Coates MI (2006) Evolutionary patterns in 60 Simpson C (2010) Species selection and driven mechanisms ONE 5(12):e15362. early tetrapods. I. Rapid initial diversification followed by decrease in jointly generate a large-scale morphological trend in monobathrid 90 Crame JA, et al. (2014) The early origin of the Antarctic marine rates of character change. Proc Biol Sci 273(1598):2107–2111. . Paleobiology 36(3):481–496. and its evolutionary implications. PLoS ONE 9(12):e114743. 30 Coates MI, Sequeira SEK, Sansom IJ, Smith MM (1998) Spines 61 Simpson C (2013) Species selection and the macroevolution of 91 Steadman DW (2006) Extinction and Biogeography of Tropical and tissues of ancient sharks. Nature 396(6713):729–730. coral coloniality and photosymbiosis. Evolution 67(6):1607–1621. Pacific Birds (Univ of Chicago Press, Chicago). 31 Davis SP, Finarelli JA, Coates MI (2012) Acanthodes and shark- 62 Morlon H, Parsons TL, Plotkin JB (2011) Reconciling molecular 92 Duncan RP, Boyer AG, Blackburn TM (2013) Magnitude and like conditions in the last common ancestor of modern phylogenies with the fossil record. Proc Natl Acad Sci USA 108(39): variation of prehistoric extinctions in the Pacific. Proc Natl Acad gnathostomes. Nature 486(7402):247–250. 16327–16332. Sci USA 110(16):6436–6441. 32 Chen J-Y, Huang D-Y, Li C-W (1999) An Early Cambrian craniate- 63 Simpson C, Kiessling W, Mewis H, Baron-Szabo RC, Müller J 93 Smith FA, Boyer AG (2012) Losing time? Incorporating a deeper like chordate. Nature 377(6761):720–722. (2011) Evolutionary diversification of reef corals: A comparison of the temporal perspective into modern ecology. Front Biogeogr 4(1):25–38. 33 Schneider I, Shubin NH (2013) The origin of the limb: molecular and fossil records. Evolution 65(11):3274–3284. 94 Kiessling W, Simpson C, Foote M (2010) Reefs as cradles of From expeditions to enhancers. Trends Genet 29(7):419–426. 64 Ezard THG, Thomas GH, Purvis A (2013) Inclusion of a near- evolution and sources of biodiversity in the . Science 34 Li C, Wu XC, Rieppel O, Wang LT, Zhao LJ (2008) An ancestral complete fossil record reveals speciation-related . 327(5962):196–198. turtle from the Late of southwestern . Nature Methods Ecol Evol 4(8):745–753. 95 Jablonski D (2005) Evolutionary innovations in the fossil record: 456(7221):497–501. 65 Gavryushkina A, Welch D, Stadler T, Drummond AJ (2014) The intersection of ecology, development, and macroevolution. J Exp 35 Caldwell MW, Nydam RL, Palci A, Apesteguía S (2015) The oldest Bayesian inference of sampled ancestor trees for and Zoolog B Mol Dev Evol 304(6):504–519. known snakes from the -Lower Cretaceous provide fossil calibration. PLOS Comput Biol 10(12):e1003919. 96 DiMichele WA, Pfefferkorn HW, Gastaldo RA (2001) Response of insights on snake evolution. Nature Comm 6:5996. 66 Heath TA, Huelsenbeck JP, Stadler T (2014) The fossilized birth- Late and Early plant communities to climate 36 Luo ZX (2007) Transformation and diversification in early death process for coherent calibration of divergence-time estimates. change. Annu Rev Earth Planet Sci 29:461–487. mammal evolution. Nature 450(7172):1011–1019. Proc Natl Acad Sci USA 111(29):E2957–E2966. 97 Hopkins MJ (2014) The environmental structure of 37 Meng QJ, et al. (2015) Mammalian evolution. An arboreal 67 Jablonski D (2002) Survival without recovery after mass morphological disparity. Paleobiology 40(3):352–373. docodont from the Jurassic and mammaliaform ecological extinctions. Proc Natl Acad Sci USA 99(12):8139–8144. 98 Wood HM, Matzke NJ, Gillespie RG, Griswold CE (2013) Treating diversification. Science 347(6223):764–768. 68 Friedman LC, Sallan LC (2012) Five hundred million years of fossils as terminal taxa in divergence time estimation reveals ancient 38 Brusatte SL, Lloyd GT, Wang SC, Norell MA (2014) Gradual extinction and recovery: A Phanerozoic survey of large-scale diversity vicariance patterns in the palpimanoid spiders. Syst Biol 62(2): assembly of avian culminated in rapid rates of evolution patterns in fishes. Palaeontology 55(4):707–742. 264–284. across the dinosaur-bird transition. Curr Biol 24(20):2386–2392. 69 Badgley C, Finarelli JA (2013) Diversity dynamics of mammals 99 Hellberg ME, Balch DP, Roy K (2001) Climate-driven range 39 Thewissen JGM, Williams EM (2002) The early of in relation to tectonic and climatic history: Comparison of three expansion and morphological evolution in a marine gastropod. Cetacea (Mammalia): Evolutionary pattern and developmental records from . Paleobiology 39(3):373–399. Science 292(5522):1707–1710. correlations. Annu Rev Ecol Syst 33:73–90. 70 Badgley C, et al. (2008) Ecological changes in Miocene 100 Brasier MD, Antcliffe J, Saunders M, Wacey D (2015) Changing 40 Deméré TA, McGowen MR, Berta A, Gatesy J (2008) mammalian record show impact of prolonged climatic forcing. the picture of Earth’s earliest fossils (3.5–1.9 Ga) with new Morphological and molecular evidence for a stepwise evolutionary Proc Natl Acad Sci USA 105(34):12145–12149. approaches and new discoveries. Proc Natl Acad Sci USA transition from teeth to baleen in mysticete whales. Syst Biol 57(1): 71 O’Dea A, et al. (2007) Environmental change preceded 112:4859–4864. 15–37. Caribbean extinction by 2 million years. Proc Natl Acad Sci USA 101 Droser ML, Gehling JG (2015) The advent of animals: The 41 White TD, Lovejoy CO, Asfaw B, Carlson JP, Suwa G (2015) 104(13):5501–5506. view from the Ediacaran. Proc Natl Acad Sci USA 112:4865–4870. Neither chimpanzee nor human, Ardipithecus reveals the 72 Williams JW, Jackson ST (2007) Novel climates, no-analog 102 Pieretti J, et al. (2015) Organogenesis in deep time: A problem surprising ancestry of both. Proc Natl Acad Sci USA 112: communities, and ecological surprises. Front Ecol Environ 5(9): in genomics, development, and paleontology. Proc Natl Acad Sci 4877–4884. 475–482. USA 112:4871–4876.

Jablonski and Shubin PNAS | April 21, 2015 | vol. 112 | no. 16 | 4857 Downloaded by guest on September 28, 2021 103 Hunt G, Hopkins MJ, Lidgard S (2015) Simple versus complex 109 Huang D, Goldberg EE, Roy K (2015) Fossils, phylogenies, and 115 Cunningham JA, Rahman IA, Lautenschlager S, Rayfield EJ, models of trait evolution and stasis as a response to environmental the challenge of preserving evolutionary history in the face of Donoghue PC (2014) A virtual world of paleontology. Trends Ecol change. Proc Natl Acad Sci USA 112:4885–4890. anthropogenic extinctions. Proc Natl Acad Sci USA 112:4909–4914. Evol 29(6):347–357. 104 Goswami A, Binder WJ, Meachen J, O’Keefe FR (2015) The 110 Jackson ST, Blois JL (2015) Community ecology in a changing 116 Bright JA (2014) A review of paleontological finite element fossil record of phenotypic integration and modularity: A deep-time environment: Perspectives from the Quaternary. Proc Natl Acad Sci models and their validity. J Paleontol 88(4):760–769. perspective on developmental and evolutionary dynamics. Proc Natl USA 112:4915–4921. 117 Erwin DH (2008) Macroevolution of ecosystem Acad Sci USA 112:4891–4896. 111 Kidwell SM (2015) Biology in the Anthropocene: Challenges engineering, niche construction and diversity. Trends Ecol Evol 105 Slater GJ (2015) Iterative adaptive radiations of fossil canids and insights from young fossil records. Proc Natl Acad Sci USA 23(6):304–310. show no evidence for diversity-dependent trait evolution. Proc Natl 112:4922–4929. 118 Jablonski D (2008) Biotic interactions and macroevolution: Acad Sci USA 112:4897–4902. 112 Orlando L, Cooper A (2014) Using ancient DNA to understand Extensions and mismatches across scales and levels. Evolution 62(4): 106 Valentine JW, Jablonski D, Krug AZ, Roy K (2008) Incumbency, evolutionary and ecological processes. Annu Rev Ecol Evol Syst 715–739. diversity, and latitudinal gradients. Paleobiology 34(2):169–178. 45:573–598. 119 Klompmaker AA, Schweitzer CE, Feldmann RM, 107 Erwin DH (2012) Novelties that change carrying capacity. JExp 113 Shapiro B, Hofreiter M (2014) A paleogenomic perspective on Kowalewski M (2013) The influence of reefs on the rise of Zoolog B Mol Dev Evol 318(6):460–465. evolution and gene function: New insights from ancient DNA. Mesozoic marine crustaceans. Geology 41(11):1179–1182. 108 Huang S, Roy K, Valentine JW, Jablonski D (2015) Convergence, Science 343(6169):1236573. 120 Pagani M, Caldeira K, Berner R, Beerling DJ (2009) The role of

divergence, and parallelism in marine biodiversity trends: Integrating 114 Niklas KJ (2013) Biophysical and size-dependent perspectives terrestrial plants in limiting atmospheric CO(2) decline over the past 24 present-day and fossil data. Proc Natl Acad Sci USA 112:4903–4908. on plant evolution. J Exp Bot 64(15):4817–4827. million years. Nature 460(7251):85–88.

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